18 Colibacillosis
H. John Barnes, Jean-Pierre Vaillancourt, and W. B. Gross
INTRODUCTION
Definitions and Synonyms
Colibacillosis refers to any localized or systemic infection
caused entirely or partly by avian pathogenic Escherichia
coli (APEC), including colisepticemia, coligranuloma
(Hjarre’s disease), air sac disease (chronic respiratory dis-
ease, CRD), coliform cellulitis (inflammatory process),
swollen-head syndrome, coliform peritonitis, coliform
salpingitis, coliform osteomyelitis/synovitis (turkey
osteomyelitis complex), coliform panophthalmitis, and
coliform omphalitis/yolk sac infection. Lesions alone
should not be used to infer an E. coli infection without the
descriptor “coliform” being added, because other oppor-
tunistic bacteria can behave similarly to E. coli in sec-
ondary infections. Colibacillosis in mammals is most
often a primary enteric disease; whereas colibacillosis in
poultry is typically a localized or systemic disease occur-
ring secondarily when host defenses have been impaired
or overwhelmed by virulent E. coli strains (13).
For reviews on colibacillosis in poultry see references
14, 56, and 98.
Economic Significance
Collectively, infections caused by E. coli are responsible
for significant economic losses to the poultry industry.
Colibacillosis is the most frequently reported disease in
surveys of poultry diseases or condemnations at process-
ing. For example, 43% of broiler carcasses condemned for
disease at processing had lesions consistent with colisep-
ticemia (279).
Public Health Significance
Most APEC isolated from poultry are pathogenic only for
birds and represent a low risk of disease for people or
other animals (34). However, chickens are susceptible to
colonization with E. coli O157:H7, an important Shiga
toxin-producing, enterohemorrhagic pathogen of
humans, and a low occurrence of natural infection has
been found in both chickens and turkeys in different geo-
graphic areas (101, 117, 209). Contamination of chicken
meat with this organism can occur, and a food-borne out-
break of diarrheal disease was associated with contami-
nated turkey meat (15, 60, 90, 238). Clonally related,
Shiga toxin-producing E. coli infected between 6—16% of
urban pigeons. Infection was significantly higher in
young pigeons than older pigeons (17.9% versus 8.2%).
These findings indicate that pigeons represent a natural
reservoir for the organism and that it could potentially
represent a health hazard to people (49, 164, 223). Infec-
tion of cattle with E. coli O157 in Scotland was epidemio-
logically linked to contact with wild geese (244).
Functional receptors for heat-stable enterotoxin occur
throughout the avian intestinal tract (136). However,
serotypes associated with diarrheal disease in humans and
strains that produce both heat-labile and heat-stable
enterotoxins have been isolated infrequently from chick-
ens (3, 23).
Characteristics of virulent E. coli in birds and other
animals often are shared, and avian strains potentially
can be a source of genes and plasmids that encode for
antimicrobial resistance and virulence factors (41, 140).
Antibiotic resistance of fecal E. coli was greater in broilers
and turkeys that received antibiotics relatively frequently
compared to layers that had little exposure to antibiotics.
Similar antibiotic resistance patterns were present in E.
coli isolated from people who worked with these birds,
and, in some instances, specific strains were shared
among the birds and workers. These findings indicate that
transmission of resistant organisms or plasmids from
poultry to people is common (254).
HISTORY
Mortality of fowls and isolation of a bacterium from
heart, liver, and spleen that was consistent with E. coli was
first reported by Lignieres in 1894 (200). Following experi-
mental inoculation, the isolate was virulent for pigeons,
variably virulent for chickens depending on dose and
route of administration, and not virulent for guinea pigs
or rabbits. Subsequently, diseases in grouse, pigeons,
swans, turkeys, quail, and additional chicken flocks asso-
ciated with a similar organism were documented between
1894 and 1922 (200).
631
632 SECTION II BACTERIAL DISEASES

The first description of colisepticemia was published in Table 18.1. Diagnostic characteristics of Escherichia coli (14).
1907 based on chickens dying from a cholera-like disease
Gram-negative
while being transported. It was concluded that, “Bacterium
Rod (bacillus) shape
(Escherichia) coli may, under certain conditions, take on Non-sporeforming
the ability to leave the intestines, become virulent, and MacConkey agar () Pink colonies, precipitate
cause a septicemia in hens, especially if their resistance Tergitol-7 agar () Yellow colonies
has been weakened by hunger, thirst, cold, or lack of good EMB agar () Dark colonies, metallic sheen
Motility (v)
ventilation” (200).
Catalase ()
Infectious enteritis characterized by birds “going light” Oxidase ()
(infectious asthenia) and paralysis from which E. coli Nitrates-7 nitrites ()
could be isolated was described in 1923 (200). In 1938, a Gelatin ()
pullorum-like disease caused losses of 15—40% in chicks Hydrogen sulfide ()
Indole ()
less than 10 days of age that came from the same hatch-
Methyl red ()
ery. The chicks had pericarditis, perihepatitis, and white Voges-Proskauer ()
spots on the liver. E. coli was isolated from tissues. Poor Citrate (Simmons) ()
incubation resulting in weak chicks was identified as the Urease ()
reason for their susceptibility to infection (46). KCN medium ()
Lysine decarboxylase ()
Between 1938 and 1965, coligranuloma (Hjarre’s dis-
Ornithine decarboxylase (v)
ease) and the role of E. coli in a variety of lesions including Phenylalanine deaminase ()
air sac disease, arthritis, plantar abscesses (bumblefoot), Glucose ()
omphalitis, panophthalmitis, peritonitis, and salpingitis Lactose ()
were identified and described. E. coli infections following Mannitol ()
Dulcitol (v)
vaccination or natural virus infections were also docu-
Sucrose (v)
mented (231). Salicin (v)
Adonitol ()
Inositol ()
ETIOLOGY
() growth or reaction occurs.
The etiology of colibacillosis is Escherichia coli. Other () growth or reaction does not occur.
infectious agents and noninfectious factors usually predis- (v) reaction or character is variable among isolates.
pose an animal to infection. A related species, E. fergusonii,
has been isolated from turkeys, but its role as a potential
Growth Requirements
pathogen is unknown (73).
E. coli grows on ordinary nutrient media at temperatures
of 18—44°C or lower. Generation time and number of
Classification organisms during a specific time period are related to tem-
Escherichia is the type genus of the family Enterobacteri-
perature (Table 18.2).
aceae, which is composed of organisms that can grow aer-
obically or anaerobically and use simple carbon and Colony Morphology
nitrogen sources (18, 71). On agar plates incubated for 24 hours at 37°C, colonies
E. coli is the type species of the genus Escherichia. Addi- are low, convex, smooth, and colorless. Colonies are
tional species have been assigned to the genus, but E. coli bright pink and surrounded by a precipitate on Mac-
occurs most commonly and is most important as a Conkey’s agar, have a dark green-black metallic sheen on
pathogen. The genus Escherichia is most closely related to eosin-methylene blue (EMB) agar, and are yellow on tergi-
the genus Shigella.

Name and Synonyms. Escherichia coli initially was Table 18.2. Effect of temperature on generation time and
named Bacterium (Bacillus) coli commune, which was short- numbers of Escherichia coli that could develop within 24 hours in
ened and modified to B. coli before being given its present the absence of limits on growth (nutrition, accumulation of
inhibiting substances, etc.).
name by Castellani and Chalmers in 1919 (71). It is typi-
cal of bacterial species within the family Enterobacteri- Temperature
aceae (14). Diagnostic characteristics of the organism are Generation
(°F) (°C) time (hours) No. of E.coli in 24 hours
presented in Table 18.1.
32 0.4 20 2
40 4.4 6 8
Morphology and Staining 50 10.0 3 128
E. coli is a gram-negative, non-acid-fast, uniform staining, 60 15.6 2 2,048
non-spore-forming bacillus, usually 2—3  0.6 µm. The 70 21.1 1 8,388,608
organism may be variable in size and shape. Most strains 80 26.7 0.75 3,435,973,800
are motile and have peritrichous flagella. In one study 90 32.2 0.50 24,073,749,000,000
100 37.8 0.30 236,118,320,000,000,000,000
(226), 57% of 607 isolates were motile.
 CHAPTER 18 COLIBACILLOSIS
tol-7 agar. They are usually 1—3 mm in diameter with
granular structure and an entire margin. Rough colonies
are larger with irregular margins. In contrast to the fre-
quent occurrence of hemolysis by mammalian pathogenic
E. coli on blood agar, this is not a common characteristic
of avian isolates. E. coli rapidly produces turbidity in broth
cultures.
Biochemical Properties
Acid and gas are produced in glucose, maltose, mannitol,
xylose, glycerol, rhamnose, sorbitol, and arabinose but
not in dextrin, starch, or inositol. Sorbitol MacConkey
agar is useful for distinguishing E. coli O157:H7 from
other E. coli because it does not ferment sorbitol. Most iso-
lates ferment lactose, but negative strains, which must be
differentiated from Salmonella, occasionally are isolated.
Fermentation of adonitol, sucrose, salicin, raffinose, and
dulcitol is variable. E. coli produces indole, a positive
methyl red reaction and reduces nitrate to nitrite. Voges-
Proskauer and oxidase reactions are negative and hydro-
gen sulfide is not produced on Kligler’s iron medium. It
does not grow in the presence of potassium cyanide,
hydrolyze urea (urease negative), liquefy gelatin, or grow
in citrate medium. Biochemical tests can be used to distin-
guish E. coli from other Escherichia species (18) and bacte-
ria in the family Enterobacteriaceae (71). E. coli isolates
from poultry have biochemical properties similar to those
from other sources (143).
Susceptibility to Chemical and Physical Agents
E. coli possesses no unique resistance capabilities and has
a susceptibility pattern to chemical and physical agents
typical of vegetative, gram-negative bacteria. Tempera-
tures between 60—70°C at times of 30 to 2 minutes, respec-
tively, will inactivate a majority of strains. Thorough
precleaning and/or the presence of a germicide enhance
thermal inactivation. The organism survives freezing and
persists for extended periods at cold temperatures. Ther-
mal inactivation in litter to achieve a 90% reduction in
the number of bacteria is dependent on time and temper-
ature ranging from 1—2 days at 37°C to 6—22 weeks at 4°C.
Inactivation in litter is slower in the presence of high
moisture and more rapid when free ammonia is present
(118). Reproduction of most strains is inhibited by a pH of
less than 4.5 or greater than 9, but the organism is not
killed. Organic acids are more effective than inorganic
acids at inhibiting growth. Similarly, a salt concentration
of 8.5% will prevent growth but not inactivate the organ-
ism (16). A stabilized chlorine dioxide product is highly
effective as a water disinfectant (203).
Antigenic Structure
Various serotypes of E. coli are classified according to the
Ewing scheme (71). Knowledge about the antigenic struc-
ture of E. coli and its relationship to other species has been
reviewed (231). Currently, 167 O, 74 K, 53 H, and 17 F
antigens are recognized (149). Rough strains autoaggluti-
nate and cannot be serotyped.
633
O (Somatic) Antigen. The O antigen is the endotoxin
liberated following lysis of smooth cells. It is composed of
a polysaccharide-phospholipid complex with a protein
fraction resistant to boiling. Methods for preparation and
use of O antisera, which agglutinate antigen at high titers
(usually more than 1:2560) when the antigen-antibody
mixture is incubated at 50°C for 24 hours, have been
described (274).
K (Capsular) Antigen. K antigens are polymeric acids
containing 2% reducing sugars that are associated with
virulence, are on the surface of the cell, interfere with O
agglutination, and can be removed by heating for 1 hour
at 100°C. A few strains require heating for 2.5 hours at
121°C. On the basis of heat stability, K antigens are subdi-
vided into L, A, and B forms. Antisera are prepared in rab-
bits by inoculating live organisms intravenously. Tube
agglutination titers are determined by incubating antigen-
antibody mixtures at 37°C for 2 hours and overnight at
4°C. Titers are low (1:100—1:400). Most of these antigens
can be identified by the slide agglutination test using
appropriately diluted serum (274).
H (Flagellar) Antigen. To examine for H antigens, iso-
lates must be grown under conditions that promote
motility. H antigens are not often used in antigenic iden-
tification of E. coli isolates and are not correlated with
pathogenicity. They are proteins that are destroyed by
heating to 100°C. Tube agglutination tests are read after
incubation at 50°C for 2 hours (274).
F (Pilus) Antigen. F antigens are involved in attachment
to cells. They are expressed variably depending on the
environment in which the organism is growing both in
vitro and in vivo. Pili are classified as being mannose sensi-
tive or mannose resistant depending on whether or not
agglutination is inhibited or unaffected respectively when
mannose is present. A variety of tests have been devel-
oped for detecting fimbrial antigens (274).
Strain Classification
Serotypes. Surveys have been made in many parts of the
world to determine serotypes most frequently associated
with diseases caused by E. coli. Variations according to
geographic region occur, but in most studies the common
serotypes have been O1, O2, O35, and O78 (115, 231).
Many other serotypes have been found less frequently,
and some pathogenic isolates do not belong to known
serotypes or are untypeable. A recent study compared the
serotypes of 458 E. coli isolates from chickens with col-
ibacillosis with 167 isolates from healthy chickens. Sixty-
two different O-types were found among the strains that
were typeable. Only 15% of the strains belonged to the
serogroups O1, O2, O35, O36, and O78 that have been
associated previously with avian colibacillosis. Several iso-
lates from diseased birds belonged to 5 serogroups (O18,
O81, O115, O116, O132), which have not previously been
associated with colibacillosis. It was suggested that this
might signal the emergence of new pathogenic serotypes.
634 SECTION II BACTERIAL DISEASES

Although serotypes from diseased birds were significantly Table 18.3. Factors that may correlate with virulence of
different from serotypes from healthy birds, intestinal Escherichia coli for poultry. See also 56.
infection of healthy birds with serotypes isolated from
Factora References
diseased birds still occurred frequently (24).
Multiple virulence factors (6, 23, 89, 128, 129,
Other Characteristics. In addition to serotyping, iso- 134, 161, 191, 202)
lates of E. coli can be further characterized by antibiotic Genetically related clonal groups (39, 157, 191, 264)
Certain O serotypes (24, 43, 115, 231)
resistance, toxigenicity, presence of adhesins including K1 and K80 capsular antigens (32, 266)
piliation, cell attachment, hemagglutination, lysogeny Adonitol fermentation (218)
(phage typing), and occurrence of plasmids. DNA probes Antibiotic resistance (41, 269)
and polymerase chain reactions have been developed to Congo red dye uptake (17, 239)
detect specific genes important in virulence (149, 274). Presence of large plasmids (57, 86, 257, 266, 269)
Colicin production (esp. ColV) (257, 271)
Random amplification of polymorphic DNA (RAPD) is a Presence of siderophores (aerobactin) (32, 128, 141, 257,
rapid, cost-effective procedure for determining clonal 266, 269)
types of E. coli in epidemiologic studies (39, 157). It is less Fimbria (54, 61, 62, 63, 103,
costly and quicker than molecular fingerprinting using 128, 138, 210, 212,
restriction fragment length polymorphism (RFLP) analysis 240, 256, 269, 273,
278)
(157). RAPD analysis of 55 isolates revealed 50 subtypes in Non-fimbrial adhesins (240)
3 clusters. It was not helpful in discriminating pathogenic Motility (269)
and nonpathogenic isolates (39). Sixteen different RAPD Outer membrane proteins (traT, iss) (37, 76, 122, 195, 206)
types were identified in a collection of isolates from dis- Smooth lipopolysaccharide (272)
eased and healthy poultry in Georgia. Differences in the (endotoxin)
Cell adherence (esp. avian cells) (32, 278)
types were discovered but, with the exception of one Complement resistance (37, 194, 196, 257,
RAPD type that occurred only in diseased chickens and 269, 272)
accounted for 23% of the isolates, the differences were not Resistance to phagocytosis or killing (12)
absolute. Also, RAPD types did not correlate with antibi- Hemagglutinins (64, 237)
otic resistance profiles (157). Multilocus enzyme elec- Enterotoxins (STx,VTx,LT,ST) (3, 70)
Cytopathic toxins (84, 201)
trophoresis identified specific genotypes, which Hemolysins (170, 216)
demonstrated that relatively few clonal types are responsi- Invasion of cells and tissues (257)
ble for different forms of colibacillosis in chickens and Persistence in circulation or tissues (12, 55)
turkeys in widespread geographic areas. Virulence varied a
No single factor identifies all virulent strains and conflicting
little among isolates within a clonal group but varied con- correlations between most factors and virulence occasionally
siderably between clonal groups (264). Pulsed-field gel have been found.
electrophoresis permitted fingerprinting of E. coli isolates
from chickens with cellulitis. Specific types of the organ-
ism were found consistently associated with farms and literature that exists is beyond the scope of this chapter,
successive flocks (228, 229). but a summary is provided in Table 18.3. See also refer-
ence 56.
Virulence Factors Other than ability to cause mortality in embryos or
Pathogenic and nonpathogenic isolates of E. coli are simi- chicks (268), no single virulence factor has been identified
lar in biochemical characteristics and drug sensitivities that will distinguish all pathogenic strains from nonpath-
(43, 218). Hemolysins, heat-stable toxins, metabolic activ- ogenic isolates. An embryo lethality test can be used to
ity, motility, R-plasmids, and phage resistance generally test avian E. coli isolates for virulence. Eleven 12-day-old
do not correlate with virulence (114, 115, 227, 257, 270). chicken embryos are inoculated via the allantoic cavity
Colicins (129) and type I fimbriae (128) are often identi- with 100 cfu of the test organism. Two-day mortality is
fied in APEC. Iron-acquiring capabilities also appear to be 610% for nonvirulent strains, 10—29% for intermediate
important (128). strains, and 729% for virulent strains (268). Resistance to
A number of potential virulence factors have been complement (serum resistance), which may be mediated
identified in APEC strains isolated from diseased birds, but by presence of K1 capsular antigen and is related to the iss
their role in causing disease is not completely understood. (increased serum survival) gene (76, 122, 206), correlates
Many are known virulence factors for colibacillosis in well with virulence of most strains (194, 196, 269, 272).
mammals. Characterization of virulence factors in experi- Virulent strains can persist in the intestinal tract longer
mental studies can provide insights into the pathogenesis and in greater numbers than avirulent ones, which may
of colibacillosis (128). Numerous studies have been pub- be related to colicin production (145, 271).
lished based on direct demonstration of the virulence fac- Seventy-four (48%) of 154 E. coli serotypes caused peri-
tor by biological or immunological methods or carditis and mortality in 3-week-old chicks following
identifying the presence of the genes that encode for the inoculation of air sacs and/or death of 13-day-old
virulence attribute. A comprehensive review of the vast embryos following allantoic inoculation (226).
 CHAPTER 18 COLIBACILLOSIS
Toxins. In addition to endotoxin, a structural compo-
nent of the organism’s cell wall, pathogenic E. coli can
elaborate several toxins that are important in disease.
Avian pathogenic E. coli tend to be less toxigenic than
mammalian pathogenic E. coli (23, 161). This difference
may be due to the lack of toxin production or that toxins
produced by avian strains are not detectable with tests for
toxins produced by mammalian strains. The type of toxin
an organism produces defines the type of pathogen (188).
Enterohemorrhagic E. coli (EHEC), typified by O157, pro-
duce Shiga or Shiga-like toxins (Stx), which are also
known as verocytotoxins (VT) because of the effect they
have on Vero cells. These isolates are also referred to as
Shiga-toxin producing E. coli (STEC). Enterotoxigenic E.
coli (ETEC) produce heat stable (ST) and/or heat labile (LT)
enterotoxins, which cause acute diarrhea. LT is closely
related to cholera toxin produced by Vibrio cholerae.
Enteropathogenic (EPEC) and enteroinvasive (EIEC) are
characterized by the absence of specific toxins and either
their ability to bind or invade enterocytes respectively.
Subtypes of toxins have been identified, and there are
other, less-well known toxins including cytotoxins (201,
221) and hemolysins (170, 216).
Adhesins. Another group of virulence factors are
adhesins, which may be fimbrial or nonfimbrial. The role
of fimbria in causing colibacillosis in poultry is unclear.
Fimbria can undergo phase variation depending on the
types present on the organism and tissue being colonized.
F1 fimbria, but not P(F11) fimbria, are expressed during
initial colonizing of tracheal epithelial cells, whereas P
fimbrial are expressed later when the organism is in the
lower respiratory tract or body tissues. Bacteria were
rapidly killed by macrophages when they were expressing
F1 fimbria (210, 212).
A significant nonfimbrial adhesin is intimin produced
by the eae (E.coli attaching and effacing)-gene that is
found in EHEC and EPEC. It permits the bacterial cell to
adhere to the surface of the enterocyte, which causes a
characteristic attaching and effacing lesion. Organisms
producing this type of lesion are known as attaching
effacing E. coli (AEEC).
A novel avian respiratory soluble lectin, distinct from
pulmonary collectins and ficolins, that binds with surface
polysaccharides of pathogenic E. coli (serogroups O2 and
O78) has been discovered in air-sac fluids of turkeys. Its
role, if any, in colibacillosis has yet to be defined (260).
EPIDEMIOLOGY
The various serotypes of E. coli are intestinal inhabitants
of animals including humans and probably infect most
mammals and birds; therefore, they have a cosmopolitan
distribution. E. coli is a common inhabitant in the intesti-
nal tracts of poultry at concentrations up to 106/g. Higher
numbers are found in younger birds, birds without an
established normal flora, and in the lower intestinal tract
(58, 145, 271). Its presence in drinking water is considered
635
indicative of fecal contamination. Among normal chick-
ens, 10—15% of intestinal coliforms belong to potentially
pathogenic serotypes (111). Intestinal strains are not nec-
essarily the same serotype as those from the pericardial
sac of the same bird. Egg transmission of pathogenic E.
coli is common and can be responsible for high chick
mortality. Pathogenic coliforms are more frequent in the
gut of newly hatched chicks than in the eggs from which
they hatched (112), suggesting rapid spread after hatch-
ing. The most important source of egg infection seems to
be fecal contamination of the egg surface with subsequent
penetration of the shell and membranes. Coliform bacte-
ria can be found in litter and fecal matter. Dust in poultry
houses may contain 105—106 E. coli/g. These bacteria per-
sist for long periods, particularly under dry conditions
(110). There was a reduction of 84—97% in 7 days follow-
ing wetting of dust with water. Feed is often contaminated
with pathogenic coliforms, but hot pelleting processes
can destroy these. Rodent droppings frequently contain
pathogenic coliforms. Pathogenic serotypes can also be
introduced into poultry flocks through contaminated well
water (173).
PATHOBIOLOGY
Natural and Experimental Hosts
Most, if not all avian species, are susceptible to colibacillo-
sis. Clinical disease is reported most often in chickens,
turkeys, and ducks. Collectively, the various forms of col-
ibacillosis are considered to be the most common infec-
tious disease of broiler chickens and turkeys. Natural
infections of quail (8, 77, 282), pheasant (243), pigeons
(27, 49, 223), guinea fowl (28, 107), waterfowl (19, 20, 26,
144), ostriches (134, 248, 263), and emus (119, 267) have
been reported.
Susceptibility and severity of infection are greatest in
young birds, including developing embryos (108, 130, 162).
Host Susceptibility Factors. Compared with bacterial
virulence factors, host susceptibility and resistance factors
are probably a greater determinant of colibacillosis occur-
rence (Tables 18.4, 18.5). Normal, healthy birds with
intact defenses are remarkably resistant to naturally
occurring E. coli exposure including virulent strains. Infec-
tion occurs when skin or mucosal barriers are compro-
mised (e.g., unhealed navel, wounds, mucosal damage
from viral, bacterial, or parasitic infections, lack of normal
flora, etc.), the mononuclear-phagocytic system is
impaired (e.g., viral infections, toxins, nutritional defi-
ciencies), there is immunosuppression (e.g., viral infec-
tions, toxins), exposure is overwhelming (e.g.,
environmental contamination, poor ventilation, contam-
inated water), or birds are exposed to abnormal stress (too
little or too much). Effective control of colibacillosis
depends on identifying and eliminating the predisposing
causes of the disease.
Infection with infectious bronchitis virus in chickens
(44, 85, 178, 230), infection with hemorrhagic enteritis
636 SECTION II BACTERIAL DISEASES

Table 18.4. Factors known or suspected to increase host sus- Table 18.5. Factors known or suspected to decrease host sus-
ceptibility to Escherichia coli infections in poultry. See also 14. ceptibility to Escherichia coli infections in poultry. See also 14.

Factor References Factor

Viruses Immunity Nutrition

Adenovirus (Type 1) (51, 52, 119, 218, 258) Passive Protein
Avian pneumovirus (4, 154, 253) Active Vitamin A
Chicken infectious anemia virus (215) Immunostimulants (?) Vitamin D
Duck enteritis virus (low virulent) (225) Phagocyte priming ß-carotene
Hemorrhagic enteritis virus (189, 207, 255) Vitamin C
Infectious bronchitis virus (44, 85, 178, 230) Physiologic Vitamin E
Infectious bursal disease virus (179, 186, 218) Genetics High iron-oral
Infectious laryngotracheitis virus (148, 178) Age—older Selenium
Influenza virus (135, 192, 245) Sex—Female
Marek’s disease virus (78) Moderate stress
Newcastle disease virus (96, 181, 207, 208) Socialization
Reovirus (218) Deoxycorticosterone
Turkey coronavirus (102, 187) Intestinal flora
Bacteria
Bordetella avium (74, 120, 207, 252)
Chlamydia psittaci (?) (120)
Clostridium perfringens (?) (168) system increases resistance to subsequent respiratory E.
Mycoplasma gallisepticum (96, 181) coli infection (249). Resistance to intra-air sac E. coli chal-
M. meleagridis (163, 192, 208, 219) lenge followed primary NDV vaccination with the Roakin
M. synoviae (152, 235)
strain, which could be prevented by giving the chickens
Parasites
Ascaridia (larvae) corticosterone (123). Individual survival likely derives
A. dissimilis (197) from utilization of feed-derived resources for antibacterial
A. galli (205) defense rather than growth (99).
Eimeria brunetti (113, 172)
Eimeria tenella (177)
Cryptosporidium baileyi
Transmission, Carriers, and Vectors
Histomonas meleagridis (31, 234) E. coli is present in the intestinal tracts of most animals
Toxins and shed in the feces, often in high numbers. Direct or
Ammonia (171, 199) indirect contact with other animals or feces can introduce
Cyclophosphamide (50, 68, 176) new strains into the poultry flock. Free-living birds are
Iron-parenteral (30)
Mycotoxins (?)
especially important as they are colonized with strains
Physiologic that are already adapted to avian species. E. coli was iso-
Age—young (130, 162) lated readily from passerine birds, especially European
Stress—minimal or severe (126, 156) starlings (166), and free-living waterfowl, especially mal-
Sex—male (124) lard ducks (72).
Fast-growing strains (280)
Environmental
Trachea, ceca, and oviduct of recovered laying hens
Contaminated water (173) remained persistently colonized for at least 21 weeks after
Dry, dusty conditions (110) either oral or intra-air sac inoculation with pathogenic E.
Feed/water restriction coli. Hens with colonized oviducts continued to lay eggs
Inadequate ventilation of which 2.7% contained the organism. Interestingly, E.
Overcrowding
Poor litter conditions
coli was not isolated from the shell surface, even if the
Temperature extremes oviduct was heavily colonized (7).
Larval and adult darkling beetles (Alphitobius diaperi-
nus) could contribute to E. coli transmission and its spread
virus in turkeys (189, 207, 255), and exposure of avian among poultry houses and farms following consumption
species to ammonia (171, 199) are the most common of infected larvae or beetles or contact with their feces by
reported factors that predispose to colibacillosis. Interac- the birds. Following exposure, larvae and adults were pos-
tions between infectious bronchitis virus and E. coli have itive for E. coli both externally and internally for up to 12
been studied extensively and used to determine virulence days. The organism was shed in their feces for 6—10 days.
of both organisms and efficacy of vaccination programs Chicks became colonized with E. coli after eating infected
(45, 180). larvae or adults, but the number of infected chicks was
Moderate stress increases resistance, possibly as a result higher when the birds ate larvae (158).
of the development of immunity following contact of
organisms with the immune system (145) or as a result of Pathology
developing and exercising defense mechanisms and main- Immediately after E. coli contacts host tissues, there is an
taining them in a state of readiness (97). Similarly, pro- acute inflammatory response. Acute phase proteins pro-
voking mild, nonspecific inflammation of the respiratory duced in the liver and cytokines IL-1, IL-6, and tumor
 CHAPTER 18 COLIBACILLOSIS
necrosis factor increase rapidly following exposure to
endotoxin or E. coli and can serve as nonspecific markers
(38, 185, 275). Vascular permeability increases, and fluid
and protein accumulate in the tissue. Serous membranes
become wet and edematous, and liquid begins to accumu-
late in body cavities. Chemotactic factors attract het-
erophils, which marginate in post-capillary venules and
emigrate into surrounding tissues (153). Between 6 and 12
hours soft, gelatinous exudate becomes grossly visible. Het-
erophils can kill E. coli extracellularly by substances such as
-defensins released as they degranulate and die (106).
After 12 hours, there is a gradual shift in inflammatory
cells from heterophils to macrophages and lymphocytes.
Exudate continues to accumulate and eventually
undergoes caseation to form a firm, dry, yellow, irregular,
cheese-like mass. Microscopically caseous exudate consists
of heterophilic granulomatous exudate containing vari-
able numbers of embedded bacterial colonies. Exudate is
surrounded by a palisade of multinucleated giant cells and
macrophages (40). An extended period of time, depend-
ing on the size of the mass of exudate, will be required for
it to be slowly eroded away by the action of surrounding
phagocytic cells. Epithelial tissue may be restored if dam-
age has not been too severe, but usually there is some
degree of fibrosis, which may be complete (scarring) if tis-
sue destruction has been extensive. Exudate containing
fibrin may undergo organization eventually being con-
verted to scar tissue. Lesions are inversely related to viru-
lence (i.e., severe, acute infections result in less change
compared to milder, subacute, or chronic infections).
Toxins in cell-free culture filtrates, most likely endo-
toxin, produce the same acute inflammatory response as
the living organism (50). Phagocytic cells (macrophages)
located primarily in the spleen and liver remove bacteria
that gain access to the circulation by phagocytosis (12).
Complement and antibodies to O-antigens (endotoxin),
outer-membrane-proteins (siderophores), and fimbria
serve as opsonins to promote phagocytosis and destruc-
tion of the organism (9, 10, 11).
Several localized or systemic types of colibacillosis
have been described in poultry, often based on the tis-
sue(s) affected or disease process (see Table 18.6).
Localized Forms of Colibacillosis
Coliform Omphalitis/Yolk sac Infection. Omphalitis is
an inflammation of the navel (umbilicus). In birds, the
yolk sac usually is involved, too, because of its close
anatomic relationship. Infection follows contamination
of the unhealed navel with virulent strains of E. coli. Fecal
contamination of eggs is considered to be the most
important source of infection. Bacteria may be acquired in
ovo if the hen has oophoritis or salpingitis or via contami-
nation following artificial insemination (109, 162). Yolk
sac infections also can result from translocation of bacte-
ria from the chick’s intestine or from the bloodstream. In
these cases, the navel may not be affected.
It is common to recover low numbers of E. coli from
normal yolk sacs. Between 0.5 and 6% of eggs from nor-
637
Table 18.6. Classification of the different types of pathologi-
cal manifestations of colibacillosis (adapted from reference 13).
Manifestation
Localized Infections
Coliform omphalitis/yolk sac infection
Coliform cellulitis (inflammatory process)
Swollen head syndrome
Diarrheal disease
Venereal colibacillosis (acute vaginitis)
Salpingitis/peritonitis (adult)
Systemic Infections
Colisepticemia
Respiratory-origin (air-sac disease)
Enteric-origin
Neonatal
Layer
Duck
Colisepticemia Sequelae
Meningitis/Encephalitis
Panophthalmitis
Osteomyelitis
Spondylitis
Arthritis/Polyarthritis
Synovitis/Tenosynovitis
Sternal bursitis
Chronic fibrosing pericarditis (?)
Salpingitis (juvenile)
Coligranuloma
mal hens contain E. coli. Experimentally inoculated hens
may shed E. coli in up to 26% of their eggs. Pathogenic
strains accounted for 43 of 245 isolates from dead
embryos (108). E. coli was present in yolk sacs of about
70% of chicks with “mushy chick disease” (108). Other
types of bacteria (Proteus spp., Bacillus spp., enterococci,
etc.)(see “Miscellaneous and Sporadic Bacterial Infections”
in Chapter 24) also can cause omphalitis, although E. coli
is most common.
Some embryos may die before hatching, particularly
late in incubation; others die at or shortly after hatching.
The incidence of birds with omphalitis increases after
hatching and declines after about 6 days with occasional
losses continuing up to 3 weeks. As few as 10 organisms of
serotype O1a:K1:H7 caused 100% mortality in day-old
chicks following yolk sac injection (226). When birds
become infected with low virulent strains, there may be
no embryo or chick mortality, the only manifestation of
infected yolk sacs being retained caseated yolk and
reduced weight gain (93).
Swelling, edema, redness, and possibly small abscesses
characterize acute inflammation of the navel of affected
birds. The abdomen is distended, and blood vessels are
hyperemic (Figure 18.1B). In severe cases, the body wall
and overlying skin undergo lysis and are wet and dirty.
These birds are referred to as mushy chicks or poults.
There may be other nonspecific changes such as dehydra-
tion, visceral gout, emaciation, vent pasting, and/or
enlarged gall bladder. Yolk is increased because it has not
been absorbed, and inflammatory products have been
added. It is abnormal in color, consistency, and smell and
638 SECTION II BACTERIAL DISEASES
may contain visible exudate. Blood vessels of the yolk sac
are often prominent (Figure 18.1A). Chicks or poults liv-
ing more than 4 days may have pericarditis as well as
infected yolks, indicating systemic spread of the organism
from the yolk sac.
The wall of infected yolk sacs is edematous with mild
inflammation. There is an outer connective tissue zone
followed by a layer of inflammatory cells containing het-
erophils and macrophages, a layer of giant cells, a zone of
necrotic heterophils and masses of bacteria, and then the
inner, abnormal yolk contents. A few plasma cells may be
found in some yolk sacs.
Omphalitis and yolk sac infection have been experi-
mentally reproduced in ducks by exposing eggs to E. coli
broth cultures. Dipping eggs at 18 days of incubation
resulted in a higher incidence of infection than dipping at
1 day. Low brooding temperature or fasting after hatching
increases the incidence of infection and mortality (222).
Consequences of yolk sac infections include depriva-
tion of nutrients and maternal antibodies, absorption of
toxins, and spread of E. coli by extension into the body
cavity or systemically to produce colisepticemia. Survivors
usually are stunted and do poorly. Subsequently, the yolk
sac contracts, but an abscess remains for an extended
period. E. coli often persists in the inflamed yolk sac for
weeks or months. Adhesions to intestines or other visceral
organs are common. Rarely, the stalk of the yolk sac will
loop around the intestine and cause strangulation.
Coliform Cellulitis (Inflammatory Process). Cellulitis is
an inflammation of the subcutis that extends beneath
normal skin. Cellulitis is rare in mammals but relatively
common in birds. It may have many causes, but E. coli
infection is most common in chickens. For this reason,
the term cellulitis has been used synonymously with col-
iform cellulitis. However, cellulitis in turkeys is not fre-
quently associated with E. coli infection (33, 88, 198).
Because this form of colibacillosis has emerged as a signif-
icant disease problem in broiler chickens, it is covered
separately below.
Swollen Head Syndrome. Swollen-head syndrome
(SHS) is an acute to subacute cellulitis involving the peri-
orbital and adjacent subcutaneous tissues of the head (Fig.
18.2G). SHS was first described in broilers in South Africa
associated with E. coli and an unidentified coronavirus
infection (167). The disease subsequently has been
described in most intense poultry-producing areas of the
world. The disease also affects turkeys and guinea fowl
(150, 253).
Swelling of the head is caused by inflammatory exu-
date beneath the skin that accumulates in response to
bacteria, usually E. coli, following upper respiratory viral
infections (e.g. avian pneumovirus, infectious bronchitis
virus). Ammonia aggravates the disease (65). The portal of
entry is considered to be the conjunctiva or inflamed
mucous membranes of the sinuses or nasal cavity (184).
Possible infection via the Eustachian tube has also been
suggested (65). A unique cytotoxin that may be involved
in the pathogenesis of swollen head syndrome has been
identified in a high percentage of SHS E. coli isolates (201,
202). Microscopic lesions include fibrinoheterophilic
inflammation and heterophilic granulomas in the air
spaces of the cranial bones, middle ear, and facial skin;
and lymphoplasmacytic conjunctivitis and tracheitis with
formation of germinal centers (127).
Although the pathogenesis of SHS has not been estab-
lished, conjunctival-associated lymphoid tissue inflamed
from virus infection and/or ammonia irritation may serve
as the site through which bacteria gain access to subcuta-
neous tissues. Periorbital inflammation typically is seen
early in the disease, and hyperplastic lymphoid tissue has
been shown to be a site where E. coli penetrates mucosal
surfaces (96). Scarifying the conjunctival mucosa and
instilling a pure culture of E. coli (167), or inoculation of E
coli into submucosal or subcutaneous tissues (183), will
reproduce the disease. Intranasal inoculation of avian
pneumovirus and E. coli failed to reproduce the disease
(183). SHS did not occur when day-old chicks were inocu-
lated supraconjunctivally with mixtures of avian pneu-
movirus and E. coli, but they did develop clinical disease,
which was most severe when the chicks received both
agents (4).
Diarrheal Disease. Primary enteritis in poultry caused
by E. coli has been considered rare, if it occurred at all.
However, enterotoxigenic E. coli (ETEC) that elaborate
toxins capable of causing fluid accumulation in ligated
intestinal loops of chickens have been recovered from
chickens with diarrhea (3, 131). Natural and experimental
infections of chickens, pigeons, and other avian species
with attaching effacing E. coli (AEEC) also have been iden-
tified (13, 82, 241, 258). Infections with infectious bursal
disease virus in chickens and adenovirus infection in the
pigeon were considered possible predisposing factors to
AEEC infection.
Birds infected with AEEC may have diarrhea and be
dehydrated. Intestines are pale and distended with fluid,
especially ceca, which are fluid filled and may contain gas.
Bacteria intimately attach to the surface of enterocytes,
causing effacement of microvilli, pitting, and pedestal for-
mation, which are best seen by electron microscopy (Fig.
18.3). Lesions are most common in the ceca. Organisms
are identified readily in tissue sections using Giemsa stain
or by immunohistochemical methods. In turkey poults,
coinfection with turkey coronavirus results in severe
stunting and very high mortality (102).
Attempts to experimentally define a role for E. coli in
malabsorption syndrome of chickens were not successful
(232, 233). In contrast, specific strains of E. coli have been
associated with poult enteritis mortality syndrome (PEMS)
(68, 69). Turkey astrovirus, an agent involved in PEMS,
impairs macrophage function, which could explain the
enhanced susceptibility of affected poults to secondary
bacterial infections such as colibacillosis (214).
Venereal Colibacillosis (Acute Vaginitis). Venereal col-
ibacillosis is an acute, often fatal, vaginitis that affects
18.1. Colibacillosis. A. Yolk sac infection in a 4-day-old leghorn chick. Yolk sac is distended, hyperemic (note prominent ves-
sels), and filled with abnormal brown, watery contents. B. Omphalitis and yolk sac infection in a group of 3-day-old leghorn
chicks. Navels are inflamed, and yolk sacs are distended with abnormal contents. C. Advanced air sac disease in a 20-day-
broiler chicken. Polyserositis (pericarditis, perihepatitis, peritonitis, and airsacculitis) have occurred as a result of the sys-
temic spread of Escherichia coli. D. Pleuropneumonia and airsacculitis in a broiler chicken caused by E. coli infection. E.
Experimental colibacillosis in a turkey. Extension of inflammation between superficial and deep pectoral muscles from air-
sacculitis involving the interclavicular air sac. Detecting this type of lesion is important during inspection at processing. F.
Microscopic appearance of pneumonia caused by E. coli in a broiler chicken. Exudate fills the lumen of several affected
parabronchi (compare with unaffected parabronchi at the top of the figure). Exudate has expanded some atria. Some atria
have ruptured, permitting the extension of the inflammatory process through the capillary bed into the interstitium. The
process has involved almost all of one lobule with an extension to the adjacent pleural surface. ¥10. G. Pericarditis and green
discoloration of the liver in a turkey that survived the acute septic phase of colibacillosis. Pericardium is thickened, and exu-
date in the pericardial sac is beginning to undergo fibrosis. Green discoloration of the liver can indicate inflammation else-
where in the bird, especially in turkeys. H. Salpingitis in a young bird caused by E. coli. This lesion occurs infrequently but is
often associated with airsacculitis involving the left abdominal air sac. (Figs. A–C courtesy of Dr. Laddie Munger.)
18.2. Colibacillosis. A. Large caseated masses distending the oviduct of this mature laying hen are characteristic of salpingi-
tis caused by Escherichia coli. Salpingitis in the adult female most likely results from an ascending infection from the cloaca.
B. Goose breeder with acute peritonitis. Yolk was demonstrated in the peritoneum, and E. coli was isolated. C. Acute E. coli
septicemia in a turkey. Spleen is enlarged markedly and congested. Note that it is approximately the same size as the proven-
triculus. Liver is also enlarged and congested, and there is evidence of early pericarditis and peritonitis. D. Experimental col-
ibacillosis in a turkey. Liver from a bird that survived the acute septicemic phase has multiple pale foci, which were determined
microscopically to be focal areas of early heterophilic, granulomatous hepatitis. E. Advanced tenosynovitis/arthritis involving
the hock joint and flexor tendons of a lame commercial broiler. E. coli and Staphylococcus spp. were isolated from the lesion.
F. Panophthalmitis affecting the eye of a turkey that survived an earlier episode of colisepticemia. This lesion is uncommon
and affects only one eye. The organism can be isolated from the eye for an extended period after it is no longer present in other
tissues. G. Swollen-head syndrome in a broiler chicken. There is conjunctival inflammation and periorbital swelling due to cel-
lulitis. Evidence of exposure to high ammonia levels and infection with infectious bronchitis virus and E. coli were found in
this flock. H. Avian cellulitis (inflammatory process). Subcutaneous yellow, caseous exudate is present over the abdomen of this
affected bird. (Figs. E and G courtesy of Dr. Laddie Munger.)
 CHAPTER 18 COLIBACILLOSIS 639

A B

18.3. Attaching effacing E. coli bind tightly to the apical surface of enterocytes, destroying the normal brush border.
On light microscopy, the surface epithelium appears irregular, and numerous bacteria can be seen attached to the
affected cells (A). By EM, the organisms characteristically occupy small pits in the cell surface or are on pedestals. The
number of bacteria and extent of brush border effacement can be seen clearly (B). (Courtesy of Dr. H. L. Shivaprasad.)

turkey breeder hens shortly after they are first insemi-
nated. Puncturing the hymen of young turkey hens can
lead to a severe localized E. coli infection characterized by
vaginitis, cloacal and intestinal prolapse, peritonitis, egg
binding, and internal laying. The affected mucosa is
markedly thickened, ulcerated, and covered with a diph-
theritic, caseonecrotic membrane, which causes obstruc-
tion of the lower reproductive tract. The upper oviduct is
grossly and histologically normal. Increased mortality and
culling amounting to as much as 8% of the flock has
occurred. Egg production is below normal, and there is an
increased number of cull eggs due to small size. No other
infectious agents have been identified as contributing to
the disease (83).
Salpingitis/Peritonitis (Adult). Inflammation of the
oviduct caused by E. coli results in decreased egg produc-
tion and sporadic mortality in laying chickens and breed-
ers. It is one of the most common causes of mortality in
laying hens (21) and affects other types of female birds,
especially ducks and geese (20). Salpingitis sometimes is
confused with egg binding. Infection occurs when E. coli
ascends the oviduct from the cloaca. Spread to the
oviduct from an airsacculitis is also possible, but this form
of salpingitis occurs more frequently in young birds as
part of a systemic infection. Heavy egg production and
associated estrogenic activity predispose to salpingitis by
relaxing the sphincter between the vagina and cloaca.
Infection can be reproduced by injecting large (109) num-
bers of bacteria into the reproductive tract. Mucosal infec-
tions with viruses (e.g., infectious bronchitis virus) or
mycoplasmas also may predispose to salpingitis. The
oviduct is distended markedly and thin-walled with single
or multiple masses of caseous exudate in the general form
of the oviduct (Fig. 18.2A). The mass of exudate may
expand to the point that it fills much of the body cavity.
Exudate is laminated and often contains a central egg,
shells, and/or membranes. It is malodorous. Extension
into the body cavity through the compromised oviduct
wall leads to concurrent peritonitis. Peritonitis in the
absence of salpingitis can also occur due to free yolk in
the body cavity. If E. coli is also present because of an
ascending infection, peritonitis may be severe (100) (Fig.
18.2B). Affected birds cannot produce and lay eggs.
Abdominal laying and misovulated ova may accompany
salpingitis and contribute to peritonitis. Microscopically,
the tissue reaction in the oviduct is mild, consisting
largely of multifocal to diffuse heterophil accumulations
subjacent to the epithelium.
Systemic Forms of Colibacillosis
Colisepticemia. The presence of E. coli in the blood
stream characterizes colisepticemia. Virulence of the
organism and efficiency of the host defenses determine
the duration, degree, and outcome of the disease, as well
as the pattern and severity of lesions (210, 211). Stages
through which colisepticemia progresses are acute sep-
ticemia, subacute polyserositis, and chronic granuloma-
tous inflammation (40). Altough lesions are typical of
colisepticemia, other bacteria capable of producing sep-
ticemia also can cause similar changes. Characteristic fea-
tures of colisepticemia at necropsy are tissues that develop
a green discoloration following exposure to air and a char-
acteristic odor, possibly related to indole produced by the
organism. The bursa of Fabricius is often atrophic or
inflammed as a result of colisepticemia. It should not be
interpreted that a small bursa is evidence of a prior
immune suppressing disease such as infectious bursal dis-
ease (59, 175, 182).
Pericarditis is commonly seen in colisepticemia. It usu-
ally is associated with myocarditis and results in marked
changes in the electrocardiogram (94), often before gross
lesions appear. The pericardial sac becomes cloudy, and
the epicardium becomes edematous and covered with a
640 SECTION II BACTERIAL DISEASES
light-colored exudate. Typically, the pericardial sac fills
with fibrinous exudate (Fig. 18.1C). Microscopically, het-
erophils are numerous in the epicardium initially, but in
less than 24 hours, macrophages become more numerous.
Within the myocardium, particularly close to the epi-
cardium, there are accumulations of lymphoid cells, and
by 7—10 days, there are many plasma cells. Subsequently,
exudate in the pericardial sac undergoes organization (Fig.
18.1G), which can eventually result in constrictive peri-
carditis and liver fibrosis due to chronic passive conges-
tion in survivors. Cardiac lesions reduce arterial blood
pressure from a norm of about 150 mmHg to about 40
mmHg just before death.
Several distinct clinical forms of colisepticemia can be
distinguished, depending on how the organism gains
access to the circulation and the age and type of bird.
Respiratory-Origin Colisepticemia. Respiratory-origin
colisepticemia affects both chickens and turkeys and is
the most common type of colisepticemia. E. coli gains
access to the circulation following damage to the respira-
tory mucosa by infectious or noninfectious agents (85,
92). Infectious bronchitis virus (IBV) and Newcastle dis-
ease virus (NDV), including vaccine strains, mycoplasmas,
and ammonia are the most common predisposing agents.
Avian pneumovirus increases susceptibility of turkeys to
the disease (253). Severity of the resulting disease, which
commonly is referred to as air sac disease, chronic respira-
tory disease (CRD), or multicausal respiratory disease
(120), is directly related to the number of agents that are
involved. A diversity of E. coli serotypes can be identified
in a disease outbreak. Those in the tissues are usually dif-
ferent from those in the intestinal tract of the same bird
but can be found in the intestinal tracts of other birds and
the environment.
Susceptibility is increased when only IBV or NDV
infection occurs. Five days after administration of a vac-
cine strain of NDV, clearance of aerosol-administered E.
coli is reduced. Microscopically, the pseudostratified,
columnar epithelium of the trachea is replaced by 3—8 lay-
ers of immature, nonciliated cells (75). Mixed IBV-E. coli
infections are more severe than those caused by either
agent alone (178, 230). Antibodies against E. coli produced
by chickens infected with infectious bursal disease virus
and/or infectious bronchitis had a significant decrease in
the opsonizing ability compared to antibodies produced
by normal chickens. Reduced opsonization of the organ-
ism resulted in decreased macrophage function, which
could contribute to the frequent infection with E. coli that
follows infectious bronchitis virus infection (186).
Mycoplasmal infection increases susceptibility to E.
coli about 12—16 days postinoculation, and susceptibility
persists for at least 30 days. Infection with IBV or NDV in
addition to mycoplasma further decreases resistance to E.
coli, and the period of increased susceptibility begins ear-
lier and persists longer.
Inhaled coliform-contaminated dust has been impli-
cated as one of the most important sources for infecting
air sacs of susceptible birds. Exposure to chicken-house
dust and ammonia results in deciliation of the upper res-
piratory tract of birds (171, 199), permitting inhaled E.
coli to colonize and cause respiratory infection.
Lesions are prominent in respiratory tissues (trachea,
lungs, and air sacs), pericardial sac, and peritoneal cavi-
ties and are typical of the subacute polyserositis stage of
colibacillosis (40, 211) (Figs. 18.1C—F). Infected air sacs
are thickened and often have caseous exudate on the res-
piratory surface. Microscopically, the earliest changes
consist of edema and heterophil infiltration. Mononu-
clear phagocytes frequently are seen 12 hours after inocu-
lation. Later, macrophages become common, with giant
cells along margins of necrotic areas. There is fibroblast
proliferation and an accumulation of vast numbers of
necrotic heterophils in caseous exudate. Lesions of pre-
disposing respiratory disease usually are present and con-
sist of lymphoid follicles, epithelial hyperplasia, and
epithelium-lined air passages that may contain het-
erophils. Pneumonia is more common in turkeys than
chickens, which usually have pleuritis or pleuropneumo-
nia. Extension of the disease process into the oviduct
may occur and cause salpingitis in juvenile birds (Fig.
18.1H).
Lesions of uncomplicated coliform infection can be
reproduced readily by inoculating pathogenic E. coli or
bacteria-free culture filtrates into the air sac (50). Airsac-
culitis occurs within 1.5 hours. Bacteremia and pericardi-
tis develop within 6 hours. In birds that survive, lesions
are well-developed 48 hours postinoculation. Most mor-
tality occurs during the first 5 days. Recovery is usually
rapid if birds survive the initial infection, although a few
with persistent anorexia become emaciated and die.
Enteric-Origin Colisepticemia. Enteric-origin colisep-
ticemia is most common in turkeys. E. coli gains access to
the circulation following damage to the intestinal mucosa
by infectious agents. The most common predisposing
agent is hemorrhagic enteritis virus (189, 207, 255). Usu-
ally only 1 or 2 types of E. coli are involved in the disease
outbreak, and those in the tissues and intestinal tract are
the same.
Lesions are typical of the acute septicemia stage of col-
ibacillosis (40). Affected birds are in good physical condi-
tion and often have full crops containing feed and/or
water, which indicate the acute nature of the infection.
The most characteristic lesions are congestion or green
discoloration of the liver, marked enlargement and con-
gestion of the spleen, and congested muscles (Fig. 18.2C).
Microscopically, the spleen is congested with proteina-
ceous fluid in sinuses and has multifocal necrosis, often
containing intralesional bacteria. Fibrin thrombi are pre-
sent in liver sinusoids and occasionally renal glomeruli. In
some cases, multiple, pale foci in the liver are seen. Micro-
scopically, these are areas of acute necrosis initially, but
with time, they evolve into granulomatous hepatitis in
survivors (Fig. 18.2D). Birds eventually develop lesions
similar to those of respiratory-origin colisepticemia.
 CHAPTER 18 COLIBACILLOSIS
Neonatal Colisepticemia. Chicks are affected within the
first 24—48 hours after hatching. Mortality remains ele-
vated for 2—3 weeks and usually totals 10—20%. Up to 5%
of the flock may be runted and require culling. Unaffected
birds grow normally, and the disease does not appear to
spread. Initial lesions consist of congested lungs, edema-
tous serous membranes, and splenomegaly. Microscopi-
cally, bacteria are numerous in affected tissues and easily
identified. After a few days, the typical pattern of acute,
fibrinoheterophilic polyserositis involving the pericardial
sac, pleura, air sacs, and peritoneum becomes evident.
Lesions are often extensive and severe in birds that sur-
vive into the second week. Occasionally, birds with arthri-
tis and/or osteomyelitis may be found late in the disease.
Most affected birds have yolk sac abscesses suggesting the
navel is the portal of entry. Alternatively, in ovo infection
may be responsible (162).
Acute Septicemia of Layers. Colisepticemia is most
often a disease of young birds, but occasionally outbreaks
of acute E. coli infection resembling fowl typhoid or fowl
cholera occur in mature chickens and turkeys (14, 53,
281). Outbreaks typically are associated with the onset of
egg production but continue as the flock ages and may
spread to affect older flocks on the same farm. Death is
usually sudden, and mortality is generally between 5%
and 10%. Lesions are typical of acute colisepticemia. Iso-
lates have been lactose-negative and belong to serogroups
O85 or O111. Control has been through chlorination of
water or treatment with antibiotics. The disease was
reproduced by intramuscular inoculation and, less fre-
quently, by oro-nasal administration of the O111 isolate.
The pathogenesis of the disease is unknown, but stress
associated with the onset of egg production is believed to
be an important contributing factor (281).
Coliform Septicemia of Ducks. Coliform septicemia of
ducks is characterized by moist, granular to curd-like exu-
date of variable thicknesses causing pericarditis, perihep-
atitis, and airsacculitis. A characteristic odor is often
noted at necropsy. The liver is frequently swollen, dark,
and bile stained, and the spleen is swollen and dark. E. coli
(usually O78) usually can be recovered from any internal
organs (144). Riemerella anatipestifer causes similar lesions,
but it can be identified by appropriate cultural procedures.
Coliform septicemia occurs throughout the growing
season but becomes more frequent in late fall and winter.
All ages of ducklings are susceptible. Distribution of losses
suggests that individual farms, rather than hatcheries, are
the source of infection (144).
Colisepticemia Sequelae
Death is the usual outcome of colisepticemia, but some
birds may completely recover or recover with residual
sequelae. If E. coli is not controlled, it can localize in
poorly protected sites including the brain, eyes, synovial
tissues (joints, tendon sheaths, sternal bursa), and bones.
641
In immature females, salpingitis can occur when there is
involvement of nearby air sacs. Infectious bronchitis virus
infection of the oviduct may also be an important predis-
posing factor in juvenile salpingitis. After E. coli is no
longer present, constrictive pericarditis and liver fibrosis
may result as the exudate in the pericardial sac undergoes
organization (Fig. 18.1G). Residual pulmonary damage
from combined E. coli and infectious bronchitis infection
can lead to ascites (250, 276).
Meningitis. E. coli localization in the brain is uncom-
mon. Meninges are affected (meningitis), but in some
birds, there is also involvement of the brain (encephalitis)
and ventricles (ventriculitis). Meningeal lesions are evi-
dent at necropsy as zones of discoloration adjacent to
major blood vessels. Fibrinoheterophilic to heterophilic
exudate is seen microscopically early in the infection; the
lesion becomes more granulomatous with time.
Panophthalmitis. Like the brain, involvement of the eye
is uncommon. However, if it is infected the resulting
panophthalmitis is severe (91, 174). Typically, there is
hypopyon and/or hyphema, and infection is unilateral
(Fig. 18.2F). The eye is swollen, cloudy to opaque, and
may be hyperemic initially. Later, the eye shrinks as it
undergoes atrophy. Fibrinoheterophilic exudate and
numerous bacterial colonies are present throughout the
eye. Inflammation, especially adjacent to necrotic tissue,
becomes granulomatous with time. Varying degrees of
retinal detachment and atrophy, and lysis of the lens may
also be seen. The organism persists in diseased eyes for
long periods of time.
Osteoarthritis and Synovitis. Localization of E. coli in
bones and synovial tissues is a common sequel to colisep-
ticemia (Fig. 18.2E). Affected birds likely have insufficient
resistance to completely clear the bacteria. A high per-
centage of turkeys develop lesions following treatment
with dexamethasone and intra-air sac inoculation of
small numbers of E. coli (125) (see also “Turkey
Osteomyelitis Complex” in Chapter 24). Intravenous
inoculation to simulate hematogenous spread to bones
and joints can be used, but mortality from the initial sep-
ticemia is often high. Hematogenous spread of E. coli fol-
lowing hemorrhagic enteritis virus infection of turkeys
resulted in synovitis, osteomyelitis, and green liver discol-
oration in turkeys (66). The term osteoarthritis is used
when a joint is inflamed and one or more bones making
up that joint have osteomyelitis. Polyarthritis refers to the
involvement of more than one joint. Bacterial chon-
dronecrosis and osteomyelitis is another name that has
been used (159). For a recent review see reference 159.
Mild to severe lameness and poor growth are seen clini-
cally, and affected birds are more likely to be victims of per-
secution (that is, cannibalism). Often multiple sites are
involved. Bacteria colonize the vascular sprouts that invade
the physis of a growing bone, provoking an inflammatory
response that results in osteomyelitis. Transphyseal blood
642 SECTION II BACTERIAL DISEASES

vessels in birds serve as a conduit for the process to spread

into the joint and surrounding soft tissues. Bones most
often affected are tibiotarsus, femur, thoracolumbar verte-
bra, and humerus. Hock, stifle, hip, and wing joints are sites
where arthritis is most likely to occur.
Lesions that develop in joint spaces of articulating
thoracolumbar vertebrae cause spondylitis (spondylosis),
which results in progressive paresis and paralysis (80) (Fig.
18.4). Tenosynovitis frequently accompanies arthritis. An
infectious sternal bursitis is also common, but it must be
distinguished from traumatic sternal bursitis in which
fluid but not exudate is seen. When inflammatory lesions
involve the shoulder joint or proximal humerus, exten-
sive exudate can accumulate between the superficial and
deep pectoral muscles (Fig. 18.1E). Birds with infectious,
inflammatory lesions in bones or joints have enlarged,
green discolored livers, which are used at processing to
indicate the possible presence of intraosseous lesions (42,
66, 125).

Coligranuloma (Hjarre’s Disease). Coligranuloma of

chickens and turkeys is characterized by multiple granulo-

18.5. Coligranuloma in a market-age turkey. Numer-

ous, nodular lesions are located in gastrointestinal tis-
sues including liver, but they do not involve the spleen. A
mucoid Escherichia coli was isolated.

mas in liver, ceca, duodenum, and mesentery but not in

the spleen (Fig. 18.5). It is an uncommon form of sys-
temic colibacillosis but can cause mortality as high as 75%
when a flock is affected. Serosal lesions resemble leukosis
tumors. Early in the disease, there is confluent coagula-
tion necrosis involving as much as half the liver. Only
scattered heterophils are seen, and at the edge of the
necrotic areas are a few giant cells. Subsequently, typical
heterophilic granulomas are present in the affected tis-
sues. Pyogranulomatous typhlitis and hepatitis, which
may be related to coligranuloma, have been described in
turkeys with cecal cores and ruptured ceca (165).

18.4. Spondylitis involving articulating thoracolumbar
vertebrae of 2 lame turkeys (fixed tissues). Pressure from
the lesion on the spinal cord has caused demyelination
of the ventral tracts. Escherichia coli is a common cause
of this lesion, but other bacteria, which can localize in
bones and synovial tissues, may also be a cause.
DIAGNOSIS
Isolation and Identification of Causative Agent
Diagnosis is based on the isolation and identification of E.
coli from lesions typical of colibacillosis. Care must be
taken to avoid fecal contamination of samples. Isolation
of the organism from visceral organs of birds undergoing
decomposition must be interpreted cautiously as E. coli
 CHAPTER 18 COLIBACILLOSIS
rapidly spreads from the intestinal tract of dead birds.
Bone marrow cultures are easy to obtain and are generally
free of contaminating bacteria. Material should be
streaked on eosin-methylene blue (EMB), MacConkey, or
tergitol-7 agar, as well as noninhibitory media. A pre-
sumptive diagnosis of E. coli infection can be made if
most of the colonies are characteristically dark with a
metallic sheen on EMB agar, bright pink with a precipitate
surrounding colonies on MacConkey agar, or yellow on
tergitol-7 agar. Strains of E. coli can be slow or nonlactose
fermenters and appear as nonlactose-fermenting colonies.
Definitive identification of E. coli is based on the organ-
ism’s characteristics (see “Etiology”). A flow chart for the
isolation and identification of E. coli has been published
(143).
Antigenic identification, determination of virulence
factors, or fingerprinting of the isolate might be helpful,
particularly when done as part of an epidemiologic inves-
tigation. The correlation between virulence and comple-
ment resistance suggests that this may be a good method
for screening isolates for possible disease association. A
relatively simple rapid turbidimetric assay has been
described (204).
Survival after challenge correlated better with anti-
body titers detected by an enzyme-linked immunosorbent
assay (ELISA) than by the standard indirect hemagglutina-
tion procedure (147).
Procedures to detect acute phase proteins (38, 185,
275) or shifts in the heterophil/lymphocyte ratio (95) can
serve as nonspecific markers of the inflammation and
stress that accompany colibacillosis.
Differential Diagnosis
Many other organisms including viruses, mycoplasmas,
and other bacteria can cause synovial lesions similar to
those resulting from E. coli infection. A great variety of
organisms such as Aerobacter spp., Klebsiella spp., Proteus
spp., salmonellae, Bacillus spp., staphylococci, entero-
cocci, or clostridia frequently are isolated (often as mixed
cultures) from yolk sacs of embryos and chicks (108). Peri-
carditis can also be caused by chlamydia. Pasteurellae or
streptococci sometimes cause peritonitis, and other bacte-
ria, mycoplasmas, and chlamydia can cause airsacculitis.
Acute septicemic diseases may result from pasteurellae,
salmonellae, streptococci, and other organisms. Liver
granulomas have many causes, including anaerobic bacte-
ria belonging to the genera Eubacterium and Bacteroides.
PREVENTION, CONTROL, AND TREATMENT
Management Procedures
The most important source for the transmission of patho-
genic E. coli between flocks is fecal contamination of
hatching eggs. Collecting eggs frequently, keeping nest
material clean, not using floor eggs, discarding cracked
eggs or those with obvious fecal contamination, and
fumigating or disinfecting eggs within 2 hours after they
are laid can reduce transmission. If infected eggs are bro-
643
ken during incubation or hatching, the contents are a
serious source of infection to others, especially when per-
sonnel and egg-handling equipment are contaminated.
Eggs are particularly susceptible just before hatching.
Methods for preventing incubator and hatcher dissemina-
tion are unknown. However, venting incubators and
hatchers to the outside and having as few breeder flocks as
possible represented in each unit will help reduce losses.
Contaminated chicks survive better if kept warm and not
starved.
High protein diets, increased selenium (142), and
increased vitamins A and E (193, 246, 247) apparently
favor survival. However, high levels of vitamin E can be
detrimental to the resistance to coliform cellulitis, col-
ibacillosis, and antibody production (79, 151, 224).
Response to vitamin E is likely interrelated with the geno-
type of the bird (277). Feeding can have an impact on the
severity of colibacillosis. Chickens provided feed on alter-
nate days were more resistant to E. coli challenge than
full-fed chickens (25, 213).
There are no known methods for reducing the level of
pathogenic E. coli in the intestinal tract and feces,
although consideration that 1) pelleted feed has fewer E.
coli than mash, 2) rodent droppings are a source of patho-
genic E. coli, and 3) contaminated water can contain high
numbers of the organism should not be overlooked. Chlo-
rination of drinking water and the use of closed (nipple)
watering systems have decreased the occurrence of col-
ibacillosis and condemnations for airsacculitis (29, 53,
203). Pathogenic strains of E. coli can be excluded compet-
itively from the intestines of chicks by seeding them with
native microflora from resistant chickens (261), commer-
cial competitive exclusion products (105, 121), or Bacillus
subtilis spores (139). A similar effect was achieved follow-
ing in ovo inoculation of Lactobacillus reuteri (67). Infection
with M. gallisepticum and/or infectious bronchitis virus
overcame the protective effect of native flora colonization
(262). Similarly, food and water deprivation increased the
occurrence of spontaneous bacteremia (146).
E. coli infection of the respiratory tract of birds can be
reduced by raising Mycoplasma-free birds and reducing the
exposure of birds to viruses causing respiratory diseases.
Proper ventilation will reduce respiratory tract damage by
ammonia and the level of bacterial and aerial endotoxin
exposure. Effective vaccination to protect against respira-
tory tract pathogens and immunosuppressive agents that
predispose to colibacillosis will aid greatly in reducing
occurrence of the disease.
Birds acquire nonspecific resistance to colibacillosis
following moderate stress and socialization with people.
Both low and high stress increases susceptibility to the
disease. Chickens that produce high levels of antibody are
more resistant to respiratory colisepticemia, but that is
due to the bird’s response to the predisposing agents
rather than E. coli. Birds with low antibody responses are
most resistant to the bacterium (98). Nonspecific resis-
tance is short-lived and can be suppressed by cold stress or
corticosterone (156).
644 SECTION II BACTERIAL DISEASES
Immunization
Inactivated Vaccines. Effective inactivated vaccines
against various serotypes, including O2:K1 and O78:K80,
have been produced (9, 35, 47, 48, 251). They provide
protection against the homologous serogroups but little if
any cross protection against heterologous serogroups. An
inactivated O78 vaccine protected ducks (222). Both
homologous and heterologous protection was provided
by a vaccine prepared by ultrasonic inactivation of the
organism followed by irradiation (160). A vaccine con-
taining bacterial membrane vesicles was effective in pro-
tecting chickens against challenge with pathogenic E. coli
by stimulating antibody production, bacterial-lysis activ-
ity of complement, T cell proliferation, and cytotoxic T
cell activity (36). Multivalent vaccines made from pili
containing low levels (180 µg) of protein per dose reduced
the severity of challenge infection (104). Absorbed sera
indicate pili of serotypes O1, O2, and O78 are antigeni-
cally different (242). Passive immunization results in
increased resistance to aerosol challenge and clearance of
bacteria from blood (169). Use of an inactivated vaccine
in breeders provided passive protection against homolo-
gous challenge in progeny, which was complete for 2
weeks and partial for several additional weeks post-hatch
(116).
Live Vaccines. A live vaccine prepared from a naturally
occurring, nonpathogenic, piliated strain (BT-7) was effi-
cacious when used in chickens older than 14 days of age.
Protection against both homologous and heterologous
strains was demonstrated (81). E. coli J5, a mutant strain
that has incomplete endotoxin in the cell wall, was both
safe and effective for protecting chicks (1, 2). A carAB
mutation of a virulent O2 serotype caused defective uti-
lization of arginine and pyrimidines, increasing their
requirement by the mutant. As low levels of these sub-
stances are generally available in vivo, the organism was
unable to sustain itself, which resulted in a self-limiting
infection. The mutant strain was found to be stable,
immunogenic, and attenuated. Turkeys orally vaccinated
with the mutant were protected against colibacillosis in a
hemorrhagic enteritis virus-parent wild-type strain chal-
lenge model (137). A recombinant vaccine using Salmo-
nella typhimurium was constructed to produce
homologous group B determinants and E. coli O78 anti-
gen. Vaccinated birds seroconverted and were protected
against subsequent challenge with a pathogenic E. coli
O78 strain (217).
Treatment
E. coli may be sensitive to many drugs such as ampicillin,
chloramphenicol, chlortetracycline, neomycin, nitrofu-
rans, gentamicin, ormethiprim-sulfadimethoxine,
nalidixic acid, oxytetracycline, polymyxin B, spectino-
mycin, streptomycin, and sulfa drugs. Water administra-
tion of apramycin proved effective in reducing the
numbers of organisms in the digestive tract and prevent-
ing bacteremia in chickens (146). Neomycin reduced mor-
tality in turkey poults exposed naturally to litter from
flocks with colibacillosis (155). Recently, fluoroquinolones
have become available in the United States and elsewhere
for treatment of colibacillosis in poultry, which generally
have proven to be highly efficacious (190) although some
strains have been shown to be resistant (87, 265). Anticoc-
cidials can also have antimicrobial activity-monensin
reduced colonization of chickens with E. coli O157:H7 to
undetectable levels 14 days post-exposure compared with
unmedicated controls and chickens receiving other coc-
cidiostats (236).
Isolates of E. coli from poultry are frequently resistant
to one or more drugs, especially if they have been widely
used in the poultry industry over a long period (e.g.,
tetracyclines) (6, 22, 190). Antibiograms have been deter-
mined for isolates of bacteria, including E. coli, from clin-
ically diseased chickens (133), turkeys (220), and ducks
(259). It is imperative to determine drug sensitivity of E.
coli strains involved in a disease outbreak so that ineffec-
tive drugs can be avoided. Even a highly effective drug
may not result in improvement of the flock if too little is
used or it is incapable of reaching the site of infection.
Under-dosing promotes the development of resistance.
When chicks were given feeds with increasing low con-
centrations of ampicillin (1.7 and 5 g/ton), development
of resistance was directly correlated to amount of antibi-
otic in the feed (5).
There is concern about antibiotic resistance and its trans-
mission to human pathogens. Resistance generally occurs
following response to prior contact with the antimicrobial
but can occur naturally in the absence of pervious exposure.
Resistance to florfenicol, an antibiotic related to chloram-
phenicol that has never been used in poultry in the United
States was found in E. coli isolates from chickens (132).
REFERENCES
1. Abdul Aziz, T. A. and S. N. El Sukhon. 1996. Serum sensitiv-
ity and apathogenicity for chickens and chick embryos of
Escherichia coli J5 strain. Vet Res 27:267—271.
2. Abdul Aziz, T. A. and S. N. El Sukhon. 1998. Chickens
hyperimmunized with Escherichia coli J5 strain are pro-
tected against experimental challenge with Escherichia coli
O78 serotype. Vet Res Comm 22:7—9.
3. Akashi, N., S. Hitotsubashi, H. Yamanaka, Y. Fujii, T. Tsuji,
A. Miyama, J. E. Joya, and K. Okamoto. 1993. Production of
heat-stable enterotoxin II by chicken clinical isolates of
Escherichia coli. FEMS Microbiol Lett 109:311—316.
4. Al Ankari, A. R., J. M. Bradbury, C. J. Naylor, K. J. Worthing-
ton, C. Payne Johnson, and R. C. Jones. 2001. Avian pneu-
movirus infection in broiler chicks inoculated with
Escherichia coli at different time intervals. Avian Pathol
30:257—267.
5. Al Sam, S., A. H. Linton, P. M. Bennett, and M. Hinton.
1993. Effects of low concentrations of ampicillin in feed on
the intestinal Escherichia coli of chicks. J Appl Bacteriol
75:108—112.
6. Allan, B. J., J. V. van den Hurk, and A. A. Potter. 1993. Char-
acterization of Escherichia coli isolated from cases of avian
colibacillosis. Can J Vet Res 57:146—151.
 CHAPTER 18 COLIBACILLOSIS
7. Ardrey, W. B., C. F. Peterson, and M. Haggart. 1968. Experi-
mental colibacillosis and the development of carriers in lay-
ing hens. Avian Dis 12:505—511.
8. Arenas, A., S. Vicente, I. Luque, J. C. Gomez-Villamandos,
R. Astorga, A. Maldonado, and C. Tarradas. 1999. Outbreak
of septicaemic colibacillosis in Japanese quail (Coturnix
coturnix japonica). Zentralbl Veterinarmed [B] 46:399—404.
9. Arp, L. H. 1982. Effect of passive immunization on phago-
cytosis of blood-borne Escherichia coli in spleen and liver
of turkeys. Am J Vet Res 43:1034—1040.
10. Arp, L. H. 1984. Effect of antipili antibody on clearance of
piliated Escherichia coli from the bloodstream of turkeys.
Abstracts of papers presented at the 65th Annual Meeting of
the Conference of Research Workers in Animal Disease. 123.
11. Arp, L. H. 1985. Effect of antibodies to type 1 fimbriae on
clearance of fimbriated Escherichia coli from the blood-
stream of turkeys. Am J Vet Res 46:2644—2647.
12. Arp, L. H. and N. F. Cheville. 1981. Interaction of blood-
borne Escherichia coli with phagocytes of spleen and liver
in turkeys. Am J Vet Res 42:650—657.
13. Barnes, H. J. 2000. Pathological manifestation of colibacil-
losis in poultry. Proc 21st World’s Poultry Congress, Mon-
tréal, Canada, Aug 20—24.
14. Barnes, H. J. and F. Lozano. 1994. Colibacillosis in Poultry.
Pfizer Veterinary Practicum, Pfizer Animal Health: Lee’s
Summit, MO, 45.
15. Beery, J. T., M. P. Doyle, and J. L. Schoeni. 1985. Coloniza-
tion of chicken cecae by Escherichia coli associated with
hemorrhagic colitis. Appl Environ Microbiol 49:310—315.
16. Bell, C. and A. Kyriakides. 1998. E. coli A Practical Approach
to the Organism and Its Control in Foods. Blackie Academic
& Professional: London, 200.
17. Berkhoff, H. A. and A. C. Vinal. 1986. Congo red medium to
distinguish between invasive and non-invasive Escherichia
coli pathogenic for poultry. Avian Dis 30:117—121.
18. Bettelheim, K. A. 1994. Biochemical characteristics of
Escherichia coli. In C. L. Gyles (ed.). Escherichia coli in
Domestic Animals and Humans. CAB Int’l: Wallingford,
UK, 3—30
19. Bisgaard, M. 1981. Arthritis in ducks. I. Aetiology and pub-
lic health aspects. Avian Pathol 10:11—21.
20. Bisgaard, M. 1995. Salpingitis in web-footed birds: preva-
lence, aetiology and significance. Avian Pathol 24:443—452.
21. Bisgaard, M. and A. Dam. 1981. Salpingitis in poultry. II.
Prevalence, bacteriology, and possible pathogenesis in egg-
laying chickens. NordVet 33:81—89.
22. Blanco, J. E., M. Blanco, A. Mora, and J. Blanco. 1997.
Prevalence of bacterial resistance to quinolones and other
antimicrobials among avian Escherichia coli strains isolated
from septicemic and healthy chickens in Spain. J Clin Micro-
biol 35:2184—2185.
23. Blanco, J. E., M. Blanco, A. Mora, and J. Blanco. 1997. Pro-
duction of toxins (enterotoxins, verotoxins, and necrotox-
ins) and colicins by Escherichia coli strains isolated from
septicemic and healthy chickens: Relationship with in vivo
pathogenicity. J Clin Microbiol 35:2953—2957.
24. Blanco, J. E., M. Blanco, A. Mora, W. H. Jansen, V. Garcia,
M. L. Vazquez, and J. Blanco. 1998. Serotypes of Escherichia
coli isolated from septicaemic chickens in Galicia (north-
west Spain). Vet Microbiol 61:229—235.
25. Boa Amponsem, K., A. Yang, N. K. Praharaj, E. A. Dunning-
ton, W. B. Gross, and P. B. Siegel. 1997. Impact of alternate-
day feeding cycles on immune and antibacterial responses
of White Leghorn chicks. J Appl Poult Res 6:123—127.
26. Boado, E. and G. Rojas. 1990. Diagnosis and pathological
study of goose diseases. I. Rev Cubana Ciencia Avicola
17:19—25.
645
27. Boado, E., L. Zaldivar, and A. Gonzalez. 1992. Diagnosis,
report and incidence of diseases of the pigeon (Columba
livia) in Cuba. Rev Cubana Ciencia Avicola 19:74—78.
28. Boado, E., L. Zaldivar, S. Lopez, A. Gonzalez, and D. Quin-
tero. 1991. Diagnosis and pathology of diseases of
guineafowls in Cuba. Rev Cubana Ciencia Avicola 18:156—161.
29. Boado, E., A. Gonzalez, V. Masdeu, C. Fonseca, O. Via-
montes, and Y. J. Camejo. 1988. Chlorination of drinking
water against coli septicaemia in fowls. Revista Avicultura
32:45—58.
30. Bolin, C. A. 1986. Effects of exogenous iron on Escherichia
coli septicemia of turkeys. Am J Vet Res 47:1813—1816.
31. Bradley, R. E. and W. M. Reid. 1966. Histomonas melea-
gridis and several bacteria as agents of infectious enterohep-
atitis in gnotobiotic turkeys. Exp Parasitol 19:91—101.
32. Bree, A., M. Dho, and J. P. Lafont. 1989. Comparative infec-
tivity for axenic and specific-pathogen-free chickens of O2
Escherichia coli strains with or without virulence factors.
Avian Dis 33:134—139.
33. Carr, D., D. Shaw, D. A. Halvorson, B. Rings, and D. Roepke.
1996. Excessive mortality in market-age turkeys associated
with cellulitis. Avian Dis 40:736—741.
34. Caya, F., J. M. Fairbrother, L. Lessard, and S. Quessy. 1999.
Characterization of the risk to human health of pathogenic
Escherichia coli isolates from chicken carcasses. J Food Prot
62:741—746.
35. Cessi, D. 1979. Prophylaxis of Escherichia coli infection in
fowls with emulsified vaccines. Clinica Veterinaria 102:270—
278.
36. Chaffer, M., B. Schwartsburd, and E. D. Heller. 1997. Vacci-
nation of turkey poults against pathogenic Escherichia coli.
Avian Pathol 26:377—390.
37. Chaffer, M., E. D. Heller, and B. Schwartsburd. 1999. Rela-
tionship between resistance to complement, virulence and
outer membrane protein patterns in pathogenic Escherichia
coli O2 isolates. Vet Microbiol 64:323—332.
38. Chamanza, R., L. v. Veen, M. T. Tivapasi, M. J. M. Toussaint,
and L. van Veen. 1999. Acute phase proteins in the domes-
tic fowl. World’s Poult Sci J 55:61—71.
39. Chansiripornchai, N., P. Ramasoota, J. Sasipreeyajan, and S.
B. Svenson. 2001. Differentiation of avian pathogenic
Escherichia coli (APEC) strains by random amplified poly-
morphic DNA (RAPD) analysis. Vet Microbiol 80:75—83.
40. Cheville, N. F. and L. H. Arp. 1978. Comparative pathologic
findings of Escherichia coli infection in birds. J Am Vet Med
Assoc 173:584—587.
41. Chulasiri, M. and O. Suthienkul. 1989. Antimicrobial resis-
tance of Escherichia coli isolated from chickens. Vet Micro-
biol 21:189—194.
42. Clark, S. R., H. J. Barnes, A. A. Bickford, R. P. Chin, and R.
Droual. 1991. Relationship of osteomyelitis and associated
soft-tissue lesions with green liver discoloration in tom
turkeys. Avian Dis 35:139—146.
43. Cloud, S. S., J. K. Rosenberger, P. A. Fries, R. A. Wilson, and
E. M. Odor. 1985. In vitro and in vivo characterization of
avian Escherichia coli. I. Serotypes, metabolic activity, and
antibiotic sensitivity. Avian Dis 29:1084—1093.
44. Cook, J. K. A., H. W. Smith, and M. B. Huggins. 1986. Infec-
tious bronchitis immunity: Its study in chickens experi-
mentally infected with mixtures of infectious bronchitis
virus and Escherichia coli. J Gen Virol 67:1427—1434.
45. Cook, J. K. A., M. B. Huggins, and M. M. Ellis. 1991. Use of
an infectious bronchitis virus and Escherichia coli model
infection to assess the ability to vaccinate successfully
against infectious bronchitis in the presence of maternally-
derived immunity. Avian Pathol 20:619—626.
46. Davis, C. R. 1938. Colibacillosis in young chicks. J Am Vet
Med Assoc 92:518—522.
646 SECTION II BACTERIAL DISEASES
47. Deb, J. R. and E. G. Harry. 1976. Laboratory trials with inac-
tivated vaccines against Escherichia coli (O78 K80) infec-
tion in fowls. Res Vet Sci 20:131—138.
48. Deb, J. R. and E. G. Harry. 1978. Laboratory trials with inac-
tivated vaccines against Escherichia coli (O2:K1) infection
in fowls. Res Vet Sci 24:308—313.
49. Dell’ Omo, G., S. Morabito, R. Quondam, U. Agrimi, F. Ciu-
chini, A. Macri, and A. Caprioli. 1998. Feral pigeons as a
source of verocytotoxin-producing Escherichia coli. Vet Rec
142:309—310.
50. DeRosa, M., M. D. Ficken, and H. J. Barnes. 1992. Acute air-
sacculitis in untreated and cyclophosphamide-pretreated
broiler chickens inoculated with Escherichia coli or
Escherichia coli cell-free culture filtrate. Vet Pathol 29:68—78.
51. Dhillon, A. S. 1986. Pathology of avian adenovirus
serotypes in the presence of Escherichia coli in infectious-
bursal-disease-virus-infected specific-pathogen-free chick-
ens. Avian Dis 30:81—86.
52. Dhillon, A. S. and F. S. Kibenge. 1987. Adenovirus infection
associated with respiratory disease in commercial chickens.
Avian Dis 31:654—657.
53. Dhillon, A. S. and O. K. Jack. 1996. Two outbreaks of col-
ibacillosis in commercial caged layers. Avian Dis 40:742—746.
54. Dho, M. and J. P. Lafont. 1982. Escherichia coli colonization
of the trachea in poultry: comparison of virulent and aviru-
lent strains in gnotoxenic chickens. Avian Dis 26:787—797.
55. Dho, M. and J. P. Lafont. 1984. Adhesive properties and
iron uptake ability in Escherichia coli lethal and nonlethal
for chicks. Avian Dis 28:1016—1025.
56. Dho-Moulin, M. and J. M. Fairbrother. 1999. Avian patho-
genic Escherichia coli (APEC). Vet Res 30:299—316.
57. Doetkott, D. M., L. K. Nolan, C. W. Giddings, and D. L.
Berryhill. 1996. Large plasmids of avian Escherichia coli iso-
lates. Avian Dis 40:927—930.
58. Dominick, M. A. and A. E. Jensen. 1984. Colonization and
persistence of Escherichia coli in axenic and monoxenic
turkeys. Am J Vet Res 45:2331—2335.
59. Dominick, M. A. and N. F. Cheville. 1985. Pathology of
cloacal bursae of gnotobiotic turkeys orally inoculated with
Escherichia coli. Vet Pathol 22:262—271.
60. Doyle, M. P. and J. L. Schoeni. 1987. Isolation of Escherichia
coli O157:H7 from retail fresh meats and poultry. Appl Envi-
ron Microbiol 53:2394—2396.
61. Dozois, C. M., S. A. Pourbakhsh, and J. M. Fairbrother. 1995.
Expression of P and type 1 (F1) fimbriae in pathogenic
Escherichia coli from poultry. Vet Microbiol 45:297—309.
62. Dozois, C. M., J. Harel, and J. M. Fairbrother. 1996. P-fim-
briae-producing septicaemic Escherichia coli from poultry
possess fel-related gene clusters whereas pap-hybridizing P-
fimbriae-negative strains have partial or divergent P fimbr-
ial gene clusters. Microbiol 142:2759—2766.
63. Dozois, C. M., N. Chanteloup, M. Dho-Moulin, A. Bree, C.
Desautels, and J. M. Fairbrother. 1994. Bacterial coloniza-
tion and in vivo expression of F1 (type 1) fimbrial antigens
in chickens experimentally infected with pathogenic
Escherichia coli. Avian Dis 38:231—239.
64. Dozois, C.M., M. Dho-Moulin, A. Bree, J.M. Fairbrother, C.
Desautels, and R. Curtiss, 3rd. 2000. Relationship between
the Tsh autotransporter and pathogenicity of avian
Escherichia coli and localization and analysis of the Tsh
genetic region. Infect Immun 68:4145—4154.
65. Droual, R. and P. Woolcock. 1994. Swollen head syndrome
associated with E. coli and infectious bronchitis virus in the
Central Valley of California. Avian Pathol 23:733—742.
66. Droual, R., R. P. Chin, and M. Rezvani. 1996. Synovitis,
osteomyelitis, and green liver in turkeys associated with
Escherichia coli. Avian Dis 40:417—424.
67. Edens, F. W., C. R. Parkhurst, I. A. Casas, and W. J. Dobro-
gosz. 1997. Principles of ex ovo competitive exclusion and
in ovo administration of Lactobacillus reuteri. Poult Sci
76:179—196.
68. Edens, F. W., C. R. Parkhurst, M. A. Qureshi, I. A. Casas, and
G. B. Havenstein. 1997. Atypical Escherichia coli strains
and their association with poult enteritis and mortality syn-
drome. Poult Sci 76:952—960.
69. Edens, F. W., R. A. Qureshi, C. R. Parkhurst, M. A. Qureshi,
G. B. Havenstein, and I. A. Casas. 1997. Characterization of
two Escherichia coli isolates associated with poult enteritis
and mortality syndrome. Poult Sci 76:1665—1673.
70. Emery, D. A., K. V. Nagaraja, D. P. Shaw, J. A. Newman, and
D. G. White. 1992. Virulence factors of Escherichia coli
associated with colisepticemia in chickens and turkeys.
Avian Dis 36:504—511.
71. Ewing, W. H. 1986. Edwards and Ewing’s Identification of
Enterobacteriaceae. 4th ed. Elsevier, Amsterdam, 536.
72. Fallacara, D. M., C. M. Monahan, T. Y. Morishita, and R. F.
Wack. 2001. Fecal shedding and antimicrobial susceptibility
of selected bacterial pathogens and a survey of intestinal
parasites in free-living waterfowl. Avian Dis 45:128—135.
73. Farmer, J. J., 3rd, G. R. Fanning, B. R. Davis, C. M. O’Hara,
C. Riddle, F. W. Hickman-Brenner, M. A. Asbury, V. A. Low-
ery, 3rd, and D. J. Brenner. 1985. Escherichia fergusonii and
Enterobacter taylorae, two new species of Enterobacteri-
aceae isolated from clinical specimens. J Clin Microbiol
21:77—81.
74. Ficken, M. D., J. F. Edwards, and J. C. Lay. 1986. Clearance
of bacteria in turkeys with Bordetella avium-induced tra-
cheitis. Avian Dis 30:352—357.
75. Ficken, M. D., J. F. Edwards, J. C. Lay, and D. E. Tveter. 1987.
Tracheal mucus transport rate and bacterial clearance in
turkeys exposed by aerosol to La Sota strain of Newcastle
disease virus. Avian Dis 31:241—248.
76. Foley, S. L., S. M. Horne, C. W. Giddings, M. Robinson, and
L. K. Nolan. 2000. Iss from a virulent avian Escherichia coli.
Avian Dis 44:185—191.
77. Franchesi, M. D., S. Viora, and H. Barrios. 1995. Escherichia
coli infections in layer quails. Rev Med Vet Buenos Aires
76:416—420.
78. Friedman, A., E. Shalem Meilin, and E. D. Heller. 1992.
Marek’s disease vaccines cause temporary B-lymphocyte
dysfunction and reduced resistance to infection in chicks.
Avian Pathol 21:621—631.
79. Friedman, A., I. Bartov, and D. Sklan. 1998. Humoral
immune response impairment following excess vitamin E
nutrition in the chick and turkey. Poult Sci 77:956—962.
80. Friedman, J., M. S. Dison, S. Perl, and Y. Weisman. 1988.
Spondylosis in turkeys. Israel J Vet Med 44:97—102.
81. Frommer, A., P. J. Freidlin, R. R. Bock, G. Leitner, M. Chaf-
fer, and E. D. Heller. 1994. Experimental vaccination of
young chickens with a live, non-pathogenic strain of
Escherichia coli. Avian Pathol 23:425—433.
82. Fukui, H., M. Sueyoshi, M. Haritani, M. Nakazawa, S.
Naitoh, H. Tani, and Y. Uda. 1995. Natural infection with
attaching and effacing Escherichia coli (O 103:H-) in chicks.
Avian Dis 39:912—918.
83. Gazdzinski, P. and H. J. Barnes. 2002. Venereal colibacillosis
(acute vaginitis) in turkey breeder hens. Proc 51st Western
Poult Dis Conf: Puerto Vallarta, MX, May 1—4, 176—177.
84. Gerardin, J., L. Lalioui, E. Jacquemin, J. G. Mainil, and C. le
Bouguenec. 2000. The afa-related gene cluster in necrotoxi-
genic and other Escherichia coli from animals belongs to
the afa-8 variant. Vet Microbiol 76:175—184.
85. Ginns, C. A., G. F. Browning, M. L. Benham, and K. G.
Whithear. 1998. Development and application of an
 CHAPTER 18 COLIBACILLOSIS
aerosol challenge method for reproduction of avian col-
ibacillosis. Avian Pathol 27:505—511.
86. Ginns, C. A., M. L. Benham, L. M. Adams, K. G. Whithear,
K. A. Bettelheim, B. S. Crabb, and G. F. Browning. 2000.
Colonization of the respiratory tract by a virulent strain of
avian Escherichia coli requires carriage of a conjugative
plasmid. Infect Immun 68:1535—1541.
87. Giraud, E., S. Leroy-Setrin, G. Flaujac, A. Cloeckaert, M.
Dho-Moulin, and E. Chaslus-Dancla. 2001. Characteriza-
tion of high-level fluoroquinolone resistance in Escherichia
coli O78:K80 isolated from turkeys. J Antimicrob Chemother
47:341—343.
88. Gomis, S., A. K. Amoako, A. M. Ngeleka, L. Belanger, B. Alt-
house, L. Kumor, E. Waters, S. Stephens, C. Riddell, A. Pot-
ter, and B. Allan. 2002. Histopathologic and bacteriologic
evaluations of cellulitis detected in legs and caudal abdomi-
nal regions of turkeys. Avian Dis 46:192—197.
89. Gomis, S. M., C. Riddell, A. A. Potter, and B. J. Allan. 2001.
Phenotypic and genotypic characterization of virulence fac-
tors of Escherichia coli isolated from broiler chickens with
simultaneous occurrence of cellulitis and other colibacillo-
sis lesions. Can J Vet Res 65:1—6.
90. Griffin, P. M. and R. V. Tauxe. 1991. The epidemiology of
infections caused by Escherichia coli O157:H7, other
enterohemorrhagic E. coli, and the associated hemolytic
uremic syndrome. Epidemiol Rev 13:60—98.
91. Gross, W. B. 1957. Escherichia coli infection of the chicken
eye. Avian Dis 1:37—41.
92. Gross, W. B. 1961. The development of “air sac disease.”
Avian Dis 5:431—439.
93. Gross, W. B. 1964. Retained caseous yolk sacs caused by
Escherichia coli. Avian Dis 8:438—441.
94. Gross, W. B. 1966. Electrocardiographic changes of
Escherichia coli-infected birds. Am J Vet Res 27:1427—1436.
95. Gross, W. B. 1984. Effect of a range of social stress severity
on Escherichia coli challenge infection. Am J Vet Res
45:2074—2076.
96. Gross, W. B. 1990. Factors affecting the development of res-
piratory disease complex in chickens. Avian Dis 34:607—610.
97. Gross, W. B. 1992. Effect of short-term exposure of chickens
to corticosterone on resistance to challenge exposure with
Escherichia coli and antibody response to sheep erythro-
cytes. Am J Vet Res 53:291—293.
98. Gross, W. B. 1994. Diseases due to Escherichia coli in poul-
try. In C. L. Gyles (ed.). Escherichia coli in Domestic Ani-
mals and Humans. CAB Int’l: Wallingford, UK, 237—260
99. Gross, W. B. 1995. Relationship between body-weight gain
after movement of chickens to an unfamiliar cage and
response to Escherichia coli challenge infection. Avian Dis
39:636—637.
100. Gross, W. B. and P. B. Siegel. 1959. Coliform peritonitis of
chickens. Avian Dis 3:370—373.
101. Guo, W., C. Ling, F. Cheng, W. Z. Guo, C. S. Ling, and F. H.
Cheng. 1998. Preliminary investigation on enterohaemor-
rhagic Escherichia coli O157 from domestic animals and
fowl in Fujian province. Chinese J Zoonoses 14:3—6.
102. Guy, J. S., L. G. Smith, J. J. Breslin, J. P. Vaillancourt, and H.
J. Barnes. 2000. High mortality and growth depression
experimentally produced in young turkeys by dual infec-
tion with enteropathogenic Escherichia coli and turkey
coronavirus. Avian Dis 44:105—113.
103. Gyimah, J. E. and B. Panigrahy. 1988. Adhesin-receptor inter-
actions mediating the attachment of pathogenic Escherichia
coli to chicken tracheal epithelium. Avian Dis 32:74—78.
104. Gyimah, J. E., B. Panigrahy, and J. D. Williams. 1986.
Immunogenicity of an Escherichia coli multivalent pilus
vaccine in chickens. Avian Dis 30:687—689.
647
105. Hakkinen, M. and C. Schneitz. 1996. Efficacy of a commer-
cial competitive exclusion product against a chicken patho-
genic Escherichia coli and E. coli O157:H7. Vet Rec
139:139—141.
106. Harmon, B. G. 1998. Avian heterophils in inflammation
and disease resistance. Poult Sci 77:972—977.
107. Harpreet, S., B. B. Dash, P. K. Dash, K. Sanjeev, H. Singh,
and S. Kumar. 1993. Mortality pattern in indigenous guinea
fowl under confinement rearing. Indian J Poult Sci 28:56—62.
108. Harry, E. G. 1957. The effect on embyonic and chick mor-
tality of yolk contaminated with bacteria from the hen. Vet
Rec 69:1433—1439.
109. Harry, E. G. 1963. Some observations on the bacterial content
of the ovary and oviduct of the fowl. Br Poult Sci 4:63—70.
110. Harry, E. G. 1964. The survival of E. coli in the dust of poul-
try houses. Vet Rec 76:466—470.
111. Harry, E. G. and L. A. Hemsley. 1965. The association
between the presence of septicaemia strains of Escherichia
coli in the respiratory and intestinal tracts of chickens and
the occurrence of coli septicaemia. Vet Rec 77:35—40.
112. Harry, E. G. and L. A. Hemsley. 1965. The relationship
between environmental contamination with septicaemia
strains of Escherichia coli and their incidence in chickens.
Vet Rec 77:241—245.
113. Hein, H. and L. Timms. 1972. Bacterial flora in the alimen-
tary tract of chickens infected with Eimeria brunetti and in
chickens immunized with Eimeria maxima and cross-
infected with Eimeria brunetti. Exp Parasitol 31:188—193.
114. Heller, E. D. and M. Perek. 1968. Pathogenic Escherichia
coli strains prevalent in poultry flocks in Israel. Br Vet J
124:509—513.
115. Heller, E. D. and N. Drabkin. 1977. Some characteristics of
pathogenic E. coli strains. Br Vet J 133:572—578.
116. Heller, E. D., G. Leitner, N. Drabkin, and D. Melamed. 1990.
Passive immunisation of chicks against Escherichia coli.
Avian Pathol 19:345—354.
117. Heuvelink, A. E., J. T. Zwartkruis-Nahuis, F. L. van den
Biggelaar, W. J. van Leeuwen, and E. de Boer. 1999. Isolation
and characterization of verocytotoxin-producing
Escherichia coli O157 from slaughter pigs and poultry. Int J
Food Microbiol 52:67—75.
118. Himathongkham, S., H. Riemann, S. Bahari, S. Nuanual-
suwan, P. Kass, and D. O. Cliver. 2000. Survival of Salmo-
nella typhimurium and Escherichia coli O157:H7 in poultry
manure and manure slurry at sublethal temperatures. Avian
Dis 44:853—860.
119. Hines, M. E., II, E. L. Styer, C. A. Baldwin, and J. R. Cole, Jr.
1995. Combined adenovirus and rotavirus enteritis with
Escherichia coli septicemia in an emu chick (Dromaius
novaehollandiae). Avian Dis 39:646—651.
120. Hinz, K. H., M. Ryll, U. Heffels Redmann, and M. Poppel.
1992. Multicausal infectious respiratory disease of turkey
poults. Dtsch Tierarztl Wochenschr 99:75—78.
121. Hofacre, C. L., A. C. Johnson, B. J. Kelly, and R. Froyman.
2002. Effect of a commercial competitive exclusion culture
on reduction of colonization of an antibiotic-resistant path-
ogenic Escherichia coli in day-old broiler chickens. Avian
Dis 46:198—202.
122. Horne, S. M., S. J. Pfaff McDonough, C. W. Giddings, and L.
K. Nolan. 2000. Cloning and sequencing of the iss gene
from a virulent avian Escherichia coli. Avian Dis 44:179—184.
123. Huang, H. J. and M. Matsumoto. 2000. Nonspecific innate
immunity against Escherichia coli infection in chickens
induced by vaccine strains of Newcastle disease virus. Avian
Dis 44:790—796.
124. Huff, G. R., W. E. Huff, J. M. Balog, and N. C. Rath. 1999.
Sex differences in the resistance of turkeys to Escherichia
648 SECTION II BACTERIAL DISEASES
coli challenge after immunosuppression with dexametha-
sone. Poult Sci 78:38—44.
125. Huff, G. R., W. E. Huff, N. C. Rath, and J. M. Balog. 2000.
Turkey osteomyelitis complex. Poult Sci 79:1050—1056.
126. Huff, G. R., W. E. Huff, J. M. Balog, and N. C. Rath. 2001.
Effect of early handling of turkey poults on later responses
to multiple dexamethasone-Escherichia coli challenge. 2.
Resistance to air sacculitis and turkey osteomyelitis com-
plex. Poult Sci 80:1314—1322.
127. Ishii, E., M. Goryo, S. Kikuchi, and K. Okada. 1997. Pathol-
ogy of swollen head syndrome in broiler chickens. J Japan
Vet Med Assoc 50:214—219.
128. Janssen, T., C. Schwarz, P. Preikschat, M. Voss, H. C. Philipp,
and L. H. Wieler. 2001. Virulence-associated genes in avian
pathogenic Escherichia coli (APEC) isolated from internal
organs of poultry having died from colibacillosis. Intl J Med
Microbiol 291:371—378.
129. Jeffrey, J. S., L. K. Nolan, K. H. Tonooka, S. Wolfe, C. W. Gid-
dings, S. M. Horne, S. L. Foley, A. M. Lynne, J. O. Ebert, L.
M. Elijah, G. Bjorklund, S. J. Pfaff-McDonough, R. S. Singer,
and C. Doetkott. 2002. Virulence factors of Escherichia coli
from cellulitis or colisepticemia lesions in chickens. Avian
Dis 46:48—52.
130. Johnson, L. C., S. F. Bilgili, F. J. Hoerr, B. L. McMurtrey, and
R. A. Norton. 2001. The influence of Escherichia coli strains
from different sources and the age of broiler chickens on
the development of cellulitis. Avian Pathol 30:475—479.
131. Joya, J. E., T. Tsuji, A. V. Jacalne, M. Arita, T. Tsukamoto, T.
Honda, and T. Miwatani. 1990. Demonstration of entero-
toxigenic Escherichia coli in diarrheic broiler chicks. Eur J
Epidemiol 6:88—90.
132. Keyes, K., C. Hudson, J. J. Maurer, S. Thayer, D. G. White,
and M. D. Lee. 2000. Detection of florfenicol resistance
genes in Escherichia coli isolated from sick chickens.
Antimicrob Agents Chemother 44:421—424.
133. Klein, L. K., R. J. Yancey, Jr., C. A. Case, and S. A. Salmon.
1996. Minimum inhibitory concentrations of selected
antimicrobial agents against bacteria isolated from 1—14-
day-old broiler chicks. J Vet Diag Invest 8:494—495.
134. Knobl, T., M. R. Baccaro, A. M. Moreno, T. A. T. Gomes, M.
A. M. Vieira, C. S. A. Ferreira, and A. J. P. Ferreira. 2001. Vir-
ulence properties of Escherichia coli isolated from ostriches
with respiratory disease. Vet Microbiol 83:71—80.
135. Kodihalli, S., V. Sivanandan, K. V. Nagaraja, D. Shaw, and D.
A. Halvorson. 1994. Effect of avian influenza virus infection
on the phagocytic function of systemic phagocytes and pul-
monary macrophages of turkeys. Avian Dis 38:93—102.
136. Krause, W. J., R. H. Freeman, S. L. Eber, F. K. Hamra, K. F.
Fok, M. G. Currie, and L. R. Forte. 1995. Distribution of
Escherichia coli heat-stable
enterotoxin/guanylin/uroguanylin receptors in the avian
intestinal tract. Acta Anat 153:210—219.
137. Kwaga, J. K., B. J. Allan, J. V. van der Hurk, H. Seida, and A.
A. Potter. 1994. A carAB mutant of avian pathogenic
Escherichia coli serogroup O2 is attenuated and effective as
a live oral vaccine against colibacillosis in turkeys. Infect
Immun 62:3766—3772.
138. La Ragione, R. M., A. R. Sayers, and M. J. Woodward. 2000.
The role of fimbriae and flagella in the colonization, inva-
sion and persistence of Escherichia coli O78:K80 in the day-
old-chick model. Epidemiol Infect 124:351—363.
139. La Ragione, R. M., G. Casula, S. M. Cutting, and M. J.
Woodward. 2001. Bacillus subtilis spores competitively
exclude Escherichia coli O78:K80 in poultry. Vet Microbiol
79:133—142.
140. Lafont, J. P., A. Bree, and M. Plat. 1984. Bacterial conjuga-
tion in the digestive tracts of gnotoxenic chickens. Appl
Environ Microbiol 47:639—642.
141. Lafont, J. P., M. Dho, H. M. D’Hauteville, A. Bree, and P. J.
Sansonetti. 1987. Presence and expression of aerobactin
genes in virulent avian strains of Escherichia coli. Infect
Immun 55:193—197.
142. Larsen, C. T., F. W. Pierson, and W. B. Gross. 1997. Effect of
dietary selenium on the response of stressed and unstressed
chickens to Escherichia coli challenge and antigen. Biol
Trace Element Res 58:169.
143. Lee, M. D. and L. H. Arp. 1998. Colibacillosis. In D. E.
Swayne, J. R. Glisson, M. W. Jackwood, J. E. Pearson, and W.
M. Reed (eds.). A Laboratory Manual for the Isolation and
Identification of Avian Pathogens. Am Assoc Avian Patholo-
gists: Kennett Square, PA, 14—16
144. Leibovitz, L. 1972. A survey of the so-called “anatipestifer
syndrome.” Avian Dis 16:836—851.
145. Leitner, G. and E. D. Heller. 1992. Colonization of
Escherichia coli in young turkeys and chickens. Avian Dis
36:211—220.
146. Leitner, G., R. Waiman, and E. D. Heller. 2001. The effect of
apramycin on colonization of pathogenic Escherichia coli
in the intestinal tract of chicks. Vet Q 23:62—66.
147. Leitner, G., D. Melamed, N. Drabkin, and E. D. Heller. 1990.
An enzyme-linked immunosorbent assay for detection of
antibodies against Escherichia coli: association between
indirect hemagglutination test and survival. Avian Dis
34:58—62.
148. Linares, J. A., A. A. Bickford, G. L. Cooper, B. R. Charlton,
and P. R. Woolcock. 1994. An outbreak of infectious laryn-
gotracheitis in California broilers. Avian Dis 38:188—192.
149. Lior, H. 1994. Classification of Escherichia coli. In C. L.
Gyles (ed.). Escherichia coli in Domestic Animals and
Humans. CAB Int’l: Wallingford, UK, 31—72
150. Litjens, J. B., F. C. van Willigen, and M. Sinke. 1989. A case
of swollen head syndrome in a flock of guinea fowl. Tijdschr
Diergeneeskd 114:719—720.
151. Macklin, K. S., R. A. Norton, J. B. Hess, and S. F. Bilgili.
2000. The effect of vitamin E on cellulitis in broiler chick-
ens experiencing scratches in a challenge model. Avian Dis
44:701—705.
152. MacOwan, K. J., C. J. Randall, H. G. R. Jones, and T. F.
Brand. 1982. Association of Mycoplasma synoviae with res-
piratory disease of broilers. Avian Pathol 11:235—244.
153. Madhu, S., A. K. Katiyar, J. L. Vegad, and M. Swamy. 2001.
Bacteria-induced increased vascular permeability in the
chicken skin. Indian J An Sci 71:621—622.
154. Majo, N., X. Gibert, M. Vilafranca, C. J. O’Loan, G. M.
Allan, L. Costa, A. Pages, and A. Ramis. 1997. Turkey rhino-
tracheitis virus and Escherichia coli experimental infection
in chickens: Histopathological, immunocytochemical and
microbiological study. Vet Microbiol 57:29—40.
155. Marrett, L. E., E. J. Robb, and R. K. Frank. 2000. Efficacy of
neomycin sulfate water medication on the control of mor-
tality associated with colibacillosis in growing turkeys. Poult
Sci 79:12—17.
156. Matsumoto, M., H. Huang, and H. J. Huang. 2000. Induc-
tion of short-term, nonspecific immunity against
Escherichia coli infection in chickens is suppressed by cold
stress or corticosterone treatment. Avian Pathol 29:227—232.
157. Maurer, J. J., M. D. Lee, C. Lobsinger, T. Brown, M. Maier,
and S. G. Thayer. 1998. Molecular typing of avian
Escherichia coli isolates by random amplification of poly-
morphic DNA. Avian Dis 42:431—451.
158. McAllister, J. C., C. D. Steelman, J. K. Skeeles, L. A. New-
berry, and E. E. Gbur. 1996. Reservoir competence of Alphi-
tobius diaperinus (Coleoptera: Tenebrionidae) for
Escherichia coli (Eubacteriales: Enterobacteriaceae). J Med
Entomol 33:983—987.
 CHAPTER 18 COLIBACILLOSIS
159. McNamee, P. T. and J. A. Smyth. 2000. Bacterial chon-
dronecrosis with osteomyelitis (‘femoral head necrosis’) of
broiler chickens: A review. Avian Pathol 29:253—270.
160. Melamed, D., G. Leitner, and E. D. Heller. 1991. A vaccine
against avian colibacillosis based on ultrasonic inactivation
of Escherichia coli. Avian Dis 35:17—22.
161. Mellata, M., R. Bakour, E. Jacquemin, and J. G. Mainil.
2001. Genotypic and phenotypic characterization of poten-
tial virulence of intestinal avian Escherichia coli strains iso-
lated in Algeria. Avian Dis 45:670—679.
162. Montgomery, R. D., C. R. Boyle, T. A. Lenarduzzi, and L. S.
Jones. 1999. Consequences to chicks hatched from
Escherichia coli-inoculated embryos. Avian Dis 43:553—563.
163. Moorhead, P. D. and Y. M. Saif. 1970. Mycoplasma melea-
gridis and Escherichia coli infections in germfree and spe-
cific-pathogen-free turkey poults: pathologic
manifestations. Am J Vet Res 31:1645—1653.
164. Morabito, S., G. Dell’Omo, U. Agrimi, H. Schmidt, H. Karch,
T. Cheasty, and A. Caprioli. 2001. Detection and characteri-
zation of Shiga toxin-producing Escherichia coli in feral
pigeons. Vet Microbiol 82:275—283.
165. Morishita, T. Y. and A. A. Bickford. 1992. Pyogranulomatous
typhlitis and hepatitis of market turkeys. Avian Dis
36:1070—1075.
166. Morishita, T. Y., P. P. Aye, E. C. Ley, and B. S. Harr. 1999. Sur-
vey of pathogens and blood parasites in free-living passer-
ines. Avian Dis 43:549—552.
167. Morley, A. J. and D. K. Thomson. 1984. Swollen-head syn-
drome in broiler chickens. Avian Dis 28:238—243.
168. Murakami, S., Y. Okazaki, T. Kazama, T. Suzuki, I. Iwabuchi,
and K. Kirioka. 1989. A dual infection of Clostridium per-
fringens and Escherichia coli in broiler chicks. J Japan Vet
Med Assoc 42:405—409.
169. Myers, R. K. and L. H. Arp. 1987. Pulmonary clearance and
lesions of lung and air sac in passively immunized and
unimmunized turkeys following exposure to aerosolized
Escherichia coli. Avian Dis 31:622—628.
170. Nagai, S., T. Yagihashi, and A. Ishihama. 1998. An avian
pathogenic Escherichia coli strain produces a hemolysin,
the expression of which is dependent on cyclic AMP recep-
tor protein gene function. Vet Microbiol 60:227—238.
171. Nagaraja, K. V., D. A. Emery, K. A. Jordan, V. Sivanandan, J.
A. Newman, and B. S. Pomeroy. 1984. Effect of ammonia on
the quantitative clearance of Escherichia coli from lungs,
air sacs, and livers of turkeys aerosol vaccinated against
Escherichia coli. Am J Vet Res 45:392—395.
172. Nagi, M. S. and W. J. Mathey. 1972. Interaction of
Escherichia coli and Eimeria brunetti in chickens. Avian Dis
16:864—873.
173. Nagi, M.S. and L. G. Raggi. 1972. Importance to ‘airsac’ dis-
ease of water supplies contaminated with pathogenic
Escherichia coli. Avian Dis 16:718—723.
174. Nakamura, K. and F. Abe. 1987. Ocular lesions in chickens
inoculated with Escherichia coli. Can J Vet Res 51:528—530.
175. Nakamura, K., Y. Imada, and M. Maeda. 1986. Lymphocytic
depletion of bursa of Fabricius and thymus in chickens
inoculated with Escherichia coli. Vet Pathol 23:712—717.
176. Nakamura, K., Y. Imada, and F. Abe. 1987. Effect of
cyclophosphamide on infections produced by Escherichia
coli of high and low virulence in chickens. Avian Pathol
16:237—252.
177. Nakamura, K., T. Usobe, and M. Narita. 1990. Dual infec-
tions of Eimeria tenella and Escherichia coli in chickens.
Res Vet Sci 49:125—126.
178. Nakamura, K., K. Imai, and N. Tanimura. 1996. Comparison
of the effects of infectious bronchitis and infectious laryn-
gotracheitis on the chicken respiratory tract. J Comp Pathol
114:11—21.
649
179. Nakamura, K., N. Yuasa, H. Abe, and M. Narita. 1990. Effect
of infectious bursal disease virus on infections produced by
Escherichia coli of high and low virulence in chickens.
Avian Pathol 19:713—721.
180. Nakamura, K., J. K. Cook, J. A. Frazier, and M. Narita. 1992.
Escherichia coli multiplication and lesions in the respira-
tory tract of chickens inoculated with infectious bronchitis
virus and/or E. coli. Avian Dis 36:881—890.
181. Nakamura, K., H. Ueda, T. Tanimura, and K. Noguchi. 1994.
Effect of mixed live vaccine (Newcastle disease and infec-
tious bronchitis) and Mycoplasma gallisepticum on the
chicken respiratory tract and on Escherichia coli infection. J
Comp Pathol 111:33—42.
182. Nakamura, K., M. Maeda, Y. Imada, T. Imada, and K. Sato.
1985. Pathology of spontaneous colibacillosis in a broiler
flock. Vet Pathol 22:592—597.
183. Nakamura, K., M. Mase, N. Tanimura, S. Yamaguchi, and N.
Yuasa. 1998. Attempts to reproduce swollen head syndrome
in specific-pathogen-free chickens by inoculating with
Escherichia coli and/or turkey rhinotracheitis virus. Avian
Pathol 27:21—27.
184. Nakamura, K., M. Mase, N. Tanimura, S. Yamaguchi, M.
Nakazawa, and N. Yuasa. 1997. Swollen head syndrome in
broiler chickens in Japan: Its pathology, microbiology and
biochemistry. Avian Pathol 26:139—154.
185. Nakamura, K., Y. Mitarai, M. Yoshioka, N. Koizumi, T.
Shibahara, and Y. Nakajima. 1998. Serum levels of inter-
leukin-6, alpha1-acid glycoprotein, and corticosterone in
two-week-old chickens inoculated with Escherichia coli
lipopolysaccharide. Poultry Sci 77:908—911.
186. Naqi, S., G. Thompson, B. Bauman, and H. Mohammed.
2001. The exacerbating effect of infectious bronchitis virus
infection on the infectious bursal disease virus-induced sup-
pression of opsonization by Escherichia coil antibody in
chickens. Avian Dis 45:52—60.
187. Naqi, S. A., C. F. Hall, and D. H. Lewis. 1971. The intestinal
microflora of turkeys: comparison of apparently healthy
and bluecomb-infected turkey poults. Avian Dis 15:14—21.
188. Nataro, J. P. and J. B. Kaper. 1998. Diarrheagenic Escherichia
coli. Clin Microbiol Rev 11:142—201.
189. Newberry, L. A., J. K. Skeeles, D. L. Kreider, J. N. Beasley, J.
D. Story, R. W. McNew, and B. R. Berridge. 1993. Use of vir-
ulent hemorrhagic enteritis virus for the induction of col-
ibacillosis in turkeys. Avian Dis 37:1—5.
190. Ngeleka, M., L. Brereton, G. Brown, and J.M. Fairbrother.
2002. Pathotypes of avian Escherichia coli as related to tsh-,
pap-, pil-, and iuc-DNA sequences, and antibiotic sensitivity
of isolates from internal tissues and the cloacae of broilers.
Avian Dis 46:143—152.
191. Ngeleka, M., J. K. Kwaga, D. G. White, T. S. Whittam, C.
Riddell, R. Goodhope, A. A. Potter, and B. Allan. 1996.
Escherichia coli cellulitis in broiler chickens: Clonal rela-
tionships among strains and analysis of virulence-associ-
ated factors of isolates from diseased birds. Infect Immun
64:3118—3126.
192. Nivas, S. C., A. C. Peterson, M. D. York, B. S. Pomeroy, L. D.
Jacobson, and K. A. Jordan. 1977. Epizootiological investi-
gations of colibacillosis in turkeys. Avian Dis 21:514—530.
193. Nockels, C. F. 1979. Protective effects of supplemental vita-
min E against infection. Fed Proc 38:2134—2138.
194. Nolan, L. K., R. E. Wooley, and R. K. Cooper. 1992. Transpo-
son mutagenesis used to study the role of complement
resistance in the virulence of an avian Escherichia coli iso-
late. Avian Dis 36:398—402.
195. Nolan, L. K., R. E. Wooley, C. W. Giddings, and J. Brown.
1994. Characterization of an avirulent mutant of a virulent
avian Escherichia coli isolate. Avian Dis 38:146—150.
650 SECTION II BACTERIAL DISEASES
196. Nolan, L. K., R. E. Wooley, J. Brown, K. R. Spears, H. W.
Dickerson, and M. Dekich. 1992. Comparison of a comple-
ment resistance test, a chicken embryo lethality test, and
the chicken lethality test for determining virulence of avian
Escherichia coli. Avian Dis 36:395—397.
197. Norton, R. A., B. A. Hopkins, J. K. Skeeles, J. N. Beasley, and
J. M. Kreeger. 1992. High mortality of domestic turkeys
associated with Ascaridia dissimilis. Avian Dis 36:469—473.
198. Olkowski, A. A., L. Kumor, D. Johnson, M. Bielby, M.
Chirino Trejo, and H. L. Classen. 1999. Cellulitis lesions in
commercial turkeys identified during processing. Vet Rec
145:228—229.
199. Oyetunde, O. O. F., R. G. Thomson, and H. C. Carlson.
1978. Aerosol exposure of ammonia, dust and Escherichia
coli in broiler chickens. Can Vet J 19:187—193.
200. Palmer, C. C. and H. R. Baker. 1923. Studies on infectious
enteritis of poultry caused by Bacterium coli communis. J
Am Vet Med Assoc 63:85—96.
201. Parreira, V. R. and T. Yano. 1998. Cytotoxin produced by
Escherichia coli isolated from chickens with swollen head
syndrome (SHS). Vet Microbiol 62:111—119.
202. Parreira, V. R., C. W. Arns, and T. Yano. 1998. Virulence fac-
tors of avian Escherichia coli associated with swollen head
syndrome. Avian Pathol 27:148—154.
203. Pedersen, K. and N. Jahromi. 1993. Inactivation of bacteria
with SMAC—a stable solution of chlorine dioxide in water.
Vatten 49:264—270.
204. Pelkonen, S. and J. Finne. 1987. A rapid turbidometric assay
for the study of serum sensitivitiy of Escherichia coli. FEMS
Microbiol Lett 42:53—57.
205. Permin, A., J. P. Christensen, and M. Bisgaard. 2000. The
interactions between Ascaridia galli and Escherichia coli.
Proc 21st World’s Poultry Congress: Montréal, Canada, Aug
20—24.
206. Pfaff-McDonough, S. J., S. M. Horne, C. W. Giddings, J. O.
Ebert, C. Doetkott, M. H. Smith, and L. K. Nolan. 2000.
Complement resistance-related traits among Escherichia
coli isolates from apparently healthy birds and birds with
colibacillosis. Avian Dis 44:23—33.
207. Pierson, F. W., C. T. Larsen, and C. H. Domermuth. 1996.
The production of colibacillosis in turkeys following
sequential exposure to Newcastle disease virus or Bordetella
avium, avirulent hemorrhagic enteritis virus, and
Escherichia coli. Avian Dis 40:837—840.
208. Pierson, F. W., V. D. Barta, D. Boyd, and W. S. Thompson.
1996. Exposure to multiple infectious agents and the
development of colibacillosis in turkeys. J Appl Poult Res
5:347—357.
209. Pilipcinec, E., L. Tkacikova, H. T. Naas, R. Cabadaj, and I.
Mikula. 1999. Isolation of verotoxigenic Escherichia coli
O157 from poultry. Folia Microbiol 44:455—456.
210. Pourbakhsh, S. A., M. Boulianne, B. Martineau-Doize, and J.
M. Fairbrother. 1997. Virulence mechanisms of avian fim-
briated Escherichia coli in experimentally inoculated chick-
ens. Vet Microbiol 58:195—213.
211. Pourbakhsh, S. A., M. Boulianne, B. Martineau-Doize, C. M.
Dozois, C. Desautels, and J. M. Fairbrother. 1997. Dynamics
of Escherichia coil infection in experimentally inoculated
chickens. Avian Dis 41:221—233.
212. Pourbakhsh, S. A., M. Dho Moulin, A. Bree, C. Desautels, B.
Martineau Doize, and J. M. Fairbrother. 1997. Localization
of the in vivo expression of P and F1 fimbriae in chickens
experimentally inoculated with pathogenic Escherichia
coli. Microbial Pathog 22:331—341.
213. Praharaj, N. K., W. B. Gross, E. A. Dunnington, and P. B.
Siegel. 1996. Feeding regimen by sire family interactions on
growth, immunocompetence, and disease resistance in
chickens. Poult Sci 75:821—827.
214. Qureshi, M. A., Y. M. Saif, C. L. Heggen-Peay, F. W. Edens,
and G. B. Havenstein. 2001. Induction of functional defects
in macrophages by a poult enteritis and mortality syn-
drome-associated turkey astrovirus. Avian Dis 45:853—861.
215. Randall, C. J., W. G. Siller, A. S. Wallis, and K. S. Kirkpatrick.
1984. Multiple infections in young broilers. Vet Rec
114:270—271.
216. Reingold, J., N. Starr, J. Maurer, and M. D. Lee. 1999. Identi-
fication of a new Escherichia coli She haemolysin homolog
in avian E. coli. Vet Microbiol 66:125—134.
217. Roland, K., R. Curtiss, 3rd, and D. Sizemore. 1999. Con-
struction and evaluation of a delta cya delta crp Salmonella
typhimurium strain expressing avian pathogenic
Escherichia coli O78 LPS as a vaccine to prevent airsacculi-
tis in chickens. Avian Dis 43:429—441.
218. Rosenberger, J. K., P. A. Fries, S. S. Cloud, and R. A. Wilson.
1985. In vitro and in vivo characterization of avian
Escherichia coli. II. Factors associated with pathogenicity.
Avian Dis 29:1094—1107.
219. Saif, Y. M., P. D. Moorhead, and E. H. Bohl. 1970.
Mycoplasma meleagridis and Escherichia coli infections in
germfree and specific-pathogen-free turkey poults: Produc-
tion of complicated airsacculitis. Am J Vet Res 31:1637—1643.
220. Salmon, S. A. and J. L. Watts. 2000. Minimum inhibitory
concentration determinations for various antimicrobial
agents against 1570 bacterial isolates from turkey poults.
Avian Dis 44:85—98.
221. Salvadori, M. R., T. Yano, H. F. Carvalho, V. R. Parreira, and
C. L. Gyles. 2001. Vacuolating cytotoxin produced by avian
pathogenic Escherichia coli. Avian Dis 45:43—51.
222. Sandhu, T. S. and H. W. Layton. 1985. Laboratory and field
trials with formalin-inactivated Escherichia coli (O78)-Pas-
teurella anatipestifer bacterin in White Pekin ducks. Avian
Dis 29:128—135.
223. Schmidt, H., J. Scheef, S. Morabito, A. Caprioli, L. H. Wieler,
and H. Karch. 2000. A new Shiga toxin 2 variant (Stx2f)
from Escherichia coli isolated from pigeons. Appl Environ
Microbiol 66:1205—1208.
224. Sell, J. L., D. W. Trampel, and R. W. Griffith. 1997. Adverse
effects of Escherichia coli infection of turkeys were not alle-
viated by supplemental dietary vitamin E. Poult Sci
76:1682—1687.
225. Shawky, S., T. Sandhu, and H. L. Shivaprasad. 2000. Patho-
genicity of a low-virulence duck virus enteritis isolate with
apparent immunosuppressive ability. Avian Dis 44:590—599.
226. Siccardi, F. J. 1966. Identification and disease producing
ability of Escherichia coli associated with E. coli infection of
chickens and turkeys. MS thesis, University of Minnesota,
St. Paul, MN.
227. Silveira, W. D. d., A. Ferreira, M. Brocchi, L. M. d. Hollanda,
A. F. P. d. Castro, A. T. Yamada, M. Lancellotti, W. D. da Sil-
veira, L. M. de Hollanda, and A. F. P. de Castro. 2002. Bio-
logical characteristics and pathogenicity of avian
Escherichia coli strains. Vet Microbiol 85:47—53.
228. Singer, R. S., J. S. Jeffrey, T. E. Carpenter, C. L. Cooke, R. P.
Chin, E. R. Atwill, and D. C. Hirsh. 1999. Spatial hetero-
geneity of Escherichia coli DNA fingerprints isolated from
cellulitis lesions in chickens. Avian Dis 43:756—762.
229. Singer, R. S., J. S. Jeffrey, T. E. Carpenter, C. L. Cooke, E. R.
Atwill, W. O. Johnson, and D. C. Hirsh. 2000. Persistence of
cellulitis-associated Escherichia coli DNA fingerprints in
successive broiler chicken flocks. Vet Microbiol 75:59—71.
230. Smith, H. W., J. K. A. Cook, and Z. E. Parsell. 1985. The exper-
imental infection of chickens with mixtures of infectious
bronchitis virus and Escherichia coli. J Gen Virol 66:777—786.
 CHAPTER 18 COLIBACILLOSIS
231. Sojka, W. J. 1965. Escherichia coli in Domestic Animals and
Poultry. Commonwealth Agricultural Bureau: Farnham
Royal, England.
232. Songserm, T., J. M. Pol, D. van Roozelaar, G. L. Kok, F.
Wagenaar, and A. A. ter Huurne. 2000. A comparative study
of the pathogenesis of malabsorption syndrome in broilers.
Avian Dis 44:556—567.
233. Songserm, T., B. Zekarias, D. J. van Roozelaar, R. S. Kok, J. M.
Pol, A. A. Pijpers, and A. A. ter Huurne. 2002. Experimental
reproduction of malabsorption syndrome with different
combinations of reovirus, Escherichia coli, and treated
homogenates obtained from broilers. Avian Dis 46:87—94.
234. Springer, W. T., J. Johnson, and W. M. Reid. 1970. Histomoni-
asis in gnotobiotic chickens and turkeys: Biological aspects of
the role of bacteria in the etiology. Exp Parasitol 28:383—392.
235. Springer, W. T., C. Luskus, and S. S. Pourciau. 1974. Infectious
bronchitis and mixed infections of Mycoplasma synoviae
and Escherichia coli in gnotobiotic chickens. I. Synergistic
role in the airsacculitis syndrome. Inf Immun 10:578—589.
236. Stanley, V. G., S. Woldesenbet, and C. Gray. 1996. Sensitiv-
ity of Escherichia coli O157:H7 strain 932 to selected antic-
occidial drugs in broiler chicks. Poult Sci 75:42—46.
237. Stathopoulos, C., D. L. Provence, and R. Curtiss, 3rd. 1999.
Characterization of the avian pathogenic Escherichia coli
hemagglutinin Tsh, a member of the immunoglobulin A
protease-type family of autotransporters. Infect Immun
67:772—781.
238. Stavric, S., B. Buchanan, and T. M. Gleeson. 1993. Intestinal
colonization of young chicks with Escherichia coli O157:H7
and other verotoxin-producing serotypes. J Appl Bacteriol
74:557—563.
239. Stebbins, M. E., H. A. Berkhoff, and W. T. Corbett. 1992.
Epidemiological studies of congo red Escherichia coli in
broiler chickens. Can J Vet Res 56:220—225.
240. Stordeur, P., D. Marlier, J. Blanco, E. Oswald, F. Biet, M.
Dho-Moulin, and J. Mainil. 2002. Examination of
Escherichia coli from poultry for selected adhesin genes
important in disease caused by mammalian pathogenic E.
coli. Vet Microbiol 84:231—241.
241. Sueyoshi, M., H. Fukui, S. Tanaka, M. Nakazawa, and K. Ito.
1996. A new adherent form of an attaching and effacing
Escherichia coli (eaeA+, bfp-) to the intestinal epithelial
cells of chicks. J Vet Med Sci 58:1145—1147.
242. Suwanichkul, A., B. Panigrahy, and R. M. Wagner. 1987.
Antigenic relatedness and partial amino acid sequences of
pili of Escherichia coli serotypes O1, O2, and O78 patho-
genic to poultry. Avian Dis 31:809—813.
243. Swarbrick, O. 1985. Pheasant rearing: Associated husbandry
and disease problems. Vet Rec 116:610—617.
244. Synge, B. A. 2000. Recent epidemiological studies of verocy-
totoxin-producing E coli O157 in cattle in Scotland. Cattle
Practice 8:341—343.
245. Tantaswasdi, U., A. Malayaman, and K. F. Shortridge. 1986.
Influenza A virus infection of a pheasant. Vet Rec 119:375—
376.
246. Tengerdy, R. P. and C. F. Nockels. 1975. Vitamin E or vita-
min A protects chickens against E. coli infection. Poult Sci
54:1292—1296.
247. Tengerdy, R. P. and J. C. Brown. 1977. Effect of vitamin E
and A on humoral immunity and phagocytosis in E. coli
infected chicken. Poult Sci 56:957—963.
248. Terzich, M. and S. Vanhooser. 1993. Postmortem findings of
ostriches submitted to the Oklahoma Animal Disease Diag-
nostic Laboratory. Avian Dis 37:1136—1141.
249. Toth, T. E., H. Veit, W. B. Gross, and P. B. Siegel. 1988. Cellu-
lar defense of the avian respiratory system: Protection
651
against Escherichia coli airsacculitis by Pasteurella multo-
cida-activated respiratory phagocytes. Avian Dis 32:681—687.
250. Tottori, J., R. Yamaguchi, Y. Murakawa, M. Sato, K. Uchida,
and S. Tateyama. 1997. Experimental production of ascites
in broiler chickens using infectious bronchitis virus and
Escherichia coli. Avian Dis 41:214—220.
251. Trampel, D. W. and R. W. Griffth. 1997. Efficacy of alu-
minum hydroxide-adjuvanted Escherichia coli bacterin in
turkey poults. Avian Dis 41:263—268.
252. Van Alstine, W. G. and L. H. Arp. 1987. Effects of Bordetella
avium infection on the pulmonary clearance of Escherichia
coli in turkeys. Am J Vet Res 48:922—926.
253. Van de Zande, S., H. Nauwynck, and M. Pensaert. 2001. The
clinical, pathological and microbiological outcome of an
Escherichia coli O2:K1 infection in avian pneumovirus
infected turkeys. Vet Microbiol 81:353—365.
254. van den Bogaard, A. E., N. London, C. Driessen, and E. E.
Stobberingh. 2001. Antibiotic resistance of faecal
Escherichia coli in poultry, poultry farmers and poultry
slaughterers. J Antimicrob Chemother 47:763—771.
255. van den Hurk, J. V., B. J. Allan, C. Riddell, T. Watts, A. A.
Potter, and J. V. Van den Hurk. 1994. Effect of infection
with hemorrhagic enteritis virus on susceptibility of turkeys
to Escherichia coli. Avian Dis 38:708—716.
256. Vidotto, M. C., H. R. Navarro, and L. C. Gaziri. 1997. Adher-
ence pili of pathogenic strains of avian Escherichia coli. Vet
Microbiol 59:79—87.
257. Vidotto, M. C., E. E. Muller, J. C. de Freitas, A. A. Alfieri, I.
G. Guimaraes, and D. S. Santos. 1990. Virulence factors of
avian Escherichia coli. Avian Dis 34:531—538.
258. Wada, Y., H. Kondo, M. Nakazawa, and M. Kubo. 1995. Nat-
ural infection with attaching and effacing Escherichia coli
and adenovirus in the intestine of a pigeon with diarrhea. J
Vet Med Sci 57:531—533.
259. Watts, J. L., S. A. Salmon, R. J. Yancey, Jr., B. Nersessian, and
Z. V. Kounev. 1993. Minimum inhibitory concentrations of
bacteria isolated from septicemia and airsacculitis in ducks.
J Vet Diag Invest 5:625—628.
260. Weebadda, W. K., G. J. Hoover, D. B. Hunter, and M. A.
Hayes. 2001. Avian air sac and plasma proteins that bind
surface polysaccharides of Escherichia coli O2. Comp
Biochem Physiol B Biochem Mol Biol 130:299—312.
261. Weinack, O. M., G. H. Snoeyenbos, C. F. Smyser, and A. S.
Soerjadi. 1981. Competitive exclusion of intestinal colo-
nization of Escherichia coli in chicks. Avian Dis 25:696—705.
262. Weinack, O. M., G. H. Snoeyenbos, C. F. Smyser, and A. S.
Soerjadi-Liem. 1984. Influence of Mycoplasma gallisepticum,
infectious bronchitis, and cyclophosphamide on chickens
protected by native intestinal microflora against Salmonella
typhimurium or Escherichia coli. Avian Dis 28:416—425.
263. Welsh, R. D., R. W. Nieman, S. L. Vanhooser, and L. B. Dye.
1997. Bacterial infections in ratites. Vet Med 92:992—998.
264. White, D. G., M. Dho-Moulin, R. A. Wilson, and T. S. Whit-
tam. 1993. Clonal relationships and variation in virulence
among Escherichia coli strains of avian origin. Microb
Pathog 14:399—409.
265. White, D. G., L. J. Piddock, J. J. Maurer, S. Zhao, V. Ricci, and
S. G. Thayer. 2000. Characterization of fluoroquinolone
resistance among veterinary isolates of avian Escherichia
coli. Antimicrob Agents Chemother 44:2897—2899.
266. Wittig, W., R. Prager, E. Tietze, G. Seltmann, and H.
Tschape. 1988. Aerobactin-positive Escherichia coli as
causative agents of extra-intestinal infections among ani-
mals. Arch Exp Veterinarmed 42:221—229.
267. Woolcock, P. R., H. L. Shivaprasad, and M. De Rosa. 2000.
Isolation of avian influenza virus (H10N7) from an emu
652 SECTION II BACTERIAL DISEASES
(Dromaius novaehollandiae) with conjunctivitis and respi-
ratory disease. Avian Dis 44:737—744.
268. Wooley, R. E., P. S. Gibbs, T. P. Brown, and J. J. Maurer. 2000.
Chicken embryo lethality assay for determining the viru-
lence of avian Escherichia coli isolates. Avian Dis 44:318—324.
269. Wooley, R. E., K. R. Spears, J. Brown, L. K. Nolan, and O.J.
Fletcher. 1992. Relationship of complement resistance and
selected virulence factors in pathogenic avian Escherichia
coli. Avian Dis 36:679—684.
270. Wooley, R. E., K. R. Spears, J. Brown, L. K. Nolan, and M. A.
Dekich. 1992. Characteristics of conjugative R-plasmids from
pathogenic avian Escherichia coli. Avian Dis 36:348—352.
271. Wooley, R. E., J. Brown, P. S. Gibbs, L. K. Nolan, and K. R.
Turner. 1994. Effect of normal intestinal flora of chickens
on colonization by virulent colicin V-producing, avirulent,
and mutant colicin V-producing avian Escherichia coli.
Avian Dis 38:141—145.
272. Wooley, R. E., L. K. Nolan, J. Brown, P. S. Gibbs, C. W. Gid-
dings, and K. S. Turner. 1993. Association of K-1 capsule,
smooth lipopolysaccharides, traT gene, and colicin V pro-
duction with complement resistance and virulence of avian
Escherichia coli. Avian Dis 37:1092—1096.
273. Wooley, R. E., P. S. Gibbs, T. P. Brown, J. R. Glisson, W. L.
Steffens, and J. J. Maurer. 1998. Colonization of the chicken
trachea by an avirulent avian Escherichia coli transformed
with plasmid pHK11. Avian Dis 42:194—198.
274. Wray, C. and M. J. Woodward. 1994. Laboratory diagnosis
of Escherichia coli infections. In C. L. Gyles (ed.).
Escherichia coli in Domestic Animals and Humans. CAB
Int’l: Wallingford, UK, 595—628
Coliform Cellulitis (Inflammatory Process)
Jean-Pierre Vaillancourt and H. John Barnes
INTRODUCTION
Coliform cellulitis, also known as avian cellulitis, inflam-
matory process, infectious process, or IP, is caused by
Escherichia coli and characterized by sheets of serosan-
guineous to caseated, fibrinoheterophilic exudate in sub-
cutaneous tissues. Lesions, often referred to as plaques, are
located in the skin over the abdomen or between the
thigh and midline (Figs. 18.2H, 18.6, and 18.7). Other col-
ibacillosis lesions or reduced productivity occasionally
may accompany coliform cellulitis (6, 10, 28, 39), but usu-
ally lesions are discovered at processing when inspectors
open the thickened yellow abdominal body wall of an
otherwise normal carcass. Interactions among E. coli, the
birds, and their environment contribute to the disease.
Coliform cellulitis has emerged as a significant disease
since its description in 1984 (32) because of increased con-
demnations, downgrading at processing, and higher labor
costs to process affected flocks. Between 1986 and 1996,
condemnations for coliform cellulitis increased almost 12-
fold in Canada. In 1996, more than 2.6 million broilers
were condemned for the disease, which represented 0.568%
of all birds processed and approximately 30% of total con-
demnations (17). Estimated annual losses to the U.S. broiler
industry due to coliform cellulitis have increased from $20
million in 1991 to more than $80 million in 1998 (36).
275. Xie, H., L. Newberry, F. D. Clark, W. E. Huff, G. R. Huff, J. M.
Balog, and N. C. Rath. 2002. Changes in serum ovotransfer-
rin levels in chickens with experimentally induced inflam-
mation and diseases. Avian Dis 46:122—131.
276. Yamaguchi, R., J. Tottori, K. Uchida, S. Tateyama, and S.
Sugano. 2000. Importance of Escherichia coli infection in
ascites in broiler chickens shown by experimental produc-
tion. Avian Dis 44:545—548.
277. Yang, N., C. T. Larsen, E. A. Dunnington, P. A. Geraert, M.
Picard, and P. B. Siegel. 2000. Immune competence of
chicks from two lines divergently selected for antibody
response to sheep red blood cells as affected by supplemen-
tal vitamin E. Poult Sci 79:799—803.
278. Yerushalmi, Z., N. I. Smorodinsky, M. W. Naveh, and E. Z.
Ron. 1990. Adherence pili of avian strains of Escherichia
coli O78. Infect Immun 58:1129—1131.
279. Yogaratnam, V. 1995. Analysis of the causes of high rates of
carcase rejection at a poultry processing plant. Vet Rec
137:215—217.
280. Yunis, R., A. Ben David, E. D. Heller, and A. Cahaner. 2000.
Immunocompetence and viability under commercial con-
ditions of broiler groups differing in growth rate and in
antibody response to Escherichia coli vaccine. Poultry Sci-
ence 79:810—816.
281. Zanella, A., G. L. Alborali, M. Bardotti, P. Candotti, P. F.
Guadagnini, P. A. Martino, and M. Stonfer. 2000. Severe
Escherichia coli O111 septicaemia and polyserositis in hens
at the start of lay. Avian Pathol 29:311—317.
282. Zhou, B., Y. Li, T. Wu, B. T. Zhou, Y. M. Li, and T. Wu. 1995.
Colibacillosis in quails. Chinese J Vet Sci Tech 25:34—35
ETIOLOGY
E. coli is the most frequently isolated organism from cel-
lulitis lesions and is considered the cause of coliform cel-
lulitis in chickens. Other bacteria have been found
(Pseudomonas aeruginosa, Proteus vulgaris, Enterobacter
agglomerans, Pasteurella multocida, Streptococcus dysgalac-
18.6. Coliform cellulitis lesion at processing. Skin over
the abdomen is thickened and has a yellow discol-
oration. Carcass is normal except for the skin lesion.
 CHAPTER 18 COLIBACILLOSIS Coliform Cellulitis (Inflammatory Process)
18.7. Coliform cellulitis lesion at processing. A caseous
sheet of exudate, often referred to as a plaque, is located
in the subcutaneous tissues beneath an area of thick-
ened, yellow discolored skin.
tiae, Aeromonas, etc.) but are not believed to be significant
(7, 20, 22, 32, 37, 40). E. coli isolates from cellulitis lesions
are of the same serogroups as those from birds with other
forms of colibacillosis and usually produce colicin and
aerobactin (30). Virulence properties and molecular char-
acteristics are similar among isolates from cellulitis and
colisepticemic lesions and normal birds (8, 13, 21). How-
ever, isolates from cellulitis lesions have a greater ability
to produce cellulitis in experimentally exposed birds than
E. coli isolates from airsacculitis lesions or feces of healthy
chickens (14, 31). Cellulitis-type and systemic-type strains
of avian pathogenic E. coli can be selected that cause a
predominance of either cellulitis or septicemic lesions,
respectively (12).
A vacuolating cytotoxin produced by cellulitis E. coli
isolates is also produced by isolates from chickens with
colisepticemia and swollen head syndrome but not by iso-
lates from healthy chickens. The cytotoxin is similar to
one produced by Helicobacter pylori, except H. pylori cyto-
toxin is specific for mammalian cells, and the avian E. coli
cytotoxin is specific for avian cells (34).
Initially, isolates of E. coli from litter and lesions could
not be differentiated based on biotyping, suggesting that
the litter was the source of E. coli implicated in cellulitis
lesions (5). DNA fingerprinting identified the presence of
endemic populations of specific cellulitis-associated E. coli
that exist in the broiler house environment. These organ-
isms persist for at least 6 months irrespective of partial or
complete cleaning and disinfection and cause coliform
cellulitis in successive flocks (36, 37).
EPIDEMIOLOGY
Regional differences in the prevalence of coliform cellulitis
emphasize the important roles of environmental and man-
agement factors in the occurrence of the disease. Increased
condemnation rates due to coliform cellulitis during the
past 15 years indicate that changes have occurred in either
653
the incidence or characteristics of risk factors associated
with this disease over the same period. The most notable
change during this time has been in the genotype and phe-
notype of the type of bird being raised, so it is not surprising
that bird-related factors also contribute significantly to the
incidence of scratches and subsequent coliform cellulitis.
Risk Factors
Breed. Fast-growing, heavy broiler strains are more likely
to have an increased prevalence and severity of skin
scratches, which predispose to coliform cellulitis. Several
reasons may explain this association. The strength of the
skin in broilers is related to genetics. The lack of association
between scratches and abdominal circumference suggests
that strain of bird per se could be a better predictor than
body characteristics (4). Aggressiveness or nervousness of
chickens may also be strain dependent. Birds from a more
nervous strain could be more active, increasing the chances
of being injured or scratched. If aggressiveness is a prob-
lem, the source could be farm dependent (e.g., behavioral
studies have demonstrated the importance of socialization
of the flock by the grower on the birds’ behavior) (1). Rapid
growth by modern broiler breeds results in higher stocking
density sooner in the life of the flock, at a time when feath-
ering is not yet well developed. Poor feathering and
crowded conditions could have a significant impact on the
incidence of coliform cellulitis. Breed differences in
immune response, feathering, and body conformation are
known to exist, but their possible contribution to the
occurrence of coliform cellulitis requires further studies.
Feathering. Feather coverage helps protect the skin from
damage. There is a positive association between scratches
and poor feathering (3). Birds with poor feathering have
more abdominal skin exposed for a longer period of time
than birds with good feathering. Little is known about the
nutrition and environmental factors that affect feather
growth and development.
Sex. Coliform cellulitis occurs more frequently in males
than females (2, 39). The gene responsible for sexing regu-
lates feather growth. Slower feathering males may be
more vulnerable to skin injuries because of greater expo-
sure of the skin to potential physical damage. Sex may
also contribute to coliform cellulitis because of its associa-
tion with weight, aggressiveness, or management prac-
tices. Also, production time is longer for roasters than for
broilers.
Stocking Density. Stocking density plays a dual role as a
risk factor. It leads to an increase in skin scratches (3) and
stress, but it also contributes by increasing the level of
contact between birds. Cellulitis lesions occurred more
readily when birds were palpated daily to simulate close
contact among birds (20).
Litter. Flocks grown on straw were 2.8 times more likely
to experience coliform cellulitis than flocks grown on
shavings (2). Physically, straw consists of sharp, pointed
pieces that may inflict minor injuries to the skin and pre-
654 SECTION II BACTERIAL DISEASES
dispose birds to infection. Straw may also provide a good
medium for growth and multiplication of E. coli because
of its ability to hold more moisture than shavings. Anec-
dotal clinical evidence indicates that flocks grown on very
old wood shavings litter may be severely affected with col-
iform cellulitis, but this needs to be confirmed.
Total Down time. Total down time is negatively associ-
ated with coliform cellulitis (i.e., the longer the down
time, the lower the incidence of the disease) (2). This sup-
ports the hypothesis that the bacterial load of the envi-
ronment is associated with disease prevalence.
Feed. A positive association was observed between col-
iform cellulitis and feed company in a prospective study
(2). The effect of nutrition on the pathogenic process of
the disease is not well known. Amino acid levels in the
feed may be important. Feed deficient in cysteine and
methionine can cause nervousness and affect feathering
(29, 35). A relative deficiency occurs in feeds with high
energy to total protein ratios. High-energy feeds may also
contribute to coliform cellulitis by increasing fat deposi-
tion in the skin, which may result in the skin being more
susceptible to scratches and injuries (35).
Occurrence of coliform cellulitis was higher in vegetar-
ian broilers compared to broilers fed feeds containing ani-
mal products. Condemnation rates for birds fed a
standard diet, which contained growth promotants,
antibiotics, and anticoccidials, was substantially lower
(0.26%) than for birds fed a vegetarian or organic feed
without additives (1.18%)(11).
Providing vitamin E at 300 mg/kg or vitamin A at
60,000 IU/kg improves the resistance of 6-week old broil-
ers against E. coli infection (38). Supplementation with
vitamin E had a variable impact on the development of
coliform cellulitis. Intermediate levels were superior to
both lower and higher levels of the vitamin (19). Birds fed
both vitamin E at 48 IU/kg and a zinc-protein complex at
40 ppm of zinc decreased the occurrence of coliform cel-
lulitis (27). Improved wound healing and immune system
potentiation by the supplements were considered respon-
sible for the beneficial effect.
PATHOBIOLOGY
Natural and Experimental Hosts
Coliform cellulitis affects chickens. Older chickens are
more likely to develop lesions of cellulitis following inoc-
ulation of scratches or subcutaneous injection than young
chickens, which tend to develop systemic disease and
experience high mortality (9, 14, 15, 18, 24, 26, 31).
Pathology
Cellulitis lesions are primarily unilateral and located on
the abdomen or thigh. Skin color varies from normal to
yellow or red-brown, and the skin may be swollen at the
site of inflammation (Fig. 18.6). The size of the lesion nor-
mally varies between 1—10 cm. (6). Scratches and scabs on
the skin overlying the lesions often can be identified.
Beneath the skin, there is subcutaneous edema, exudate,
and muscle hemorrhage. A fibrinous to caseous plaque
between the muscle and the subcutis is the characteristic
lesion (Figs. 18.2H, 18.7).
Lesions develop rapidly; exudate is visible as early as 6
hours postinfection, and the caseous plaque could be
experimentally produced within 18—24 hours postinfec-
tion. Rapid lesion development suggests that events
occurring late in the life of the flock could be important
in the development of lesions found at processing (9, 24).
When birds were inoculated experimentally with E. coli
strains isolated from coliform cellulitis lesions, the high-
est percentage of birds developing typical lesions had
been challenged only 3 days prior to processing (23).
Lesions were still present 3 weeks postinoculation (24).
High coliform cellulitis condemnation rates are not of
hatchery origin. Scratching the dorsal skin surface of older
birds and inoculating them with E. coli produces lesions
referred to as type I coliform cellulitis, which have been
thought to originate from navel infections in the hatch-
ery. Bacteria and inflammatory exudate gravitate from the
area where it originates to around the navel to reproduce
the so-called type I lesion (25). In Canada, only 1.7% of
coliform cellulitis lesions were consistent with a primary
navel infection (6).
Experimental exposure of young chickens to cellulitis
isolates of E. coli results in septicemia, death, or marked
stunting, indicating that most birds affected by E. coli in the
hatchery would either die or be culled before reaching the
processing plant (14, 15, 26). No association between celluli-
tis and the source of eggs, age of parent flocks, total bacterial
count, and coliform count in the hatchers was found (5).
Pathogenesis
Skin trauma, especially scratches, provides the main portal
of entry into the host for specific cellulitis-type E. coli pre-
sent in the litter. Applying bacteria to feather follicles from
which the feather had been pulled did not cause coliform
cellulitis. Oral feeding or swabbing the navel of young
chickens did not produce cellulitis but did result in mor-
tality, depressed growth, and other types of colibacillosis,
which was dose dependent (15). The disease is reproduced
readily by swabbing damaged skin with broth cultures or
subcutaneous inoculation (9, 14, 15, 18, 24, 26, 31).
Usually, an affected bird has only skin lesions, but con-
current lesions of systemic colibacillosis occasionally can
be found, suggesting that cellulitis may result from sys-
temic spread or, conversely, that localized lesions in the
skin can be a source for systemic disease. The latter is
inversely correlated with age (i.e., the younger the bird,
the more likely it is to develop systemic disease) (9, 14).
Lesions have been correlated with other categories of con-
demnation in which E. coli would be expected to play a
significant role (septicemia, airsacculitis, etc.) (5, 6, 8, 10,
39). Coliform cellulitis has been associated with earlier
outbreaks of colibacillosis in some flocks (30).
A positive association between cellulitis and ascites has
been shown, but in one study, it could only account for
 CHAPTER 18 COLIBACILLOSIS Coliform Cellulitis (Inflammatory Process)
10% of coliform cellulitis cases (5, 39). Ascites is a com-
mon condition in broiler chickens characterized by an
abnormally large abdomen. Because most cellulitis lesions
are located in the abdominal area, it may be that ascites is
a biological predisposing factor for cellulitis. Also, it is
possible that both conditions may share common risk fac-
tors such as rapid growth.
Valgus-varus leg deformity, characterized by lateral or
medial deviation of the distal tibiotarsus with a corre-
sponding deviation of the tarsometatarsus, occurred more
frequently in carcasses condemned for cellulitis, although
in one study, the association was weak (5, 39). Valgus-
varus deformity is considered to be the most frequent
cause of leg weakness and lameness in broiler chickens
(33). However, the association between valgus-varus
deformity and coliform cellulitis needs to be interpreted
with caution because of potential confounding with sex
and breed. Most valgus-varus deformity affects male birds,
and the incidence of coliform cellulitis can vary with
breed. Birds with valgus-varus leg deformity spend more
time lying on the floor (16), which results in greater con-
tact exposure between the skin and the E. coli present in
the litter. Also, prolonged resting by lame birds may result
in skin damage as other birds tread on them (5).
DIAGNOSIS
Cellulitis lesions are identified readily at processing, mak-
ing it possible to use condemnation results to assess con-
trol strategies. Lesions should be cultured aseptically to
determine the presence of E. coli. Currently, there is no in
vitro method to distinguish cellulitis-type isolates from
other types of the organism except by inoculation of
scratches inflicted in the skin of older chickens (preferably
greater than 3 weeks of age).
PREVENTION, CONTROL, AND TREATMENT
There is no treatment for coliform cellulitis, and eradication
of the disease will not be possible because of the ubiquitous
occurrence of E. coli. However, by carefully managing the
environment and nutrition of the modern, fast-growing,
heavy broiler, it is possible to substantially reduce the inci-
dence and impact of the disease. A key aspect of any control
strategy is its cost-benefit. Adequate monitoring to ensure
implementation and compliance of control strategies will
be needed to determine what is feasible. Interventions
modifying the risk factors described previously can be envi-
sioned, but the challenge will be to determine whether they
are cost-effective. Following are some recommendations.
Time of Occurrence
Very early lesions consist mainly of serosanguineous fluid
in contrast to the caseous lesions observed after 24 hours
post-infection. When increased coliform cellulitis con-
demnations occur, it is important to determine the type
of lesions (acute or chronic) found in the condemned
birds. A high prevalence of acute lesions indicate that
655
events occurring just prior to or during transportation
should be investigated, especially if at least 10 hours exists
between load-out and processing. In contrast, a majority
of chronic lesions would indicate the need to focus on
earlier events that occurred during the grow-out period.
Identify Risk Factors
Contrast problem flocks with flocks that did well during
the same time period within the same company and
determine the risk factors for each type of flock. Any man-
agement or environmental factors that affect the bird’s
resistance or contribute to skin scratches should be identi-
fied. Pay special attention to stocking density, feeder and
waterer space (effective space, i.e., in some houses, the
space is available, but the drinkers or feeders are not all
functional), type of litter, quality of litter (high moisture
content leads to high levels of ammonia that may affect
the bird’s resistance, including skin vulnerability), and
feed restriction and lighting programs. Any intervention
must first focus on improving the environment of the
birds. This includes good sanitation to reduce the bacter-
ial load of the environment.
Monitor and Review Control Strategies
The best plan will fail if it is not fully implemented. Non-
compliance is a key issue in health-related fields. Before
judging the efficacy of a prevention measure, it is impor-
tant to make sure that it was properly implemented.
REFERENCES
1. Duncan, I. J. H. 1990. Reactions of poultry to human
beings. In R. Zayan and R. Dantzer (eds.). Social Stress in
Domestic Animals. Kluwer Academic Publishers: Dordrecht,
Netherlands, 121—131
2. Elfadil, A. A., J. P. Vaillancourt, and A. H. Meek. 1996. Farm
management risk factors associated with cellulitis in broiler
chickens in southern Ontario. Avian Dis 40:699—706.
3. Elfadil, A. A., J. P. Vaillancourt, and A. H. Meek. 1996.
Impact of stocking density, breed, and feathering on the
prevalence of abdominal skin scratches in broiler chickens.
Avian Dis 40:546—552.
4. Elfadil, A. A., J. P. Vaillancourt, and I. J. H. Duncan. 1998.
Comparative study of body characteristics of different
strains of broiler chickens. J Appl Poult Res 7:268—272.
5. Elfadil, A. A., J. P. Vaillancourt, A. H. Meek, and C. L. Gyles.
1996. A prospective study of cellulitis in broiler chickens in
southern Ontario. Avian Dis 40:677—689.
6. Elfadil, A. A., J. P. Vaillancourt, A. H. Meek, R. J. Julian, and
C. L. Gyles. 1996. Description of cellulitis lesions and asso-
ciations between cellulitis and other categories of condem-
nation. Avian Dis 40:690—698.
7. Glunder, G. 1990. Dermatitis in broilers caused by
Escherichia coli: isolation of Escherichia coli field cases,
reproduction of the disease with Escherichia coli O78:K80
and conclusions under consideration of predisposing fac-
tors. J Vet Med B 37:383—391.
8. Gomis, S. M., C. Riddell, A. A. Potter, and B. J. Allan. 2001.
Phenotypic and genotypic characterization of virulence fac-
tors of Escherichia coli isolated from broiler chickens with
simultaneous occurrence of cellulitis and other colibacillo-
sis lesions. Can J Vet Res 65:1—6.
656 SECTION II BACTERIAL DISEASES
9. Gomis, S. M., T. Watts, C. Riddell, A. A. Potter, and B. J. Allan.
1997. Experimental reproduction of Escherichia coli cellulitis
and septicemia in broiler chickens. Avian Dis 41:234—240.
10. Gomis, S. M., R. Goodhope, L. Kumor, N. Caddy, C. Riddell,
A. A. Potter, and B. J. Allan. 1997. Isolation of Escherichia
coli from cellulitis and other lesions of the same bird in
broilers at slaughter. Can Vet J 38:159—162.
11. Herenda, D. and O. Jakel. 1994. Poultry abattoir survey of
carcass condemnation for standard, vegetarian, and free
range chickens. Can Vet J 35:293—296.
12. Jeffrey, J. S., R. P. Chin, and R. S. Singer. 1999. Assessing cel-
lulitis pathogenicity of Escherichia coli isolates in broiler
chickens assessed by an in vivo inoculation model. Avian
Dis 43:491—496.
13. Jeffrey, J. S., L. K. Nolan, K. H. Tonooka, S. Wolfe, C. W. Gid-
dings, S. M. Horne, S. L. Foley, A. M. Lynne, J. O. Ebert, L.
M. Elijah, G. Bjorklund, S. J. Pfaff-McDonough, R. S. Singer,
and C. Doetkott. 2002. Virulence factors of Escherichia coli
from cellulitis or colisepticemia lesions in chickens. Avian
Dis 46:48—52.
14. Johnson, L. C., S. F. Bilgili, F. J. Hoerr, B. L. McMurtrey, and
R. A. Norton. 2001. The influence of Escherichia coli strains
from different sources and the age of broiler chickens on
the development of cellulitis. Avian Pathol 30:475—479.
15. Johnson, L. C., S. F. Bilgili, F. J. Hoerr, B. L. McMurtrey, and
R. A. Norton. 2001. The effects of early exposure of celluli-
tis-associated Escherichia coli in 1-day-old broiler chickens.
Avian Pathol 30:175—178.
16. Julian, R. J. 1984. Valgus-varus deformity of the intertarsal
joint in broiler chickens. Can Vet J 25:254—258.
17. Kumor, L. W., A. A. Olkowski, S. M. Gomis, and B. J. Allan.
1998. Cellulitis in broiler chickens: epidemiological trends,
meat hygiene, and possible human health implications.
Avian Dis 42:285—291.
18. Macklin, K. S., R. A. Norton, and B. L. McMurtrey. 1999.
Scratches as a component in the pathogenesis of avian cel-
lulitis in broiler chickens exposed to cellulitis origin
Escherichia coli isolates collected from different regions of
the US. Avian Pathol 28:573—578.
19. Macklin, K. S., R. A. Norton, J. B. Hess, and S. F. Bilgili.
2000. The effect of vitamin E on cellulitis in broiler chick-
ens experiencing scratches in a challenge model. Avian Dis
44:701—705.
20. Messier, S., S. Quessy, Y. Robinson, L. A. Devriese, J. Hom-
mez, and J. M. Fairbrother. 1993. Focal dermatitis and cel-
lulitis in broiler chickens: bacteriological and pathological
findings. Avian Dis 37:839—844.
21. Ngeleka, M., J. K. Kwaga, D. G. White, T. S. Whittam, C.
Riddell, R. Goodhope, A. A. Potter, and B. Allan. 1996.
Escherichia coli cellulitis in broiler chickens: clonal rela-
tionships among strains and analysis of virulence-associ-
ated factors of isolates from diseased birds. Infect Immun
64:3118—3126.
22. Norton, R. A. 1998. Inflammatory process in broiler chick-
ens—a review and update. 33rd Natl Mtg Poult Hlth & Proc:
Ocean City, MD, Oct 14—16, 52—55.
23. Norton, R. A. and K. S. Macklin. 2000. Development and
persistence of lesions in young broiler chicks challenged
with cellulitis origin Escherichia coli. Proc 21st World’s
Poultry Congress: Montréal, Canada, Aug. 20—24.
24. Norton, R. A., S. F. Bilgili, and B. C. McMurtrey. 1997. A
reproducible model for the induction of avian cellulitis in
broiler chickens. Avian Dis 41:422—428.
25. Norton, R. A., K. S. Macklin, and B. L. McMurtrey. 1999.
Evaluation of scratches as an essential element in the devel-
opment of avian cellulitis in broiler chickens. Avian Dis
43:320—325.
26. Norton, R. A., K. S. Macklin, and B. L. McMurtrey. 2000.
The association of various isolates of Escherichia coli from
the United States with induced cellulitis and colibacillosis
in young broiler chickens. Avian Pathol 29:571—574.
27. Norton, R. A., J. B. Hess, K. M. Downs, and K. S. Macklin.
2000. Strategies for the reduction of cellulitis in broiler
chickens. Proc 21st World’s Poultry Congress: Montréal,
Canada, Aug. 20—24.
28. Onderka, D. K., J. A. Hanson, K. R. McMillan, and B. Allan.
1997. Escherichia coli associated cellulitis in broilers: corre-
lation with systemic infection and microscopic visceral
lesions, and evaluation for skin trimming. Avian Dis
41:935—940.
29. Patel, M. B., K. O. Bishawi, C. W. Nam, and J. McGinnis.
1980. Effect of drug additives and type of diet on methion-
ine requirement for growth, feed efficiency, and feathering
of broilers reared in floor pens. Poult Sci 59:2111—2120.
30. Peighambari, S. M., J. P. Vaillancourt, R. A. Wilson, and C.
L. Gyles. 1995. Characteristics of Escherichia coli isolates
from avian cellulitis. Avian Dis 39:116—124.
31. Peighambari, S. M., R. J. Julian, J. P. Vaillancourt, and C. L.
Gyles. 1995. Escherichia coli cellulitis: Experimental infec-
tions in broiler chickens. Avian Dis 39:125—134.
32. Randall, C. J., P. A. Meakins, M. P. Harris, and D. J. Watt.
1984. A new skin disease in broilers? Vet Rec 114:246.
33. Riddell, C. 2000. Management of skeletal disease, 2000.
Proc 21st World’s Poultry CongressL Montréal, Canada,
Aug. 20—24.
34. Salvadori, M. R., T. Yano, H. F. Carvalho, V. R. Parreira, and
C. L. Gyles. 2001. Vacuolating cytotoxin produced by avian
pathogenic Escherichia coli. Avian Dis 45:43—51.
35. Schleifer, J. 1988. Costly skin tear problem has several
major causes. Poult Digest 580—586.
36. Singer, R. S., J. S. Jeffrey, T. E. Carpenter, C. L. Cooke, R. P.
Chin, E. R. Atwill, and D. C. Hirsh. 1999. Spatial hetero-
geneity of Escherichia coli DNA fingerprints isolated from
cellulitis lesions in chickens. Avian Dis 43:756—762.
37. Singer, R. S., J. S. Jeffrey, T. E. Carpenter, C. L. Cooke, E. R.
Atwill, W. O. Johnson, and D. C. Hirsh. 2000. Persistence of
cellulitis-associated Escherichia coli DNA fingerprints in
successive broiler chicken flocks. Vet Microbiol 75:59—71.
38. Tengerdy, R. P. and C. F. Nockels. 1975. Vitamin E or vita-
min A protects chickens against E. coli infection. Poult Sci
54:1292—1296.
39. Tessier, M., M. A. Fredette, G. Beauchamp, and M. Boulianne.
2001. Cellulitis in broiler chickens: A one-year retrospective
study in four Quebec abattoirs. Avian Dis 45:191—194.
40. Valentin, A. and K. Willsch. 1987. Etiology and pathogene-
sis of deep dermatitis in broiler fowl. Monat Veterinarmed
42:708—711.