Advanced Topics on Zoonoses

Chao-chin Chang, DVM, MS, PhD

Professor
Graduate Institute of Microbiology and Public Health
National Chung Hsing University
Taichung, Taiwan

Figure. The host-parasite

ecological continuum
(here parasites include
viruses and parasitic
prokaryotes).
Daszak P et al., Emerging
infectious diseases of
wildlife--threats to
biodiversity and human
health. Science
2000;287(5452):443-9

Published by AAAS

BITE-ASSOCIATED
ZOONOSES

Introduction
Animal bites represent about 1% of all emergency
department visits. Between 70% and 90% of these
visits are caused by dog bites (Tan, 1997) .
It is estimated that only 3% to 5% of dog bites will
become infected.
Most infections associated with dog bites are
polymicrobial, with Staphylococcus spp.,
Streptococcus spp., and Corynebacterium spp. as
the most frequently isolated aerobic organisms
(Griege et al., 1995).
However, bite-related zoonotic bacteria mainly
include Pasteurella species and Capnocytophaga
canimorsus.

Zhang et al., Emerg Infect Dis 2009;15:946-949

Distribution of human rabies cases in mainland China, 2007.

Red stars indicate ferret badgerassociated human rabies cases.
Numbers in parentheses in key indicate number of affected provinces.

Dog and Cat Bites

Aerobes

Anaerobes

Cat bites

Pasteurella spp,
Streptococcus spp,
Staphylococcus spp,
Moraxella spp

Fusobacterium spp,
Bacteroides spp,
Porphyromonas spp
Capnocytophaga spp

Dog bites

Pasteurella spp,
Streptococcus spp,
Staphylococcus spp,
Neisseria spp

Fusobacterium spp,
Bacteroides spp,
Porphyromonas spp,
Prevotella spp,
Capnocytophaga spp

Pasteurellosis

Pasteurella are commensal bacteria isolated from the oral cavity of

dogs and cats.
Carriage rates of Pasteurella in dogs: 22% to 81% (but Ganire et al.
(1993) indicated that pathogenic strains were found in 28% of the dogs
tested (versus 77% of the cats).
Pasteurella canis is the most common isolate from dog bites and
Pasteurella multocida subspecies multocida and P. septica were the
most common isolates from cat bites (Talan et al., 1999).
Penicillin is the antibiotic of choice for treatment, but most patients are
more frequently treated with a combination of a -lactam antibiotic and
a -lactamase inhibitor (Talan et al., 1999). Usually, dog bite treatment
includes the adminstration of Amoxicillin-clavulanate (250 mg orally 3
times a day).
Untreated affection can lead to severe complications, including abscess
formation, septic arthritis, osteomyelitis, endocarditis, pneumonia or
meningitis (Griego et al., 1995).

Dog & Cat Bites: Pasteurellosis

Infectious agent:
Most common species are Pasteurella canis
and Pasteurella multocida
Commensal organism within the oral cavity
of the dog
Gram negative, facultative anaerobe,
coccobacillus

Clinical signs
Swelling, inflammation and
intense pain at the bite site a
few hours after the exposure
are the typical symptoms of
Pasteurella infection.
Dog: skin abscesses, arthritis, otitis

Capnocytophaga canimorsus

A gram-negative rod, is reported as part of the normal oral flora of

16% of dogs (Underman, 1987).
Most (91%) of the known bite-related human cases resulted from a dog
bite (Lion et al., 1996).
C. canimorsus systemic infections occur more often in
immunosuppressed or immuno-impaired individuals, such as
splenectomised individuals (33%), alcohol abuse (24%) or
immunosuppression (5%). Therefore, when fever occurs in
immunosuppressed patients after a dog bite, C. canimorsus infection
should be considered.

Dog Bites Capnocytophaga canimorsus

Clinical signs
. No major sign in non-immunocompromised patients
. Septicemia, shock, disseminated intravascular coagulation
in immuno-compromised patients

Clinical features
Fever (90%), septicemia (94%),
septic shock (40%),
disseminated intravascular coagulation (32%),
meningitis (13%), renal failure (15%),
gangrene (14%),
thrombocytopenic purpura (14%),
cardiopathy (11%), ARDS/Pneumonia (10-12%),
endocarditis (7%).
Case-fatality rate: 30%

Dog Bites Capnocytophaga canimorsus

Underlying Conditions and Fatality Rates (n=81)
Category

Condition Cases (%) Fatalities (%)

Age

> 50 yrs

42

(52)

17

(40)

Underlying

Total

57

(70)

18

(32)

Condition

Splenectomy 29

(36)

10

(34)

Neoplastic

20

(25)

(30)

Alcoholism

16

(20)

(25)

Pulmonary

13

(16)

(46)

Cardiovascul. 5

( 6)

(40)

Steroid use

( 6)

(20)

Purpura fulminans associated with Capnocytophaga canimorsus infection.

Bryson et al. British Journal of Haematology 2003;121:1.
**C. canimorsus is susceptible to most antibiotics, and penicillin G is recommended as the drug of choice (Lion et
al. (1999). The use of amoxicillin/clavulanic acid is a good alternative.

Dog Bites: Other bugs

Epidemiology

Staphylococcus sp., Streptococcus sp.

Corynebacterium sp. Proteus sp.
Bacillus sp.

Prevention

They are commensal organisms, so

they can only be prevented by
avoiding dog bites and cleaning any
wound thoroughly.

MRSA-associated infection
of the left forearm of a 15year-old
patient (A) whose cat had
developed recurrent MRSA
culture-positive skin
lesions of the perineal area
(B)
Source: Oehler et al.
Lancet Infect Dis
2009;9:439447.

GASTRO-INTESTINAL
ZOONOSES

Campylobacteriosis

Campylobacter jejuni, a Gram-negative enteric organism, is a leading

cause of human enteritis.
Campylobacteriosis has a higher incidence in AIDS patients than in the
general population, causing severe, often bloody, diarrhea and
cramping, nausea and fever (Glaser et al., 1994).
It is estimated that approximately 6% of enteric campylobacteriosis is
transmitted from pet animals (Saeed et al., 1993).
Most Campylobacter infections in dog and man are caused by C. jejuni,
though C. coli infection does occur.
Evidence indicates that contact with infected dogs, especially diarrheic
dogs can increase risk of acquiring Campylobacter jejuni (Blaser et al.,
1978; Salfield and Pugh, 1987).

Campylobacteriosis (cont.)

Puppies are more likely to acquire the infection and show clinical signs
(watery diarrhea lasting 3 to 7 days).
In dogs, symptomatic puppies usually show a 3- to 7-day course of
diarrhea with or without anorexia, fever and vomiting (Willard et al.,
1987). The diarrhea may be watery, mucoid, or bloody. Infected dogs
may or may not show clinical signs of disease.
Risk factors associated with non-clinical shedding include high density
housing, age less than six months, and autumn seasonality.
Fecal shedding of C. jejuni in the dog is age-dependent and peaks in
the first year of life.
In humans, the clinical picture of Campylobacter infection is a brutal
onset of fever, headache, abdominal pain and severe watery to bloody
diarrhea usually lasting less than a week. Rare cases of relapse, colitis,
arthritis and septicemia have been reported.

Helicobacter infections
The bacterial genus Helicobacter contains at least 18
species.
Some helicobacters, such as H. canis, H. pullorum, H.
heilmannii, and H. cinaedi may be zoonotic.
H. pylori ??
Helicobacter species have been involved in human
peptic ulcer and neoplasia, enteritis and inflammatory
bowel disease.
Chronic vomiting and subclinical gastritis are the
main manifestations of dog infection with
Helicobacter (McDonough and Simpson, 1996).

Salmonella Infections
Typhoidal Salmonella infection
-- S. Typhi, S. Paratyphi
Non-typhoidal Salmonella infection

Non-typhoidal Salmonella serovars vs. Host

Cattle S. Typhimurium, S. Dublin, S. Newport

Sheep S. Typhimurium, S. Dublin, S. Anatum, S.
Montevideo
Pigs S. Typhimurium, S. Choleraesuis
Horse S. Typhimurium, S. Anatum, S. Newport, S.
Enteritidis, S. Arizonae
Chickeni) Pullorum disease: S. Pullorum; ii) Fowl
typhoid: S. Gallinarum; ii)Avian paratyphoid: S.
Typhimurium, S. Enteritidis, S. Heidelberg
20

Salmonellosis

It has been estimated that 1% of the 40,000 annually-reported

salmonellosis cases in the United States are associated with companion
animals (Stehr-Green and Schantz, 1987).
From 1% to 30% of the fecal samples or rectal swabs taken from
healthy domestic pet dogs, 16.7% of dogs boarded in kennels, and
21.5% of dogs hospitalized were found to be positive on
bacteriological culture for Salmonella (McDonough and Simpson,
1996).
Young dogs (<6 months of age) may have higher prevalences than
older dogs and dogs may shed more than one serotype in their feces
(Willard et al., 1987).
However, transmission of Salmonella species from dogs to humans is
rare (Tan, 1997).

Salmonellosis

Salmonellosis causes clinical signs mainly in young puppies, pregnant

animals or aging dogs.

Main clinical signs, after an incubation of 3 to 5 days, include diarrhea,

fever, vomiting, malaise, anorexia, dehydration, and possible vaginal
discharge or abortion in bitches.
Mortality is usually low (< 10%).
Recovering dogs may have intermittent diarrhea for up to 3 to 4 weeks
and can shed Salmonella in the stools for up to 6 weeks (McDonough
and Simpson, 1996; Willard et al., 1987).
In humans, gastroenteritis with fever, vomiting, abdominal pain and
watery to mucoid diarrhea occurs within a few hours to 2 to 3 days
after exposure to infection.

Prevalence and antimicrobial susceptibility of

salmonellae isolates from reptiles in Taiwan.
Chen C.Y., Chen W.C., Chin S.C., Lai Y.H., Tung K.C.,
Chiou C.S., Hsu Y.M., Chang C.C.*
J Vet Diagn Invest 2010;22:44-50.

Table 1. Reports of Salmonella infection in reptiles in different countries.

Country

Species

German and Austrian

Turtle

Reference
[Geue L and Lschner U, 2002]

Total

S. Newport
47.4 % (36/76) S. Othmarschen
S. Nottingham
71.6 % (48/67)
Salmonella b 47:k:z35
54.1 % (86/159) Salmonella b 50:k:z

Turtle

72.2 % (13/18)

[Nakadai et al., 2005]

Snake

Total

S. Bardo
66.1 % (47/71) S. Newport
S. Panama
100.0 % (23/23)
S. Amsterdam
74.1 % (83/112) S. Minnesota

Turtle

25.8 % (15/58)

Lizard

62.5 % (15/24)

Snake

53.3 % (8/15)

Total

39.1 % (38/97)

Lizard
Snake

Brazilian

Serotypes

2.6 % (1/38)

Lizard

Japan

Prevalence

Salmonella b 60:r:z
S. Typhimurium
S. Enteritidis
S. Albany

[De S IVA and Solari-Braz CA,

2001]

Table 1. Reports of Salmonella infection in reptiles in different countries. (cont.)

Country
Spain

Species
Turtle

32.4 %

Lizard

40.9 %

Snake

54.3 %

Total

41.5 % (39/94)

Amphibian
Italy

Prevalence

Serotypes

Reference

S. Anatum
S. Herzliya
S. Abony
Salmonella b 18:l,v:z
Salmonella 9,12:z29:1,5

[Briones et al., 2004]

S. Berta
Salmonella 44:z4,z23:S. Fluntern
S. Trimdon
S. Apapa

[Ebani et al., 2005]

0.0 % (0/72)

Turtle

36.6 %

Lizard

26.7 %

Snake

14.1 %

Total

23.9 % (73/305)

Table 2. Prevalence (%) of Salmonella infection in pet reptiles in Taiwan.

Source
Zoo

Lizard

22.3 % (81/364) 57.1 % (16/28)

Snake

p value

Total

61.5 % (16/26)

< 0.05

27.0 % (113/418)

Hospital

39.4 % (13/33)

40.0 % (2/5)

NS

39.5 % (15/38)

Pet shop

100.0 % (3/3)

90.0 % (9/10)

100.0 % (7/7)

NS

95.0 % (19/20)

p value

< 0.05

NS

NS

Total

Turtle

24.3 % (97/400) 62.8 % (27/43)

69.7 % (23/33)

< 0.05
< 0.05

30.9 % (147/476)

by Chi-Square test
The comparison of isolation prevalence among different reptile orders from the same collection source.

The comparison of isolation prevalence among different collection sources in a reptile order.

NS: not significant by Chi-square test

Identification of several Salmonella serotypes that

were common in humans in the USA.

40.0

35.0

B
Percentage

C2

C1

30.0

D1

35.2

K M N O 50 51

51

25.0

Typhimurium
20.0

B
4,[5],12:i:Infantis

Saintpaul
15.0
10.0

Muenchen
C

C2

Newport
8.9

7.3
5.0

5.0
1.1

N O

D1 H

1.1 1.1 0.8

5.0

3.9

2.5
0.6

0.6 0.6 0.6

2.0
1.7 1.1
1.7 1.7
1.7
1.7
0.6
0.6
0.6
0.3 1.1

2.8 2.8
1.1 0.6

2.5
0.3

1.1

Ja
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ef
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0.0

Serotype

Figure 2. Percentages of Salmonella serotypes in pet reptiles in Taiwan.

Identification of several Salmonella serotypes that have been ever

reported in human cases in Taiwan. (CDC in Taiwan 2004,
unpublished data)

40.0

35.0

C1

Percentage

30.0

C2

D1

35.2

K M N O 50 51

51

25.0

Typhimurium
20.0
15.0

B Bareilly

Java Stanely

Infantis

C1

C2

N O

D1 H

Newport

10.0

8.9

7.3
5.0

5.0
1.1

1.1 1.1 0.8

5.0

3.9

2.5
0.6

0.6 0.6 0.6

2.0
1.7 1.1
1.7 1.7
1.7
1.7
0.6
0.6
0.6
0.3 1.1

2.8 2.8
1.1 0.6

2.5
0.3

1.1

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6
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0.0

Serotype

Figure 2. Percentages of Salmonella serotypes in pet reptiles in Taiwan.

Table 3. Association of Salmonella infection and risk factors.

Risk factor

Prevalence

p value

Carnivorous

66.0 % (31/47)

< 0.05

Omnivorous

42.9 % (42/98)

Herbivorous

21.7 % (68/313)

Unknown

33.3 % (6/18)

Feeding Habits

Raising condition
Group raising

25.0 % (93/360)

Individual raising

50.0 % (39/78)

< 0.05

Living environment
Aqua turtle

40.3 % (29/72)

Tortoise

20.8 % (68/327)

< 0.05

Healthy status

by

Healthy

30.0 % (112/373)

Ill

34.0 % (35/103)

Chi-Square test
NS: not significant by Chi-Square test
Analysis for turtles only

NS

Table 11. Antimicrobial-resistant pattern of the 347 Salmonella isolates.

Antimicrobial-resistant pattern
None (susceptible to all antimicrobials)
S
AMP KF C CN NA S SXT TE
AMP C S TE
AMP KF C CN NA F S SXT TE
NA
C NA F SXT TE
AMP S TE
C NA F TE
F S TE
SXT TE
AMP KF ENR S
AMP KF F TE
AMP KF TE
AMP KF
AMP TE
KF
F
S TE
Total
SerogroupsSerotypes

SerogroupsSerotypes

S. Typhimurium
S. Typhimurium
S. Typhimurium
S. Stanley
S. Stanley
UT
S. Stanley
serogroup C1 (UT)
S. Infantis
serogroup W (UT)
serogroup 53 (UT)
UT
UT
serogroup U (UT)
S. Rubislaw
UT
S. Gatow

No. of isolates

Percentage

279
28
6
6
5
4
3
2
2
2
2
1
1
1
1
1
1
1
1
347

80.4 %
8.1 %
1.7 %
1.7 %
1.4 %
1.2 %
0.9 %
0.6 %
0.6 %
0.6 %
0.6 %
0.3 %
0.3 %
0.3 %
0.3 %
0.3 %
0.3 %
0.3 %
0.3 %
100.0 %

of resistance to streptomycinS. Bredeney (2)S. Muenchen (1)S. Fayed (1)S. Panama (1)
S. Treforest (2)S. Poona (1)4,[5],12:i:- (2)serogroup C2 (UT) (1)serogroup F (UT) (3)serogroup G (UT) (2)
serogroup I (UT) (1)serogroup N (UT) (2)serogroup X (UT) (1)serogroup V (UT) (4)serogroup 64 (UT) (1)UT (3)
UTuntypable

Table 12. The comparison of percentages of Antimicrobial resistance of different

Salmonella serotypes isolated from pet reptiles.
Antimicrobial
agent

S. Heron

S. Bredeney

S. Typhimurium

S. Treforest

4,[5],12:i:-

Ampicillin

0.0 % (0/32)

0.0 % (0/26)

83.3 % (15/18)

0.0 % (0/18)

0.0 % (0/13)

Cephalothin

0.0 % (0/32)

0.0 % (0/26)

61.1 % (11/18)

0.0 % (0/18)

0.0 % (0/13)

Chloramphenicol

0.0 % (0/32)

0.0 % (0/26)

83.3 % (15/18)

0.0 % (0/18)

0.0 % (0/13)

Ciprofloxacin

0.0 % (0/32)

0.0 % (0/26)

0.0 % (0/18)

0.0 % (0/18)

0.0 % (0/13)

Enrofloxacin

0.0 % (0/32)

0.0 % (0/26)

0.0 % (0/18)

0.0 % (0/18)

0.0 % (0/13)

Gentamicin

0.0 % (0/32)

0.0 % (0/26)

61.1 % (11/18)

0.0 % (0/18)

0.0 % (0/13)

Nalidixic acid

0.0 % (0/32)

0.0 % (0/26)

61.1 % (11/18)

0.0 % (0/18)

0.0 % (0/13)

Nitrofurantoin

0.0 % (0/32)

0.0 % (0/26)

27.8 % (5/18)

0.0 % (0/18)

0.0 % (0/13)

Norfloxacin

0.0 % (0/32)

0.0 % (0/26)

0.0 % (0/18)

0.0 % (0/18)

0.0 % (0/13)

Streptomycin

3.1 % (1/32)

7.7 % (2/26)

83.3 % (15/18)

11.1 % (2/18)

15.4 % (2/13)

Trimethoprimsulfamethoxazole

0.0 % (0/32)

0.0 % (0/26)

61.1 % (11/18)

0.0 % (0/18)

0.0 % (0/13)

Tetracycline

0.0 % (0/32)

0.0 % (0/26)

83.3 % (15/18)

0.0 % (0/18)

0.0 % (0/13)

Salmonellosis
Treatment is usually supportive rather than
antimicrobial, as antibiotics have been shown
capable of extending the period of shedding and
triggering systemic disease (Willard et al., 1987).

Salmonella in pigs and humans

in Taiwan

In Taiwan, the prevalence of 1.7% was determined, and the

four most frequently isolated Salmonella serotypes were
Derby (34%), Anatum (22%), Typhimurium (11%), and
Schwarzengrund (9%), according to a large-scale
screening program in pork carcasses in 2000-2003.
Chen TH et al., J Food Prot 69:674-678.

However, serotypes commonly seen in humans were

Typhimurium, Enteritidis, Stanley, Choleraesuis and
Derby (CDC, personal communication).

33

Transmission

Usually by fecal-oral route

Animals can become infected through contaminated feed,
pasture, water or close contact with an infected host.
Humans and carnivores can be infected through meat, milk,
eggs and other animal products that are not thoroughly cooked.
Salmonella can be spread by fomites, rodents and wild birds, but
vectors are not required (??).
Salmonella can persist for months or years in the environment,
particularly in wet and warm environment.
S. Choleraesuis can survive in pig meat for up to 450 days and
for several months in feces.
Animals may become carriers for months to years.
34

S. Choleraesuis in Pigs (Clinical Signs)

The disease is generally seen in pigs 3 weeks to 5 months

of age
Piglets are reluctant to move, anorexic, with high
temperature 40.5-41.6oC.
Piglets may have a shallow cough.
Yellow soft feces may be seen in diseased animals after a
couple of days of infection.
Septicemic salmonellosis is often associated with S.
Choleraesuis.

35

S. Choleraesuis in Pigs
(Post-mortem Lesions)

Cyanosis of the ears, feet, tail and abdomen

Enlarged spleen
Congested lungs possibly with interlobular edema
Liver with white foci of necrosis
If the pigs survive the initial stages, it may present with
necrotic enterocolitis

36

S. Choleraesuis in Humans
(J. Microbiol Immunol Infect 37(2):99-102)

Males : females = 2.2 : 1

56% of the patients are aged over 60 years old.
78% of the patients were with underlying diseases, such as
D.M., malignancy, peptic ulcer.
78% of the patients developed septicemia.
Gastro-intestinal manifestations (nausea/diarrhea) were
observed only in 11%~13% of the patients.
Case-fatality rate: 18%
Most feared complication in adult is mycotic aneurysm.

37

II) The Use of Antibiotics in Food Animals

in Taiwan

38

J Microbiol Immunol Infect 2001;34:97-102

The Use of Antibiotics Critical to Human

Medicine in Food-Producing Animals in
Taiwan
McDonald LC, Chen MT, Lauderdale TL, Ho M.

39

Main Findings

Five animal drugs and the resistance of human drug/class they may select
for, included avoparcin, avilomycin, enrofloxacin, virginiamycin, and
kanamycin.
Tetracyclines were the class of antibiotic that was most widely used in the
greatest amount.
Farms(10)

Chicken feed mills(8)

Pig feed mills (6)

Avoparcin

10%

63%

0%

Avilomycin

0%

0%

50%

Enrofloxacin

40%

13%

50%

Virginiamycin

20%

63%

0%

Kanamycin

30%

13%

17%

III) Identification of Fluoroquinoloneresistant Salmonella enterica serovar

Choleraesuis in Taiwan

41

New Engl J Med 2002;346(6):413-419

The Emergence in Taiwan of

Fluoroquinolone Resistance
in Salmonella enterica serotype Choleraesuis
Chiu CH, Wu TL, Su LH, Chu CS, Chia JH,
Kuo AJ, Chien MS, Lin TY

42

Main Findings

The proportion of total salmonella isolates made up by S.

enterica serotype Choleraesuis:
Before 1995: 8.4%
1996~1998: 2.7%
1999-2000: 5%
Ciprofloxacin-resistant S. Choleraesuis has been observed
since 2000.
In the third quarter of 2001, 60% of the isolates were
resistant ciprofloxacin.
All the resistant isolates from humans and swine has
mutations that led to the substitution of Ser83Phe and
Asp87Asn.

43

Introduction (contd)

Figure 1. Emergence of Fluoroquinolone Resistance among Salmonella enterica

Serotype Choleraesuis Isolates in Taiwan.Panel A shows the total annual numbers
of salmonella isolates from Chang Gung Memorial Hospital and Chang Gung
Childrens Hospital from 1987 through 2000 (bars) and the percentage of these
44
isolates that were S. enterica serotype choleraesuis (curve).
(Chiu et al. 2002)

Introduction (contd)

Figure 1. Emergence of Fluoroquinolone Resistance among Salmonella enterica

Serotype Choleraesuis Isolates in Taiwan. Panel B shows the total quarterly
numbers of S. enterica serotype choleraesuis isolates from these hospitals from the
fourth quarter of 1996 through the third quarter of 2001 (bars) and the percentage
45
of these isolates that were resistant to ciprofloxacin (curve).
(Chiu et al. 2002)

Judgment of Cause-effect Relationship

Correct temporality
Strength of association
Consistency of association
Specificity of association
Biological plausibility
Dose-response relationship

46

Journal of Clinical Microbiology 2005;43(6):2798-2804.

Epidemiologic Relationship between

Fluoroquinolone-resistant Salmonella
enterica serovar Choleraesuis from Humans
and Pigs in Taiwan, 1997-2002
Chao-chin Chang, Yi-Hsuan Lin, Chao-Fu Chang, Kuang-Sheng
Yeh, Cheng-Hsun Chiu, Chishih Chu, Maw-Sheng Chien, YuanMan Hsu, Li-Shu Tsai, Chien-Shun Chiou*

47

Results

48

A total of
24 PFGE patterns

FIG 1. Dendrogram and PFGE patterns of Xba I-digested chromosomal DNA of Salmonella enterica serovar Choleraesuis and the numb
of isolates from pig and human origins. The dendrogram was constructed by the UPGMA algorithm and the Dice similarity using
BioNumerics software with 3% optimization and 1% position tolerance.

A total of 44 patterns
FIG 2. Dendrogram and the
antibiograms of 12 antimicrobials
for the 106 gt-1a Salmonella
enterica serovar Choleraesuis
isolates and the number of isolates
from pig and human origins. Am:
ampicillin, C: chloramphenicol, S:
streptomycin, SxT: trimethoprimsulfamethoxazole, Te: tetracycline,
Cip: ciprofloxacin, Na: nalidixic
acid, Nor: norfloxacin, Eno:
enrofloxacin, Cf: cephalothin, Gm:
gentamicin, F/m: nitrofurantoin

: resistant
: intermediate
: susceptible

52% of the isolates were resistant to more than 7 antimicrobials:

Humans: 76% vs Pigs: 46%

51

53

Discussion

Our findings suggested that the fluoroquinolone-resistant S.

Choleraesuis was evolved from a gt-1a clone, emerged in
2000, and then caused widely infections among humans
and pigs since after.
It is still debatable that the source of the infection in
humans was from pigs, on the basis of the higher
fluoroquinolone- and other antimicrobial-resistance
prevalences found in human isolates than in pig isolates.
Limitations of using molecular techniques to trace the
source of the infection
It is of urgent need to identify risk factors and
transmission routes of the infection in Taiwan.
54

J Antimicrobial Chemotherapy 2004;53:28-52.

Does the Use of Antibiotics in Food Animals

Pose a Risk to Human Health?
A Critical Review of Published Data
Phillips I, Casewell M, Cox T, Groot BD, Friis C,
Jones R, Nightingale C, Preston R, Waddell J

55

Main Conclusions

The low dosage used for growth promotion are an

unquantified hazard.
Although some antibiotics are used both in animals and
humans, most of the resistance problem in humans arisen
from human use.
Resistance can be selected in food animals, and resistant
bacteria can contaminate animal-derived food, but
adequate cooking destroys them.
In zoonotic salmonellosis, resistance may arise in animals
or humans, but human cross-infection is common.

56

Risk Assessment of S. Choleraesuis

Pigs with low level of
bacteremia but not
excreting the bacteria
in feces

The bacteria are in

the meat but not on
the surface of the
meat

Humans get the infection

cooking
process

drinking

Pigs with bacteremia

but without clinical
signs and
intermittently
shedding the bacteria
in feces

Contaminate
environmental
water and soil

Feces as
fertilizers
for organic
farms

eating

The bacteria
cannot be
detected by
traditional
methods

Pork products
available in
supermarkets

Vegetables contaminated
with the bacteria

57

Modeling the Transmission Dynamics of

Fluoroquinolone-Resistant Salmonella
between Pigs and Humans in Taiwan.

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

a*

*(V+Z+Y)*(1-)

*(V+Z+Y)*(1-)

a*

Materials & Methods

dU
dt

=V-[ a* + (V+Z+Y)(1-)]*U

dV
dt

= [ a*+(V+Z+Y)(1-)]*U *V

Prevalence of FQR S. Choleraesuis in pigs (Pa) = 1-U = V

Materials & Methods

dW
dt =Z+Y+X-[V+(V+Z+Y)(1-) +Y+Z]*W
dX
dt = [V+(V+Z+Y)(1-) +Y+Z]*W- (++a*)*X
dY
dt

=X- (+a*)*Y

dZ
dt = a*(X+Y)- Z

Prevalence of FQR S. Choleraesuis in humans (Ph) = 1-W = X+Y+Z

Materials & Methods

Parameter

Estimate

Probability of fluoroquinolone use in pigs

Rate at which bacteria becomes antibiotic-resistant after

antibiotic exposure

0.07/day

Natural loss rate, animals

0.007/day

Exposure rate from consumption/ handling of meat

10-3 /day

Colonization rate

0.01/day

Probability of fluoroquinolone use in humans

Natural loss rate, exposed

0.09/day

Natural loss rate, colonized

0.03/day

Natural loss rate, amplified

0.014/day

Exposure rate from the environment, contributed by V, Y

and Z

10-6/day

Loss rate of contaminated excretion in the environment

0.005/day

Transmission rate, amplified

0.5/day

Transmission rate, colonized

10-5/day

0.05

0.06

Results - Baseline parameter estimates

47%
34%

Results- 10-fold increase in FQ prescription

90%

47%

Results- Sensitivity analysis of FQR

S. Choleraesuis in humans
Varying FQ prescription
in humans
Varying FQ prescription in
pigs

Results- Sensitivity analysis of FQR

S. Choleraesuis in pigs

Varying FQ prescription
in pigs
Varying FQ prescription in
humans

Results- Impact of increased human exposure

via consumption of contaminated pork

Discussion
Substantial efforts have to be made to avoid
unnecessary use of antibiotics in humans
FQ prescription in pigs would only affect the time for
the emergence of FQR S. Choleraesuis in humans,
while it had little impact on the equilibrium
prevalence of antibiotic-resistant bacteria in humans.
Human FQ prescription would not only hasten the
emergence of FQR S. Choleraesuis in humans, but
also amplify their population density in the long term.

Discussion
Impact of banning animal antibiotic use
Result in a higher level of meat contamination by
common foodborne pathogen, and pose another
health risk to humans.
Increase costs to producers which will then be
transfer to consumers.

Discussion
The situation of FQR S. Choleraesuis in humans
and pigs in Taiwan
In our study,
FQR in animals was about 34%.
FQR in humans was about 47%.
In other studies,
In animals, it was about 15-34%.
In humans, it was about 60-73%.

Discussion
Better food hygiene to reduce and delay the emergence of
FQR S. Choleraesuis in humans.
Improper handling or incomplete cooking of contaminated meat
may increase the burden of FQR S. Choleraesuis among humans.
Comparing the effect of and , it was found that would have a
stronger effect on the early occurrence of FQR S. Cholereasuis in
humans.
Public health risk of Salmonella arising from the consumption of
contaminated pork can be affected by a variety of factors, while
consumers can control the risk from improper handling of pork.

Conclusion
In the past, most studies favored the idea that antibiotic
use in animals may be the most possible way to introduce
new antibiotic-resistant bacteria into humans through food
products, especially when the pathogens are zoonotic.
This study implies that antibiotic use in animal husbandry
has no substantial impact on the equilibrium prevalence of
antimicrobial-resistant bacteria in humans.
Proper handling or cooking can also eliminate the risk of
foodborne illness.

Conclusion
To combat FQR S. Choleraesuis infection in humans
our model suggested that while prudent use of
agricultural antibiotics has to be applied in hope of
lowering the emergence of resistance among animals
and delaying the onset of resistant bacteria in
humans, substantial efforts has to be made to avoid
unnecessary use of antibiotics in humans.

Using Caenorhabditis elegans Model to

Study Virulence of Salmonella Isolates
Carrying Variants of Salmonella
Genomic Island and Salmonella
Pathogenicity Island

Teacher:Chao-Chin Chang
Presenting Student:Ping-Yen Yang

80

Salmonella Pathogenicity Island

The complex infection cycle of Salmonella relies on

several sets of virulence genes, many of which are

contained on Salmonella pathogenicity islands (SPIs).

Various SPIs, SPI1-21, have been identified according to

the differences of their functional genes.

81

SPIs and Virulence Association

The mutants of SPI-1 and SPI-2 significantly decreased the

virulence of Salmonella in the chicken model, while the

strains absence of SPI1-SPI5 were barely invading to the
chickens spleen.
Ivan , et al., (2009)

The mutations in sopB, sopD and pipD genes decreased

the Salmonella enteropathogenicity in the bovine model.

Zhang , et al., (2002)

83

Multidrug Resistance
Salmonella enterica serovar Typhimurium phage type

DT104 , emerged in the 1990s, was found to own the

ability of multidrug resistance, specifically to ampicillin,
chloramphenicol, streptomycin, sulfonamides and
tetracycline (ACSSuT).

84

Salmonella Genomic Island 1

Salmonella genomic island 1 (SGI1) is a 43 kb genomic

island containing 44 open reading frames with MDR gene

cassettes.
Several studies indicated that DT104 carrying the MDR
region is a hyper-virulent strain, as compared to DT104
strains without MDR or other Salmonella enterica
serotypes.

85

Antibiotic Resistance and

Virulence Association
The positive relationship between fluoroquinolone

resistance and carriage of exoU suggests that

fluoroquinolone resistant Pseudomonas aeruginosa
infections may be attributable to enhance virulence.
Wong , et al., (2008)

The methicillin resistance reduces the virulence of

Staphylococcus aureus by interfering with the agr

quorum-sensing (QS) system that the ability of the
bacteria to secrete cytolytic toxins is reduced.
Rudkin , et al., (2012)
87

Salmonella Virulence Properties

in C. elegans (I)
The MDR Salmonella enterica Typhimurium DT104 has

been shown to be more virulent in C. elegans.

Surasri , et al., (2013)

88

Salmonella Virulence Properties

in C. elegans (II)
The mutations in sopB, sopD and pipD genes of both

Salmonella serovars did not exhibit significant decrease in

virulence towards the nematode.

Chai-Hoon , et al., (2015)

89

Caenorhabditis elegans
The soil nematode, C. elegans, has been

used as an invertebrate host model to

identify and assess virulence factors of
several human pathogens, including
Salmonella enterica Typhimurium.

90

C. elegans Life Cycle

C. elegans embryos

develop rapidly and

hatch after 14 hours.

C. elegans proceed

through four molt

cycles (L1-L4) before
becoming adults.
91

Aim
The objective of this study is to compare virulence among

Salmonella isolates carrying different SGI1 variants and

SPIs by C. elegans nematode model.

92

Selection of SGI1 Isolates

93

Selection of SPI Isolates

Salmonella pathogenicity island

Virulence genes

SPI1

invA, hilA

SPI2

spiC, ttrC

SPI3

misL, mgtC

SPI4

orfL, SPI4R

SPI5

pipD, sopB
*These isolates were without carrying SGI1 or its variants.

94

Comparison between SGI and

non-SGI isolates
With SGIs

Comparison among SGI

variants

Further comparison
among SGI variants
stratified by serovars,
hosts and phenotypes of
antibiotic resistance.

Without SGIs

Comparison among
isolates carrying different
numbers of SPIs

Further comparison
among isolates carrying
different sets of SPIs by
phenotypes of antibiotic
resistance.

95

Zoonoses through the Respiratory Tract

Bordetella bronchiseptica
B. bronchiseptica is a Gram-negative coccobacillus
commonly isolated from the respiratory tract of various
mammals.
It is one of the infectious agents involved in the higly
contagious Kennel Cough syndrome.
In the few human cases, pneumonia with interstitial
infiltrate the main clinical feature (Ford, 1995).
Causing pneumonia in a few immunocompromised
individuals
Vaccination of the dogs may help reduce such a risk, but
will not eliminate it, as these dogs can still be potential
carriers of the bacterium.

Mycobacterial infections
Tuberculosis (TB) caused by M. tuberculosis is certainly a
rare disease in dogs, most often resulting from a human
source (Acha and Szifres, 1989, Anonymous, 1999).
However, the infected dog can become the source of other
human infections.
There is potential for infection of pet dogs, especially those
owned by homeless or economically impaired persons.
Because canine tuberculosis often is the marker of the
disease in humans, its early recognition in dogs is essential
(Clercx et al., 1992).
In developing countries, where bovine tuberculosis is still
enzootic, dogs can be infected by M. bovis by consumption
of raw milk or possibly raw meat or offal from affected
cattle.

Mycobacterial infections (cont.)

Infection by M. bovis induces more commonly a digestive
form of tuberculosis in dogs.
Alimentary tuberculosis is the most likely result of M.
bovis infection in dogs, making fecal excretion a possible
zoonotic risk from affected dogs.
In dogs, tuberculous lesions resemble sarcomatous lesions,
rather than the typical tubercles, as caseation is rarely seen
(Clercx et al., 1992).
Human contamination from a M. tuberculosis-infected dog
results from infective aerosols or contact with urine, saliva
or cutaneous lesions.
Infected dogs should be destroyed and not treated, as
diagnosis is often late and treatment lasts for several
months, with the great risk of selecting multidrug resistant
strains.

Q Fever
Caused by Coxiella burnetii
mainly transmitted to humans and other mammals through
inhalation of infectious particles
In nature, C. burnetii is maintained by a wildlife-tick cycle.
Infection through tick bites has been reported for various
species, including humans.
Dermacentor, Rhipicephalus and Amblyomma ticks are
probably responsible for the transmission of C. burnetii
among dogs and wildlife (Hibler et al., 1985).
The primary reservoir hosts for C. burnetii are ticks, and
vertical transmission (trans-ovarial and trans-stadial) is
common.

Q Fever (cont.)
Laughlin et al. (1991) reported an outbreak in a family
after exposure to a deer and infected pregnant dog.
Farmers having Q fever outbreaks in their flocks or herds
should be aware of the risk associated with their pets.
Tick prevention and control is also important, especially in
dogs.

Identification of risk factors of Coxiella burnetii (Q fever)

infection in veterinary-associated populations in southern
Taiwan
Chao-Chin Chang1, Po-Shan Lin2,6, Min-Yi Hou2 , ChienChou Lin2, Min-Nan Hung3, Tzong-mu Wu4, Pei-Yun Shu2,
Wen-Yi Shih5, John Han-You Lin6, Wan-Ching Chen7, HoSheng Wu2, Li-Jen Lin3 *
Zoonoses Public Health 2010; 57:e95-101

Table 1. Univariate analysis of factors associated with Q fever in southern Taiwan.

Table 2. Seroprevalence of Q fever in different animal species in sounthern Taiwan.

Table 3. Multiple logistic regression for risk factors associated with Q fever in southern Taiwan.

ZOONOSES THROUGH
EXCRETIONS OF GENITO-URINARY
TRACT

Brucellosis
Dogs can be infected by several species of Brucella,
including B. abortus, B. melitensis and B. canis.
Evidence exists for transmission from cattle to dog by
ingestion of infected reproductive tissues.
At present, the zoonotic potential of B. abortus
transmission between dog and man appears limited.
Conversely, dogs are the main reservoir of B. canis, which
is pathogenic to humans.
B. canis is transmitted primarily by ingestion or inhalation
of aerosolized post-abortion material, but venereal
transmission is also reported (Johnson and Walker, 1992).

Brucellosis (cont.)
In the dog, B. canis infection is characterized by prolonged
bacteremia and reproductive failure in both males and
females.
In the pregnant bitch, B. canis causes embryonic or fetal
death or abortion.
In the male dog B. canis causes epididymitis and infertility.
In both genders infection is largely asymptomatic and
often remains undetected unless the animal is bred.
Treatment is based on the use of doxycycline and an
aminoglycoside (streptomycin, gentamycin, or netilmicin)
for 4 weeks followed by doxycyline (200 mg/d) and
rifampin (600-900 mg/d) orally for 4 to 8 weeks (Tan,
1997).

Brucellosis (cont.)
Symptoms of B. canis infection in humans are largely nonspecific including fever, splenomegaly, malaise, myalgia,
headache, and anorexia (Lum et al., 1985).
Septicemia has been reported in 50% of patients (Rousseau,
1985).
Though most cases respond well to antibiotic therapy, as
many as 3% of treated patients may die from endocarditis
or other complications(Rousseau, 1985).

Leptospirosis
The etiological agents of leptospirosis belong to the more
than 200 pathogenic serovars within the 23 serogroups of
Leptospira interrogans (Andr-Fontaine et al., 1994).
the main serovars involved in zoonotic transmission
between canid and humans were L. canicola and L.
icterohaemorrhagiae (Farr, 1995).
More recently, canine outbreaks caused by L. pomona and
L. grippothyphosa have been reported in Europe and in the
U.S.A. (Andr-Fontaine et al., 1994; Brown et al., 1996),
and at a lesser extent by L. australis, L. automnalis, or
some other serovars.
The range of serovars common in temperate regions is
much smaller than that found in tropical countries (Levett,
1999).

Leptospirosis (cont.)
The course of infection caused by exposure to a leptospiral
agent is largely dependent on host adaptation of the serovar.
In humans, the mortality rate may reach 10 to 20%.
Leptospira may be isolated from the patients blood or
cerebrospinal fluid during the 10 days of infection or the
urine after 21 days, and identified by dark-phase
microscopy or culture.
Laboratory diagnosis is still mainly based on serology,
especially micro-agglutination test (MAT).
Leptospires are very sensitive to penicillin G and
doxycycline,which are the most effective antibiotics in
dogs and humans, especially when administered in the
early phase of the disease.
Prevention is based on rodent control and exposure
reduction as well as dog vaccination.

Leptospirosis
Leptospirosis is solely a zoonotic disease. Human-tohuman transmission is extremely rare.
Leptospira is well adapted to a variety of mammals,
particularly wild animals and rodents.
Rodents are the only major animal species that can shed
leptospires throughout their life span without clinical
manifestations.
Humans are infected by exposure to water or food
contaminated by urine.

Leptospirosis (cont.)
Serovars

Principal hosts (clinical hosts)

L. icterohaemorrhagiae
L. grippotyphosa

Rodents (dogs, horses, cattle,

swine)
Rodents (dogs, cattle, swine)

L. canicola

Dogs (swine, cattle)

L. pomona
L. hardjo

Cattle, swine (horses, sheep, sea

lions)
cattle

L. bratislava

Swine (horses, sea lions)

Leptospirosis (cont.)
Infection with leptospires most frequently results from
handling infected animals or from aerosol exposure during
cage cleaning (a story of toothbrush).
Skin abrasions or exposure to mucous membranes may serve
as the portal of entry (a story of a polluted river).
All secretions and excretions from infected animals should be
considered infective.
The disease may vary from inapparent infection to severe
infection and death.
Infected individuals may experience a biphasic disease.
Ampicillin and doxycycline are effective in the treatment of
human patients. Tetracycline can be used to eradicate L.
ballum in a mouse colony.

Association of Natural Disaster and

Epidemics of Leptospirosis and
Melioidosis: Impact of Typhoon Morakot
in Taiwan in 2009
Hsun-Pi Su1,2,3, Ta-Chien Chan 4, Chao-chin Chang5*
Emerg Infect Dis 2011;17(7)1322-3

Figure 1. The
comparison of
epidemic curves in
2009 and between
2006-2008. (A) the
epidemic curves of
leptospirosis; (B) the
epidemic curves of
melioidosis. 20062008* means the
curve was made by
the average numbers
on a weekly basis.

VECTOR-BORNE ZOONOSES

Plague
caused by Yersinia pestis
In the dog and cat, infection is most likely to occur as a
result of flea bite or ingestion of an infected rodent
(Orloski and Eidson, 1995).
In dogs, plague is usually a mild disease, characterized by
a moderate fever, lethargy and enlarged lymph nodes
(Orloski and Eidson, 1995).
In humans, it may take bubonic, septicemic or pneumonic
forms. Clinical signs at presentation typically include
fever, myalgia, lymphadenopathy, nausea, and vomiting
(Crook and Tempest, 1992).

Plague (cont.)
As with other arthropod borne diseases, dogs potentially may
act as a vehicle for introducing vectors infected with Y. pestis
into the human environment.
Dogs pose a risk to humans by transporting fleas and fleainfested animals or carcasses into or around the home.
Human cases of acquiring plague from skinning wild canids
were documented.
very sensitive to streptomycin, but tetracycline and
doxycycline are also very effective.

Plague Pneumonia California.

MMWR 1984;33(34);481-3
The patient, who is a veterinarian and has a small-animal
practice, denied contact with wild animals or travel outside his
local area. He had no history of a needlestick injury or cut
during surgery or other procedures. His office and home
environment were investigated as potential sources of infection.
Office records and charts of all animals seen by the veterinarian
during the week before onset of symptoms were evaluated. Only
one animal, cat A, had an illness with symptoms compatible
with those usually seen with pneumonic plague (difficulty
breathing and hemoptysis) but had no fever. The cat died, and
its body was not available for autopsy. No suspicious illnesses
among neighborhood animals or owners were noted, but 51 pet
owners were contacted and advised to disinfest their pets and to
avoid contact with ground squirrels and other rodents.

Cat-Transmitted Fatal Pneumonic Plague in a

Person who Traveled from Colorado to Arizona
Doll JM et al., Am J Trop Med Hyg
1994;51:109-114
The study reported the case investigation of a patient,
presumably exposed to a plague-infected cat in Colorado,
who presented with gastrointestinal symptoms, and
subsequently died of primary pneumonic plague.
Public health officials should be vigilant for plague activity
in rodent populations
Veterinarians should suspect feline plague in ill or
deceased cats.
Physicians should have a high index of suspicion for
plague in any person who has traveled to plague enzootic
areas.

Cat Scratch Disease (Bartonella

henselae)

Epidemiology:

Cats are the main reservoir (28% of US

pet cats sero +). Cats can be
bacteremic for months. Stray cats,
young cats more likely to be bacteremic.
No vertical/horizontal transmission.

Fleas are main vector from cat to cat.

Cat to humans: mainly scratch, likely
inoculation of infective flea feces at time
of scratch.
Flea transmission to humans possible,
not clearly demonstrated.
Recent suggestion of possible tick
transmission.

Cat Scratch Disease: Mode of

transmission
Bartonella henselae
Cat Scratch: + + + (76%, Margileth, Adv. Pediatr. Infect.
Dis., 1993

Cat Bite: ? ? ?
Flea Bite: +/- ?

Cat Scratch Disease (Bartonella henselae)

Symptoms: 1 week after scratch:
papule/vesicule at inoculation site,
2-3 weeks: lymphadenopathy, fever,
Complications: Parinauds
syndrome, granulomatous lesions,
retinitis, endocarditis, encephalitis
(1 lethal case).
Diagnosis: in humans, mainly serology;
in cats: blood culture/PCR
Treatment: No benefit in classical
forms. In severe cases,
Doxycycline, Erythomycin, Rifampin,
Azithromycin: 15- 21 days.

Bacillary Angiomatosis

Molecular Epidemiology of Bartonella henselae Infection

in HIV-infected patients and their cat contacts using
pulsed field gel electrophoresis and genotyping.
Chang et al., J. Infect. Dis. , 2002, 186:1733-1739.
B. henselae was isolated from 12 HIV-infected individuals
with bacillary angiomatosis/peliosis hepatis and from their 15
domestic cat contacts.
Three of the 4 patients with B. henselae genotype I
infection, but none of the 8 genotype II patients had
hepatosplenic vascular proliferative lesions (p=0.018).
Four of the 5 human-cat pairs had closely-related PFGE
fingerprints and concordant results by 16S rDNA typing,
strongly suggesting that human infection was caused by the cat
contact.

Bartonella henselae infection in HIV-patients and their

cats. Chang et al., J. Infect. Dis. , 2002, 186:1733-1739.

130

Unknown Fever and Back Pain Caused

by Bartonella henselae in a Veterinarian
after a Needle Puncture

Lin J.W., Chen C.M., Chang C.C.*

Vector Borne Zoonotic Dis 2011; 11(5):589-591.

 A male patient who was a 32 year-old veterinarian

working in a private veterinary clinic, sought for clinical
help due to unknown fever and persistent back pain for
at least a month.
According to the patients description, the fever was
undulant and right back pain was noted during fever
bouts. Fever was only improved after use of analgesic,
but soon exacerbated with chills for several hours.
He was not noted any obvious blisters, rashes or bites
from insects or animals. However, before the illness,
he recalled a needle puncture several days ago.
132

 Therefore, this case was reported to Centers for

Disease Control, Taiwan for investigation zoonotic
infections. Serological tests for Q fever, brucellosis and
leptospirosis were all negative.
Bartonellae isolation using whole blood was
unsuccessful, but the IgG titres by IFA tested at two
different time points (more than 2 weeks apart) were
strongly positive for B. henselae (1: 131,072 and 1:
65,536, respectively).
Molecular diagnosis using extracted DNA from the
patients whole blood and lymph node aspirates,
were negative after polymerase chain reaction (PCR)
of the citrate synthase (gltA) gene for Bartonella.
133

Figure. Dot-blot analysis with a specific probe

for B. henselae. N: negative control, sterile water
substituted for DNA templates; NP: blood
sample from a normal individual without CSD; P:
positive control, B. henselae ATCC49882; B1:
the patients blood sample before treatment for
CSD; B2: the patients blood sample after
treatment for CSD; LN: lymph node aspirates
from the patient before treatment for CSD.

 For the clinical treatment, the patient was given

intravenous rocephine on the initial 6 days, and then
oral doxycycline and azithromycin were given in turn
for 4 days and 5 days, respectively. The patient was
also given intravenous decadron on the seventh day,
which was replaced by oral prednisolone for the
remaining 9 days. The pain and fever disappeared
within one week.

135

Discussion
The main route for humans acquiring CSD infection is
through the wound contaminated with infectious flea
feces after animals scratches or bites.
This event highlights the importance of wound
management for CSD prevention, especially in high
risk population, such as veterinarians.
Unknown fever combined with back pain in patients
with cat exposure and/or who are participating
veterinary-associated professionals should consider B.
henselae infection, after ruling out other suspected
infections.

Transmission of Bartonella spp.

among animals and humans
B. vinsonii subsp. berkhoffii

B. henselae, B. clarridgeiae, B.

B. elizabethae, B. grahamii,
B. vinsonii subsp. arupensis,
B. washoensis
B. henselae

B. alsatica

B. weissii, B. chomelii, B. schoen

Isolation of Bartonella species from rodents in

Taiwan, including a strain closely related to
Bartonella rochalimae from Rattus
norvegicus.
Jen-Wei Lin, Chun-Yu Chen, Wan-ching Chen, Bruno B. Chomel, Chao-chin Chang*

Journal of Medical Microbiology 2008; 57:1496-1501

Lyme Disease

Medical and Veterinary Importance

of ticks
Dermatoses
Otoacarisis
Tick paralysis: esp. female ticks; 10% casefatality rate
Transmission of animal and/or zoonotic disease
agents
Envenomization: toxic salivary components
Exsanguination: anemia

Soft tick versus hard tick

Epidemiologic Characterics
LD accounts for more than 95% of all reported
cases of vector-borne illness in the U.S.
According to CDC, the mean national annual rate
was 5.5 cases/100,000 population (1993-1997).
The highest reported rates are in children aged
<15 years and in adults aged 30-59 years.
Who is at risk?
-- persons live or work in the areas surrounded by
woods or brushy lands;
-- persons participate in recreational activities;
-- persons engage in outdoor occupations.

Routes of Transmission
Mainly from tick bites (nymphal stage)
Not spread by person-to-person transmission
Cannot be acquired by direct contact with
infected animals.
Transplacental transmission has been reported.
No report on transmission in breast milk
Since Bb can be cultured from the blood in
patients in acute phase, and can survive in stored
blood for several weeks, it is potentially
transmitted by blood transfusion.

Lyme Disease in Taiwan

Isolation of Lyme disease agents has been reported

Climatic conditions in Taiwan
Ecological factors supporting tick survival in Taiwan
Role of dogs in transmission of Lyme disease

Figure. The host-parasite

ecological continuum
(here parasites include
viruses and parasitic
prokaryotes).
Daszak P et al., Emerging
infectious diseases of
wildlife--threats to
biodiversity and human
health. Science
2000;287(5452):443-9

Published by AAAS

Thanks for Your Attention

Materials & Methods

Probability of fluoroquinolone use in pigs

0.05

Probability of fluoroquinolone use in humans

0.06

Rate at which bacteria becomes antibiotic-resistant after

antibiotic exposure

0.07/day

In Taiwan, fluoroquinolones are allowed to be used in animal husbandry only for

therapeutic purposes. Its use for growth promotion has been currently prohibited.
We assume a 5% of fluoroquinolone usage in pigs, including those for therapy and
possible violation.
In humans, about 60% of Taiwanese patients received an antibiotic prescription. Among
which, fluoroquinolones usage was about 10%.
The probability of fluoroquinolone use in humans = 60% * 10%
The average time for bacteria to become antibiotic-resistant after fluoroquinolone
exposure was studied to happen at around 2 weeks.

Materials & Methods

Natural loss rate, animals

0.007/day

Natural loss rate, exposed

0.09/day

Natural loss rate, colonized

0.03/day

Natural loss rate, amplified

0.014/day

Loss rate of contaminated excretion in the environment

0.005/day

In pigs, there would be a long-term excretion of S. Choleraesuis for about 150 days.
In humans, the duration of excretion for short term Salmonella carriers is about 11 days,
while the duration of Salmonella excretion in colonized population is about 5 weeks.
Antibiotic therapy in acute salmonellosis in humans can prolong the duration of fecal
excretion of Salmonella to approximately two-fold of that without antibiotic use.
The natural turnover rates per day is calculated by the inverse of the duration of
Salmonella excretion in each status.
In the environment, the spontaneous loss of resistant in antibiotic-resistant culture is
studied to be around 0.5%.

Materials & Methods

Colonization rate

0.01/day

Studies have shown that after exposure to antibiotic-resistant bacteria, about 1% of

antibiotic-resistant bacteria in the exposed population would colonize.

Materials & Methods

Exposure rate from the environment, contributed by V, Y

and Z

10-6/day

Exposure rate from consumption/ handling of meat

10-3 /day

In developed countries, such as Taiwan, environmental exposure of antibiotic-resistant

bacteria was considered to be rare.
Thorough cooking of meat could kill both the susceptible and resistant bacteria.
It is assumed that FQR S. Choleraesuis in pork can infect humans via improper cooking
or poor kitchen hygiene during food preparation.

Materials & Methods

Transmission rate, amplified

0.5/day

Transmission rate, colonized

10-5/day

The amplified population is assumed to carry a relatively high load of FQR S. Choleraesuis
and is highly contagious.
Thus, the transmission rate is assumed to be much higher than .

Discussion
Uncertainties in parameter estimation
Probability of FQ prescription in pigs
The exposure rate of FQR S. Choleraesuis via
consumption/handling of contaminated pork
The environmental exposure rate of FQR S.
Choleraesuis

Discussion
Rate of the development of FQR in S. Choleraesuis

Continuous low-level use of antibiotics for growth promotion in animals may

result in a faster rate for the development of antibiotic resistance in bacteria.

Double the rate of a in pigs (a*=0.14/day)

The equilibrium prevalence of FQR S. Choleraesuis in pigs would rise to 50%,

while that in humans remained at 47%.

Double the rate of a in humans (a*=0.14/day)

The equilibrium prevalence of FQR S. Choleraesuis in humans would rise to

70%. FQR S. Choleraesuis would occur much earlier.