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© 1992 MUNKSGAARD

Diseases of the Callitrichidae: A review


Potkay S. Diseases of the Callitrichidae: A review. J Med Primatol Stephen Potka,
1992:21: 189-236. USPHS, NIH, Natior '1'", t, Research
Resources, Veterinar' 'i~,;,' ' 'Ct:.,"~ram,
The Callitrichidae contains four genera that embrace up to 50 species and Bethesda, MD, U.S"'\.
subspecies found in neotropical habitats. Certain members have either
naturally occurring or induced conditions that serve as important models
of human disease. They include viral, bacterial, and parasitic infections, Key words: tamarins - marmosets - calli-
nutritional deficiencies, neoplasia, and various other conditions. The trichids - Saguinus - Callithrix - Cebuella -
spontaneous diseases of captive caIIitrichids and those to which these spe- Leontopithecus
cies are experimentally susceptible were reviewed. Stephen Potkay, Office for Protection from
Research Risks, Building 31, Room 5B59,
National Institutes of Health, Bethesda, MD
20892, U.S.A.
Accepted for publication April 1, 1992.

Introduction
Callitrichids have long been kept in zoological ex- logical, wildlife, research, and veterinary medical
hibits and as pets both in their countries of origin publications. Although many of the studies were
and abroad. There are a number of reports concern- well conducted, some were incomplete and others
ing the difficulty of maintaining and breeding them seemed to be casual observations. The large gaps
in captivity that date back 50 or more years in our understanding of the cause, prevention, and
[159,194-199,308], and their use in research, par- cure of the diseases of the callitrichids should stim-
ticularly parasitology, is longstanding. It was not ulate further study.
until the 1960s, however, that the potential of calli-
trichids for helping to understand infectious dis- Callitrichid taxonomy
eases and for cancer research began to be recog-
nized [294). Subsequently, numerous research and Callitrichids are small, arboreal neotropical mon-
breeding colonies were established for studying keys (suborder Platyrrhini, family Callitrichidae)
both specific human diseases and other biological commonly known as pygmy marmosets (genus
phenomena. This review is concerned primarily Cebuella), true marmosets, or ouistis (genus Cal-
with the spontaneous infections and noninfectious Iithrix) , tamarins (genus Saguinus), and lion tama-
diseases identified in callitrichids and secondarily rins (genus Leontopithecus). The genera are differ-
with experimentally-induced diseases. The review entiated principally on the basis of size, dentition,
does not cover a number of publications dealing and genital morphology. Within genera, more sub-
with other aspects of the captive callitrichid. Topics tle differences in the above characteristics, as well
of this other literature include husbandry [7,33, as differences in color, distribution and length of
52,159,205,206,215,228,267,294,316,324,420, hair, behavior, and geographic and ecologic distri-
443,450,453,523] reproduction [33,39,52,56,57, bution serve to define species and subspecies. De-
70,135,159,182,206,207,209,210,214,228,273, tailed descriptions of the various callitrichids have
277,280,294,295,307,310,329,365,366,377,387, been published by Hershkovitz, and the listing of
4t8,430,466,469,472,487,497,510,522] body species covered in this review (Table I) is arranged
weights and measurements [189,223,228,303,491, according to his classification (222). Table 1 also
519], gnotobiology [129,237), hematology [9,58, indicates earlier scientific names found in the litera-
133,211,212,228,315,323,328,340,492,519), blood ture cited in this review, as well as some of the
chemistry [43,74,89,95,96,133,148,239,298,492], common names of these species [72].
blood vitamin values [327,435], bi00d groups
[508], genetics [22,31,181,295], behavior [37,38,
97,130,131,132,236,257,266,326,339,363,386, Transition from the wild to captivity
453], and conservation and ecology [63,80,81,98, Many of the disease states to be described were
105,171,179,281,337,343,361,391,399,442,446, associated with newly imported animals, and virtu-
455:477,493]. ., ally all of them occurred under conditions of con-
Source material for this review came from zoo- finement. The process of bringing a callitrichid

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Table I. Taxonomic classification of the family Callitrichidae
Classification Selected synonyms Common name
Pygmy Marmosets (Cebuella) Callithrix pygmaea, Hapale pygmaea,
C. pygmaea Jacchus pygmaeus Pygmy marmoset
True marmosets (Callithrix)
A. Tufted-ear marmosets
C. jacchus penicillata C. penicillatus, Hapale penicillata Black-tufted-ear marmoset
C. jacchus geoffroyi C. geoffroyi, C. leucocephala Geoffroy's tufted-ear marmoset
C. jacchus jacchus C. jacchus, C. albicollis, Hapale jacchus Common marmoset
C. jacchus aurita C. aurita Buff-tufted-ear marmoset,
White-eared marmoset
B. Bare-ear marmosets
C. argentata melanura Hapale melanura Black-tail marmoset
C. argentata argentata C. argentata, Mico argentata, Mico mela- Silvery marmoset
nurus
C. Tassel-ear marmosets
C. humeralifer humeralifer C. santaremensis, Hapale santaremensis, Black and white tassel-ear marmoset, San-
H. humeralifer tarem tamarin, Silky tamarin
C. humeralifer chrysoleuca C. chrysoleuca Golden-white tassel-ear marmoset
Tamarins (Saguinus)
A. Hairy-face tamarins
1. White-mouth (S. nigricollis) group
a. Black-mantel (S. nigricollis) tam- Leontocebus nigricollis, Tamarinus nigri- White-lipped tamarin,
arins collis Black and red tamarin
b. Saddle-back (S. fuscicollis) tam-
arins
S. fuscicollis fuscicollis Spix's saddle-back tamarin
S. fuscicollis inustus
S. fuscicollis illigeri Illiger's saddle-back tamarin
S. fuscicollis lagonotus Red-mantel saddle-back tamarin
S. fuscicollis leucogenys Andean saddle-back tamarin
S. fuscicollis nigrifrons Geoffroy's saddle-back tamarin
S. fuscicollis weddelli Weddel's saddle-back tamarin
2. Moustached tamarin group
a. Red-chested moustached tamarin
S. labiatus Leontocebus labiatus Geoffroy's moustached tamarin,
Rufiventer marmoset, Red-bellied tamarin
b. Black-chested moustached
tamarin
S. mystax mystax Leontocebus mystax, Tamarin mystax, Spix's moustached tamarin,
Mystax mystax Moustached tamarin
c. Emperor moustached tamarin
S. imperator Emperor moustached tamarin,
Emperor tamarin
3. Midas tamarin group
a. S. midas midas Tamarinus midas Golden-handed tamarin
b. S. midas niger Mystax ursulus, Saguinus tamarin, Black-handed tamarin
Tamarin tamarin, Cercopithecus tamarin,
Leontocebus ursulus, Tamarin midas
B. Bare-face Tamarins
1. Brazilian bare-face (S. bicolor)
group
S. bicolor bicolor Marikina bicolor, Seniocebus bicolor Pied bare-faced tamarin
2. Colombian and Panamanian bare
face (S. oedipus) group
a. Silvery-brown bare-face tamarin
S.leucopus
b. Crested bare-face tamarins
S. oedipus geoffroyi Leontocebus geoffroyi, Oedipus spixi, Red-crested bare-face tamarin, rufous-
Saguinus spixi, Marikina geoffroyi naped tamarin
S. oedipus oedipus Oedipominas oedipus, Leontocebus oedipus Cotton-top tamarin
Lion tamarins (Leontopithecus)
L. rosalia chrysomelas Leontocebus chrysomelas Golden and black lion-tamarin
L. rosalia rosalia Leontocebus rosalia, Midas rosalia, Golden lion-tamarin, Golden marmoset
Leontideus rosalia
L. rosalia chrysopygus Mystax chrysopygus, Leonideus Golden-rump lion-tamarin
chrysopygus
Other species cited, but not identified
Callithrix nigrifrons and
Callithrix personata
- - - - - - - - - - - - - - - - - - - - - - - - - - - - - -- - --------

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Callitrichid diseases

from the forest to the laboratory entails capture by imental infection by herpesviruses of other New
any of several methods [445,480] followed by load- World monkeys, Old World monkeys and people
ing, off-loading, and transportation procedures in- [21,249,331,334] .
volving boats, motor veh'icles, and aircraft. During
these transportation procedures, the callitrichid may Alphaherpesvirinae (Herpes simplex virus group)
be relocated several times. The changes in location
may be swift (a few weeks) or prolonged (several Human herpesvirus (Herpes simplex or H. hominis) types 1
months), and are usually associated with exposure and 2. While natural infection with herpesvirus type
to other animals and a variety of people, changes 2 has not been reported in callitrichids [260], type
in diet, changes in ambient temperature, elimina- I was isolated from the lung of a Saguinus sp [354].
tion of social groups, changes in circadian rhythms, A live vaccine made from small plaque viruses iso-
exposure to new and different sounds and odors, lated from tissue cultures of the wild type 1 was
confinement, and individual isolation. Such condi- nonpathogenic and protected marmosets against
tions are sometimes conducive to stress, which, for otherwise fatal infections [93].
the purposes of this paper, we understand to mean
the physiological, immunological, hormonal, and Cercopithecid herpesvirus 1 (Herpesvirus simiae or Herpes-B
metabolic response to physically or psychologically virus). This naturally occurring, largely latent infec-
disturbing situations [62,432]. Under extended or tion of Old World monkeys, which is usually fatal
repeated stress, depressed inflammatory and im- for human beings, has not been reported in New
mune responses may render an animal more suscep- World monkeys. The significance of serum neu-
tible to the effects of infection and parasitic agents tralizing antibody in one of 42 marmosets surveyed
that may be present in its body or to which it may was not clear [259).
become exposed. It would seem that reports of mor-
tality and morbidity among imported callitrichids Herpesvirus tamarinus (Herpesvirus-T or H. platyrrhinae).
must be interpreted with those events in mind, and The reservoir host for this virus is Saimiri sciureus,
that particular attention should be directed toward which may develop ulcers of the lips and oral mu-
reducing stress related to capture, transportation cosa. Lagothrix sp, Cebus sp, Callithrix sp, and
and maintenance in captivity. Ateles sp were found to carry antibody, but no clini-
cal manifestations have been recorded [259]. This
Viral diseases agent, however, produces serious disease in calli-
trichids [108,238,336,352). Among captive Sagui-
The susceptibility of callitrichids to a host of viral nus oedipus, S. mystax, and S. nigricollis, for ex-
agents has been demonstrated by the results of sero- ample, infection was associated with a very high
logic surveys and virus isolations from both captive mortality rate. The incubation period was seven to
and wild populations as well as by experimental ten days, and clinical signs consisted of vesicula-
studies. Among captive animals, the most impor- tion and often severe ulceration of the lips and oral
tant naturally occurring infections are caused by mucosa, occasional ulcerative dermatitis, sneez-
herpes, pox, influenza, and parainfluenza viruses. ing, serous nasal discharge, anorexia, depression,
The viral infections described below are catego- and pruritus. Death ensued in two to three days.
rized according to the taxonomic scheme estab- Gross necropsy findings were extensive and in-
lished by the International Committee on Taxon- cluded splenomegaly, ulceration, and hemorrhage
omy of Viruses [322]. throughout the alimentary system, and hemorrhage
and focal necrosis of lymph nodes, adrenal cortices,
DNA viruses liver, and lungs. Microscopically, these lesions
Adenoviridae were typified by focal necrosis and the presence of
intranuclear inclusion bodies; multi-nucleated giant
Antibodies to adenovirus group antigen, adeno-
cells with intranuclear inclusions were also present
virus-12 tumor antigen or SA 7 were not detected
in mucocutaneous lesions. While encephalitis was
in surveys of captive Cebuella pygmaea, Saguinus
sometimes present, it was usually not extensive.
sp, and Leontopithecus rosalia [108,259,260].
Although the causative agent of hepatitis oc-
Although adenovirus type 12 administered to Sagu-
in us sp did not result in infection [398], adenovi- curring in six S. fuscicollis Uagonotus?) that died
ruses SqM-I and SqM-2 were infective for marmo- suddenly was not identified, the observation of
sets [219]. many gray-opaque, circumscribed hepatic foci char-
acterized microscopically by cytomegaly, necrosis,
Herpesviridae and large intranuclear inclusions was consistent
with herpesvirus, possibly H. tamarinus, infection
Callitrichids are the reservoir host for at least one [424].
herpesvirus, and are susceptible to natural or exper- H. tamarinus has also been isolated from 5% of

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Potkay
216 imported S. nigricollis and S. mysta:x:. none of Herpesvirus ateles. The strains of H. ateles (HVA-73,
which died unless concurrently infected with Sen- HVA-93, and HVA-94) obtained from Ateles pa-
dai virus [354]. Mortality among the doubly in- niscus induced lymphomas following inoculation
fected animals was 100%. Antibody was present in into S. oedipus, S. fuscicollis, and S. nigricollis
apparently healthy S. fuscicollis and S. nigricollis [250,334]. Animals became moribund or died
(25 of 144) and S. mysta:x: (2 of 14), but in none of within 14-32 days. The lymphomas were charac-
24 S. oedipus [108]. terized as being poorly differentiated, and no sig-
Prevention of infection consists of maintaining a nificant hematologic changes were observed [143].
policy of strict separation of species from the time
of capture through their maintenance in quarantine, Varicella zoster. Inoculation of C. pygmaea with wild
conditioning, breeding, and research· colonies. It is and attenuated forms of the OKA strain was associ-
especially important to segregate callitrichids from ated with a low antibody response: Clinical signs
Saimiri. Ateles. Cebus. and Lagothrix, which are were not observed, and virus could not be isolated
demonstrated or potential reservoirs for this virus. [ 13]. Subsequent challenge with the wild strain re-
In addition, a vaccine has been developed and used sulted in production of antibody at a higher level
to protect Saguinus and Aotus, which are equally in marmosets previously inoculated with the wild
susceptible to infection [93]. as compared with the attenuated forms. Inoculation
of C. jacchus with strains KMcC and OKA/Merck
by the oral, nasal, and conjunctival routes evoked
Herpesvirus saguinus. This virus, isolated from an S.
peak antibody responses within 6-11 weeks that
oedipus kideny cell culture, has not been reported
persisted for over a year. The delayed appearance
to cause disease in any species [332].
of antibody was consistent with the time needed for
viral replication, which occurred primarily in the
lungs [394].
Gammaherpesvirinae (Lymphoproliferative group)
Herpesvirus saimiri. H. saimiri (HVS-ll) exists as a Human herpesvirus 4 (Epstein-Barr). Epstein-Barr virus
latent infection in Saimiri sciureus. but, with one (EBV) is the causative agent of infectious mononu-
exception [475], has not been associated with natu- cleosis and may be associated with the development
rally occurring disease in this or other species of Burkitt's lymphoma and nasopharyngeal carci-
[247]. H. saimiri is the first nonhuman primate vi- noma in man. In S. oedipus. S. fuscicollis. and
rus shown to be oncogenic in primates. Experi- C. jacchus. inoculation of EB V strains B95-8
mentally, inoculation of cell-free virus or viable and Kaplan usually induced malignant lymphoma
tumor cells induced malignant lymphoma in C. and death within one to two months [148,256,
jacchus. S. oedipus, S. mysta:x:. and S. fuscicollis 360,436,461,462,514]. Affected animals had
[248,333,335,398,514]: Neutralizing antibodies lymphadenopathy and enlarged spleens and thy-
were detected two weeks after infection. Typically muses; microscopically, lymphoreticular cells were
there was proliferation of reticulum cells in the kid- seen to replace normal tissues in these organs. In-
neys, liver, spleen, lymph nodes, thymus, lungs, clusions have not been observed, and virus particles
and adrenal glands that invaded or replaced the nor- have not been recovered from tissues, but antibody
mal tissue. Inclusions and virus particles were not to several EB viral components was detected. In
demonstrated in affected animals. Signs of upper one of six S. fuscicollis, EB V strain B96-8 induced
respiratory disease and marked lymphocytosis were malignant lymphoma: Viral antigen and early anti-
sometimes observed, and affected animals gener- gen (EA) appeared two weeks after inoculation and
ally died within three to six weeks of infection. persisted [465]. In another study, the M81 strain
Vaccines consisting of attenuated and killed H. of EBV induced lymphocytosis and a heterophile
saimiri have been developed and tested in callitrich- antibody response in five C. jacchus, which devel-
ids [2,290,514]. The attenutated virus, adminis- oped no signs of disease [500]. Viral capsid anti-
tered to C. jacchus. produced a clinically inappar- gens were evident 15 weeks after infection and per-
ent, persistent infection characterized by mild sisted, and two marmosets produced antibody to
hyperplasia of lymph node follicles [516]. Immune the R component of EA infection beginning six
animals were resistent to subsequent challenge with weeks after exposure. The similarity of these find-
an oncogenic strain. S. oedipus. similarly treated, ings to EBV infection in people suggests that C.
was not protected by this vaccine. A heat and for- jacchus may be useful in studying cofactors in
malin killed vaccine protected S. oedipus against EB V-associated malignancies. In S. oedipus. com-
the oncogenic effect of untreated virus and pro- plete protection against lymphogenic doses of EBV
duced high serum antibody levels [289], but did not was afforded by immunization with small quantities
protect against tumor development after tumor cell of the EBV major envelope glycoprotein (gp 340)
transplantation [291]. incorporated into immune-stimulating complexes

192
Callitrichid diseases
and administered subcutaneously [349]. Similar tially characterized by moderate to extensive acan-
protection was obtained using a vaccinia virus (WR thosis, and later by full-thickness epidermal necro-
laboratory strain) recombinant expressing the gp sis and ulceration; dermal inflammatory changes
340 gene administered by dermal scarification or were associated with advanced lesions. Occasion-
intradermal injection [350]. The mechanism of pro- ally, degenerating keratinocytes contained granular
tection may have been cell-mediated, since no cir- intracytoplasmic inclusion bodies. A poxvirus was
culating antibody against gp 340 was detected. No identified electron microscopically from negatively
protection was achieved when the Wyeth vaccine stained direct skin scrapings; it was not related sero-
recombinant was used. Interaction between EBV logically to vaccinia, and was morphologically dif-
and Plasmodium infections are discussed under ferent from tanapox and benign epidermal mon-
Protozoan Diseases, Plasmodiidae. keypox. The significance of this viral infection is
not known.
Herpesvirus papio (HVP). Strains of Epstein-Barr-like
herpesvirus were isolated from baboons with
lymphomas (HVP-L) and from normal baboons RNA viruses
(HVP-N) [ 106]. Inoculation of adult S. oedipus and
Reoviridae
S. f. nigr{frons with HVP-L resulted in develop-
ment of marked, often lymphoproliferative disease, Reovirus. Type 3 was isolated from the throats and
whereas neonatal tamarins and C. jacchus had only feces of newly imported Saguinus sp [108], S.
transient signs of inguinal lymph node enlargement. nigricollis, and S. mystax [354]. There was no
Antibody to viral components was produced by seasonal incidence, and no signs of disease were
adults, but no antibody was detected in neonates. associated with infection. Serologic surveys
HVP-N was found to infect adult callitrichids based demonstrated the presence of antibodies to reovi-
on their antibody responses, but disease did not ruses types I, 2, and 3 in captive colonies of mar-
develop. mosets [259], S. sp [108], and S. oedipus [260].
The incidence of type 3 (35%, 64%, and 79% re-
Poxviridae spectively, in these colonies) was the most preva-
lent of these viruses. No antibody was detected
Orthopoxvirus (Vaccinia subgroup) against SV 12.
Vaccinia. Smallpox-like lesions appeared at cutane-
ous inoculation sites four to six days after adminis- Rotavirus. The results of a survey of 14 captive Cal-
tration of human vaccinia virus vaccine to Saguinus lithrix sp for antibody to the SA II strain of rotavi-
sp [108]. Healing was complete in 12-20 days. In a rus indicated that 92% were positive [261]. This
serologic survey of 20 captive S. oedipus, antibody incidence suggests that infection was with the SA
against vaccinia was found in two 1260J. 11 strain or a closely related virus. It is possible
that infections probably occur more commonly in
Monkeypox. Nonfatal monkeypox was diagnosed in captivity than in the wild, but the role of rotaviruses
one S. oedipus during an outbreak in a Dutch zoo- in the gastroenteritides of monkeys has not been
logical garden [157,235,371]. In other studies, 4 established.
of 35 presumably healthy marmosets and 4 of 20
S. oedipus had HI titers to monkeypox virus, Orbivirus. A serologic survey of captive marmosets
though the significance of this finding has not been and S. oedipus failed to demonstrate the presence
determined [258,260]. of antibodies against Colorado tick fever virus
[259,260).
Poxvirus. An unspecified poxvirus was the cause of
an epizootic among C. jacchus that began three
Orthomyxoviridae
weeks after import and lasted for six months [191].
Thirty-six percent of 80 marmosets developed cuta- Influenza. Influenza virus type A2 was isolated from
neous erythematous papules, particularly on the the throat and lung of a captive tamarin (Saguinus
tail, scrotum, and abdomen, that progressed within sp) which died with bronchopneumonia [108]. It
ten days to elevated plaques with scab formation, was in a colony exposed to personnel carrying anti-
and later to punctate hemorrhagic ulcers. Coinci- genically identical agents and suffering from flu-
dentally, multiple plaques with dark umbilicated like respiratory symptoms. Of 216 S. nigricollis
centers and grey borders were seen on the palms and S. mystax 4% carried influenza A2/Hong Kong
and soles. The duration of the clinical disease was 68 [354]. No morbidity or mortality attributable to
four to six weeks. Deaths that occurred were attrib- this virus was seen, and the tamarins had antibody
uted to intercurrent diseases (anemia and chronic when tested two months later. No antibody against
pancreatitis). Histologically, the lesions were in i- influenza A was found, although serologic evidence

193
Potkay
of influenza Band A2 infections was demonstrated mals developed a mucous nasal discharge, facial
in S. oedipus [260] and marmoset [259] colonies. erythema and edema, and maculopapules on the
lips. Infrequently, there was epilation of the ventral
abdominal and thoracic skin and a maculopapular
Paramyxoviridae
exanthem. Koplik's spots were not observed. Inap-
Parainfluenza. Parainfluenza virus type 1 (Sendai) parent infections also occurred evidenced by the
was isolated from 29 of 216 S. nigricollis and S. high neutralizing antibody titers found in callitrich-
mystax that were newly imported [354]. The only ids that survived. Significant gross lesions of mea-
clinical sign of infection was fever (40.5°C), but sles infection were not found at necropsy. The prin-
there was a wide range in mortality. At necropsy cipal histologic finding was interstitial pneumonia;
several had pulmonary lesions. Tamarins having occasionally bronchopneumonia was present. Alve-
concurrent infection with Herpesvirus tamarinus. olar walls were thickened and there were focal areas
however, invariably died. Sendai virus was isolated of giant cell formation. The nuclei of some of these
at a breeding colony from C. jacchus with clinical cells contained eosinophilic inclusion bodies.
signs consisting of rapid respiration, dyspnea, de- Warthin-Finkeldey type giant cells were seen in
pression, anorexia, sneezing, ocular and nasal dis- the lungs, mesenteric lymph nodes, spleen, and
charge, and piloerection [160]. Most cases occurred lymphoid tissue of the colon. Histologic findings
in marmosets between one and nine years old and and clinical signs can be used to make a presump-
were self-limiting. Infections in infants were some- tive diagnosis of rubeola, but virus isolation is nec-
times fatal and characterized by extensive pneumo- essary to rule out other paramyxoviral agents. In
nia. An outbreak of parainfluenza type 1 infection another colony of C. jacchus. S. Juscicol/is. S. ni-
was also reported in 69 of 91 domestically produced gricollis. and S. oedipus. measles was thought to
C. jacchus whose clinical signs were similar to have affected 40% of the animals, 70% of which
those described previously, and whose lesions con- died [74]. Clinically, incoordination, apparent
sisted of interstitial pneumonia [463]. Intranasal in- blindness, and rapid death were observed. Some
oculation of S. mystax with passaged parainfluenza giant cells were observed in the livers and spleens,
virus type 1, Sendai strain, was associated with but rubeola was not isolated. The severe effects of
sneezing, coughing, nasal discharge, and puffy measles on callitrichids have resulted in the imposi-
eyelids [213]. The incubation period was about five tion of procedures in some colonies to minimize
days and antibody was detected two to three weeks exposure to potentially infected nonhuman and hu-
after infection. Infections were readily transmitted man primates. In addition, human measles vaccine
to cage mates, and tamarins lost significant weight [4,5,404] and human gamma globulin [74] have
within 2 weeks of exposure; fever was not a consis- been used prophylactically. Immunized callitrichids
tent finding. Parainfluenza types 2 (1 %) and 3 (6%) develop measles antibody titers, and the results of
were isolated from 6 of the 216 imported animals one challenge and control study indicated that pro-
mentioned above, but no clinical signs were ob- tection was conferred by both killed and attenuated
served. Parainfluenza virus type 3 infection was live virus vaccines [304].
found in six S. sp that died from bronchopneumonia
1-15 days after delivery from suppliers at whose Paramyxovirus saguinus. A disease caused by a para-
facilities it was thought infection may have oc- myxovirus distinct from measles caused high mor-
curred [108]. S. mystax experimentally infected tality in a colony of C. lacchus and S. oedipus
with passaged parainfluenza virus 3, strain HA-I, [ 170]. Affected animals had anorexia, diarrhea, and
had transient, mild clinical signs consisting of dehydration and usually died within 24 hours of the
sneezing, puffy eyelids, nasal discharge, and onset of signs. Other epidemiological features of
weight loss [213]. Virus was isolated from their the outbreak were not described. Gross lesions con-
throats for seven to ten days, and antibody was sisted of congestion and varying degrees of hemor-
detected two to three weeks after exposure. Sero- rhagic gastroenterocolitis and enlargement of the
logic surveys for parainfluenza virus (types I, 2, spleen, Peyer's patches, and mesentric lymph
and 3) in captive callitrichids have demonstrated nodes. Prominent microscopic lesions were necro-
antibodies, principally against type 3 [108,259] sis and inflammatory cell infiltration. The gastroin-
and, to a lesser extent, type 2 [260]. testinal mucosa was thin, and giant cells with intra-
nuclear inclusions were present. Giant cells were
Morbillivirus. Measles (rubeola) is a highly conta- also observed in the pancreatic ducts and acini, he-
gious disease that has been described in captive C. patic cords, and renal tubules. Intracytoplasmic and
jacchus. S. oedipus. and S. Juscicollis. associated intranuclear inclusion bodies were found only in
with high morbidity [296]. Clinical signs include syncytial cells in the bile ducts. Hyperplasia of the
edema of the upper eyelids and progressive lethargy lymph nodules and necrosis of germinal centers
culminating in death within 8-18 hours. Some ani- were observed in lymph nodules, spleen, and

194
Callitrichid diseases
Peyer's patches. Four s. oedipus were experimen- HAV, however, appeared to be S. mystax and S.
tally infected using the agent (Paramyxovirus sag- /abiatus because the initial recovery of virus was
uinus) isolated from splenic lymphocytes of a spon- high, and they produced more antigen suitable for
taneously infected tama'rin. They died or were use in immune adherence assays [232,394,462].
moribund 8-14 days after intramuscular intrave- The least satisfactory were C. jacchus, C. argen-
nous inoculation, and their lesions were character- tata, S. oedipus, and S. fuscicollis weddelli. The
ized as being more acute, necrotic, and hemor- incubation period following inoculation with hu-
rhagic than in natural infections. In addition, each man acute illness phase hepatitis A serum was ap-
had interstitial pneumonia. proximately 30-40 days, but serial passage in tam-
A serologic survey for P. saguinus antibodies arins resulted in a diminished incubation period
showed that 26 of 69 captive S. sp were positive, [127,240,241,271). HAV infection did not evoke
but the characteristics of the population studied clinical signs of illness in tamarins: Body weight,
were not described. It was postulated that callitrich- temperature, and hematocrit were unaffected. Diag-
ids are not the natural hosts for this virus, and that nosis of infection was based on serum chemical and
infection occured as a result of contact with another liver biopsy findings. Serologic responses consisted
species. of three- to tenfold elevations in serum alanine ami-
notransferase (ALT), serum aspartate aminotrans-
Mumps. Attenuated mumps virus, administered to ferase (AST), and serum isocitrate dehydrogenase
S. sp intranasally and subcutaneously, evoked anti- (SICD). Anti-HA V antibody was also produced as
body production similar to that seen in people, but a consequence of infection. Histologic findings in-
no evidence of disease. In serologic surveys, anti- cluded hepatic necrosis with lymphocytic infiltra-
body against human mumps virus was detected in tion in periportal areas and prominence of Kupffer
captive S. oedipus [260) and 23 of 63 marmosets cells. Hepatitis A antigen was identified in livers
[259). during the acute phase of infection by immunofluo-
rescence and electron microscopic and enzyme-
Other Paramyxoviruses. In two surveys of captive mar- linked immunosorbent assay techniques [284,311,
mosets [259) and Saguinus sp [108), serologic evi- 321). HA V was excreted in quantity in the feces for
dence of infection with the following antigens was 10-30 days, usually before elevations in transferase
not found: FM 1, respiratory syncytial, SV5, SV41, levels, and was detectable in the feces for 48 days
and mumps "s" and "V" antigens. after inoculation [372]. In one study, glomerulone-
phritis and arteritis, associated with hepatitis, were
reported in S. oedipus and S. labiatus [353]. Stud-
Picornaviridae ies demonstrated that multiple injections of the for-
Enteroviruses. The results of serologic surveys malin inactivated CR 326 strain of HA V evoked a
showed the presence of antibodies 'against the fol- specific anti-HA V response, and was effective in
lowing viruses in marmosets: Coxsackie 9; Echo 7, protecting S. labiatus from infection by live HA V
11, 12, and 13; SV 19; and SV 45 [259). In S. [393]. The same strain passaged in cell cultures,
oedipus, Coxsackie A 20; Echo 7, II, 12, and 13; yielded F and FI variants, both of which stimu-
SV 16; and SV 45 antibodies were present [260). lated antibody responses and protected S. labiatus
Negative findings were reported in surveys of mar- against infection [392]. The F variant was partially
mosets and Saguinus sp for: Coxsackie group B, virulent, and infection was associated with in-
Echo 3 and 4, Polio, and SV 4 [108,259,260). Cox- creased ALT levels, while the FI variant showed
sackie B2 virus was isolated from multiple tissues no evidence of virulence. These studies indicated
of three dead S. labiatus. When inoculated into se- the feasibility of developing a live attenuated hepa-
ronegative S. labiatus the agent produced infec- titis vaccine for use in humans.
tions, but no signs of disease [28).
Arenaviridae
Hepatitis A virus (HAV). Although HAV antibody was
found in three of six C. jacchus [128], viral hepati- Callitrichid hepatitis virus (CHV). Naturally occurring
tis A is not considered a spontaneous disease of hepatitis in one British and several U.S. zoological
callitrichids. Their susceptibility to experimental collections of callitrichids have resulted in the death
HAV infection, however, has been demonstrated of at least 50 animals [309,378,400). More than
repeatedly. Susceptible species are S. nigricollis half were L. rosalia, the remainder being L.
[107,127,372], S. oedipus [107,127,395], S.fusci- chrysome/as, S. fuscicol/is, S. nigricollis, S. impe-
collis [107,372,395], S. m. mystax [127,208,234, rator, S. oedipus, C. jacchus, and C. a. me/anura.
284,305,393,394], C. jacchus, and C. argentata Disease onset was acute, and the clinical course
[394]. The most satisfactory of these species, based was rapid. Clinically, there was dyspnea, anorexia,
on results of testing using the CR-326 strain of adipsia, and lethargy; in many cases, however, the

195
Potkay

animals died without premonitory signs. At nec- nantly hemorrhagic and included interstitial pneu-
ropsy, the lungs were congested and pale areas monia, meningoencephalitis, hepatic and lymph
were seen on the serosal and cut surfaces of the node necrosis, and decreased numbers of erythro-
slightly swollen livers. Other findings includedjaun- blasts and megakaryocytes in the bone marrow. The
dice, subcutaneous and intramuscular hemorrhage, use of homologous immune serum was found to
splenomegaly, and pleuropericardial effusions. Mi- reduce mortality in C. jacchus infected with the XJ
croscopically, the hepatic architecture was disorga- strain from 100% to 25%, but survivors displayed
nized; there was swelling and necrosis of hepato- late neurological signs including hyperkinesis or
cytes throughout the lobules and some infiltration hind limb paralysis [15]. Use of the antiviral agent
by lymphocytes and neutrophiles. Acidophilic bod- Ribavirin also reduced the mortality rate and de-
ies were also observed in the cytoplasm of degen- layed the time of death [504]. Marmosets given
erated hepatocytes. Less significant degrees of in- the attenuated XJCI3 strain of Junin virus had no
flammation and necrosis were present in the spleen morbidity or mortality, and were protected from
and lymph nodes. Experimental inoculation of three challenge with virulent virus [14]. Infection with
C. jacchus with cell-free filtrate obtained from an Tacaribe virus completely protected C. jacchus that
affected S. imperator produced anorexia and weak- were subsequently challenged with the XJ strain of
ness within a week: alkaline phosphatase, aspartate Junin virus for up to 240 days [422]. The spread
aminotransferase, and serum bilirubin levels were of Junin virus in tissues was minimal; subclinical
elevated [347]. The pathologic findings were the meningitis, lymph node hyperplasia, and pulmo-
same as in the naturally occurring cases, and virus nary, pancreatic, and renal glomerular inflamma-
particles (85-105 nm in diameter) were present tory changes were observed. The findings sug-
within vesicles of the RE reticulum and Golgi com- gested a potential role for live Tacaribe virus as
plex of hepatocytes. Immunological assays indi- a vaccine against Argentine hemorrhagic fever in
cated that the causative agent belonged to the Old humans. Evidence of naturally occurring Junin vi-
World family of arenaviruses and that it was closely rus infection in callitrichids has not been reported.
related antigenically to lymphocytic choriomeningi-
tis virus [454]. Although the source of callitrichid Machupo virus. The causative agent of Bolivian hem-
hepatitis was not determined, it was suggested that orrhagic fever produces illness and death when
the reservoir may be indigenous wild rodents, given subcutaneously or by skin scarification to S.
which are relatively common in zoos, or exotic geoffroyi [495]. Results following corneal installa-
Old World rodents (e.g., Mastomys and Paromys) tion were variable, and no clinically apparent infec-
maintained in zoological exhibits. Two veterinari- tions were seen following oral administration of the
ans who worked with CHV -infected callitrichids virus. Depending on the dose, death occurred II to
subsequently developed titers to the agent, but there 21 days later. Animals became inactive, weak and
were no signs of associated illness. anorexic one to three days before dying. Virus was
recovered from their brains, spleens, hearts, livers,
Lymphocytic choriomeningitis virus. Antibody to this kidneys, urine, and throat swabs. The significance
agent was found in one of 66 captive marmosets of tamarins in the epidemiology of this disease is
1259) and none of 50 Saguinus sp 1108) or four S. not known.
oedipus [260].
Tacaribe virus. Experimental infection of C. jacchus
with this agent produced no signs of disease, vire-
Junin virus. Susceptibility of C. jacchus to the caus- mia, or alterations in the hemogram, but neutraliz-
ative agent of Argentine hemorrhagic fever has ing antibodies appeared three weeks after infection
been determined experimentally [174,188,502, 1505].
503). Infections were characterized by progressive
depression; anorexia, weight loss, and death; some
animals had hemorrhages (petechiae and ecchymo- Togaviridae
ses), erythematous skin rash, muscular tremors, Simian hemorrhagic fever virus. This agent, a possible
and clonic muscle spasms terminally. Viremia oc- togavirus, was found in none of 14 captive S. oedi-
curred one to three weeks after intramuscular in- pus surveyed [260].
oculation; hematologic findings were normocytic
normochromic anemia, reticulocytosis, erythro- Alphaviruses. (Arbovirus Group A) Antibody has
blastosis, thrombocytopenia, and leukopenia. Vi- been found against several alphaviruses in captive
rus was present in blood, urine, and all tissues marmosets, which include Chikangunya, Semliki
sampled at necropsy. Lesions consisted of mul- Forest, and Sindbis 1259). Tests for Eastern and
tifocal hemorrhages, principally in the abdomi- Western equine encephalitis were negative in the
nal cavity, gums, pharynx, esophagus, and lymph above and other surveys of Saguinus sp [108] and
nodes. The histologic appearance was predomi- S. oedipus [259,260].

196
CalIitrichid diseases
Flaviviruses (Arbovirus Group B) midzonal region. Councilman's bodies similar to
those observed in human cases were observed only
Yellow fever. Yellow fever occurs naturally among in L. rosalia. Intranuclear inclusions were observed
wild marmosets and tam'arins [176,288,473,485]. in animals infected with certain of the South Ameri-
Alamada strains I, 2, and 3 and the Bomfin strain can strains, but were consistently found associated
of virus were isolated from C. j. penicillata in with Asibi and French strain infections.
Bahia, Brazil, and undesignated strains were recov- Although cebids, notably Alouatta, serve as
ered from S. o. geofJroyi in Panama. Numerous principal vertebrate hosts of sylvatic yellow fever
studies using South American strains have been in Central and South America, callitrichids can
performed that establish the susceptibility of caIIi- function in this capacity in their absence [177].
trichids to experimental yellow fever infection. The Consequently, yellow fever should be considered
O.C. strain was easily maintained by alternate as a potential source of mortality among captive
marmoset-mosquito (C. j. aurita-Aedes aegypti, specimens in endemic areas. While the human vac-
C. j. aurita-Hemagogus equinus, and C. j. cine may afford protection against infection, there
penicillata-H. equinus) passages [488,490]. A. ae- are no reports of its use in callitrichids. Failure to
gypti was found to be a more effective vector than identify yellow fever in imported laboratory mar-
H. equinus. Similar ease of maintenance was de- mosets and tamarins may be related to the short
scribed for the Alamada strain using C. j. penicil- interval between infection and death (four to eight
lata and L. r. chrysomelas with A. aegypti [489]. days) compared to the time required to trap and
Infections were generally fatal for Callithrix, while export them to the laboratory.
?one of the Leontopithecus succumbed. Naturally
Infected H. spegazzini were also able to transmit IIheus. This virus, which is transmitted by mosqui-
virus to C. j. aurita in the laboratory [488]. Subcu- tos, was infective for C. jacchus and C. j. penicil-
taneous inoculation of blood from rhesus (Macaca lata [2821. Viremia persisted for five to seven days
mulatta) monkeys infected with J.F., N.A.J., J.Z., following intracerebral, intraperitoneal, or subcuta-
O.C., A.C. Martinez, and A.C. Bolivian strains neous inoculation; signs of encephalitis were ob-
into C. jacchus, C. j. geoffroyi, and L. rosalia served.
?enerally produced lethal infections [287 J, Similar
Inoculations of the Asibi and French strains, which Dengue 1 and 2. Antibody to these agents was tested
are of African origin, into C. jacchus and L. rosalia for, but not found, in marmosets [259],
resulted in low death rates, but these strains were
fatal for C. j. geoflroyi and C. j. aurita [302]. St. Louis encephalitis. Neither captive marmosets nor
Deaths occurred in C. j. aurita and S. midas niger S. oedipus were found to have antibody against this
f?lIowing intraperitoneal and subcutaneous injec- agent [259,260].
tIons of infected blood and liver emulsions as well
as from transmission of the Asibi strain by A. ae- Uganda S. Marmosets were found to harbor antibody
gypti [94,488]. Virus of this strain could also be against this virus [259].
transmitted from C. j. jacchus to M. mulatta by
Stegomyia mosquitoes [941. Rubiviruses
Deaths among callitrichids attributable to yellow Rubella. Antibody to rubella (German measles) was
f~ver occurred within four to eight days of infec- detected in 7 of 73 captive marmosets [259], but
tIon. Clinical signs of illness were variable; weak- none of 24 S. oedipus [260].
ness was the most consistent observation, and a
few animals developed fevers, but jaundice rarely
Bunyaviridae (Bunyamwera supergroup)
occu~red. Gross hepatic lesions were variable de-
pendmg on the strain of virus and species involved Bunyaviruses. In 24 of 44 captive marmosets main-
[94,287]. Generally, there was congestion and in- tained in Panama, Venezuela, and the United
creased friability; surface coloration was reddish- States, antibody was detected against the following
~rown to red-yellow, and cut surfaces were some- viruses [259]: Bunyamwera group-Bunyamwera;
tImes yellow. Infrequently there was splenic California group-California encephalitis, Key-
~nlargement and renal congestion. When present, stone, LaCrosse, Tahyna, and Trivittatus; Simbu
Icterus was evident in the tarsal plates, kidneys and, group-Buttonwillow; Turlock group-Turlock.
less ~requently, in the aortic intima. Congestion of
the lIvers of Callithrix infected with South Ameri-
can .strains had parenchymal necrosis, fatty degen- Coronaviridae
eratIon, and cloudy swelling throughout the liver Coronavirus. Coronavirus-Iike particles have been de-
lobules. In L. rosalia infected with the African tected electron microscopically in bowel contents
strains, hepatic lesions were more restricted to the [479] and in the feces of one adult S. oedipus, but

197
Potkay

not in those of single specimens of S. fuscicollis or 1M or SC inoculation included fibrosarcomas, and


C. jacchus [439]. The significance of the findings mixed fibro- and rhabdosarcomas. Tumor develop-
is not known. ment was generally evident 23-90 days after inocu-
lation, and both the latency period and regression
rate were inversely related to the age of the host.
Rhabdoviridae
About 50% of infected callitrichids developed se-
Vesiculovirus. Neutralizing antibody was found rum neutralizing antibody, but Type-C virus parti-
against vesicular stomatitis virus (VSV)-Indiana in cles were not recovered from induced tumors. Tu-
75% of 12 and 9% of 96 S. geoffroyi tested in mors induced by SR-RSV in S. nigricollis younger
Darien and Panama Provinces, Panama [448]. than three months were not transplantable to alloge-
Tamarins with VSV complement fixing antibodies neic hosts [318]. Virus (RSV-M) rescued from
were also found in Darien Province. It was sug- these tumors by cocultivation with chic embryo fi-
gested that there may be a cycle of VSV infection broblasts, however, did induce neoplasms that en-
among arboreal wild animals, including nonhuman larged rapidly, metastasized, and killed young, but
primates, in addition to that which is normally not adult, tamarins within 29-59 days. These trans-
found in domestic livestock. Phlebotomine sand- plantable marmoset cell lines were suitable for in-
flies, and perhaps other insects, harbor VSV and vestigation of malignant transformation. Suscepti-
may be involved in transmitting the virus. No clini- bility of S. fuscicollis and S. oedipus to the Bryan
calor pathologic findings associated with VSV (Br-RSV) and Carr-Zilber (CZ-RSV) strains ap-
have been reported in tamarins or in cebids which, peared to be lower than to SR-RSV.
as a group, have a much higher percentage of ex-
posed individuals. Feline sarcoma virus (FeSV). This virus induced highly
invasive, ultimately fatal tumors that could be de-
Lyssavirus. Rabies has been diagnosed in single tected 28-46 days after intraperitoneal inoculation
specimens of S. nigricollis and Leontopithecus in neonatal S. fuscicollis [514]. Older tamarins
sp from Peru and Guatemala, respectively [1,408, were progressively less susceptible. The Snyder-
409]. Although the disease could have been con- Thielen strain (ST-FeSV) was associated with undif-
tracted by natural means in the source countries, it ferentiated or poorly differentiated fibrosarcomas,
was more likely the result of vaccination of these and the Gardener-Arnstein strain (GA-FeSV) with
pets using a live, attenuated rabies vaccine, since well-differentiated sarcomas. Type C particles were
clinical signs appeared within two weeks of immu- found in tumors induced by tumor cell inoculation,
nization. None of the rabies vaccines currently but not by viruses alone. Most tamarins in which
available in the United States are licensed for use tumors formed developed antibody against FeSV.
in wildlife species. Should antirabies prophylaxis
be considered necessary, consideration may be Woolly monkey sarcoma virus. This agent, called simian
given to using one of the killed virus vaccines de- sarcoma virus, type I (SSV-I) and Gibbon ape leu-
veloped for use in people and tested for efficacy in kemia virus, induced tumors with various histologic
nonhuman primates. characteristics depending on the site of inoculation
in neonatal S. fuscicollis, S. oedipus, and S. mystax
[398,514]. The latent period was three to six
Retroviridae
weeks, and well-differentiated, slowly progressive
Oncornavirinae. The numerous experimental studies fibrosarcomas or fibromas, which regressed in three
conducted in callitrichids to study the oncogenic to six months, resulted from intramuscular inocula-
effects of type C viruses have been reviewed in tion. Intracerebral inoculation was associated with
detail [398,513] and are briefly summarized below. glioma or astrocytoma formation.
Type 0 viruses have not been identified in calli-
trichids [158]. Baboon oncovirus. Intramuscular and intraperitoneal
inoculation of baboon endogenous virus (BaEV) in
Type C oncornaviruses. Callitrichids were used to S. oedipus, S. fuscicollis, and C. jacchus failed to
study the oncogenicity of one avian and five mam- produce clinical signs of infection or lesions [220].
malian viruses in this group, and were found to S. fuscicollis, but not C. jacchus developed serum
be quite susceptible to tumor formation following neutralizing antibodies to this agent.
experimental infection.
Murine sarcoma virus (MSV). S. oedipus, S. fuscicollis,
Rous sarcoma virus (RSV). S. nigricollis, S. oedipus and C. jacchus developed tumors one week after
and possibly C. jacchus are highly susceptible to inoculation with the Kirsten murine sarcoma-BaEV
the Schmidt-Rupert strain (SR-RSV) [297,364, pseudotype [220]. Although rare for a malignant
398,514]. The types of tumors induced following neoplasm to do so, the fibrosarcomas subsequently

198
CalIitrichid diseases
regressed; they were thought to be the result of the by brain preparations from CJD patients given
growth of inoculated tumor cells. Saguinus devel- intracerebrally [374,375]. The initial incubation
oped serum neutralizing antibodies to this agent, periods (43-54 months) were reduced (18-34
but Callithrix did not. . months) in subsequent serial passages. Signs of in-
fection and histologic features were similar to those
C-type virus HL-23VC. This agent, isolated from hu- described for kuru.
man myelogenous leukemia cells and cultured in
canine thymus cells, produced fibromas following Gerstmann-Straussler syndrome. Spongiform encepha-
intramuscular, but not intraperitoneal, inoculation lopathy, indistinguishable from that observed in
into neonatal S. f nigrifrons and S. f illigeri [35]. Creutzfeld Jacob disease, was seen in C. jacchus
Virus isolated from the tumors was indistinguish- 20-23 months after inoculation with brain prepara-
able from woolly monkey sarcoma virus type 1 tions from affected patients [415J.
(SSV-I). All treated tamarins developed antibody
against HL-23V, but showed no abnormalities in Syncytium-forming virus
their peripheral blood.
Peripheral lymphocytes and skin explant cultures
Simian immunodeficiency virus (SIV). C. jacchus and S. obtained from C. jacchus yielded a syncytium-
oedipus were susceptible to infection with SIV MND' forming virus that produced cytopathogenic effects
which was originally isolated from a mandrill in fibroblastic cell cultures [317J. Serum antibody
[344]. Both species developed low antibody titers against this agent was present in 55% of C. jacchus.
within two weeks of inoculation, and virus was re- but in none of the S. oedipus maintained in the
covered from Saguinus from two to nine weeks colony.
after inoculation. No clinical signs of infection
were evident. Hepatitis
Hepatitis virus B. Results of a serologic survey of six
Other. Examination of C. jacchus uteri collected 13, captive C. jacchus and 12 S. oedipus were negative
16, 19, 23, and 31 days after ovulation revealed for hepatitis B surface antigen [128 J.
that C-type viral particles were consistently present
in large numbers on the plasma membranes of the Hepatitis non-A, non-B. S. nigricollis and S. fusci-
syncytiotrophoblast where it was in contact with collis. inoculated with marmoset-passaged GB
the cytotrophoblast [438]. It was suggested that that strain of non-A, non-B human hepatitis, developed
particles, which were found only at this site, may elevated SGPT levels and histologic evidence of
?e endogenous components of the genome having hepatitis after a mean incubation period of 17 days
Immunosuppressive properties that permit cell fu- [3721. Infections lasted for two or three weeks but
sion during syncytiotrophoblast development and none of the tamarins seroconverted. S. labiatus
locally suppress the maternal response in the pla- responded to intravenous inoculation of infected
centa. The viral particles were not considered to be human blood products with an increase in alanine
horizontally transmitted infective agents. aminotransferase (ALT), which began 7 days and
peaked 15 days after injection [263,464 J. Hepatic
necrosis was limited to small intralobular foci asso-
Slow viruses
ciated with mononuclear cell infiltrates. S. mystax
Kuru. Intracerebral inoculation of brain preparations and S. labiatus were also susceptible to Strains F
from human kuru patients induced disease in S. and H derived from acute and chronic cases of
oedipus. S. fuscicollis. and S. nigricollis after a non-A, non-B, but the incubation periods varied
26-94 month incubation period [183,374,375J. widely and were prolonged [147J. Microscopically,
The incubation period was markedly reduced subse- liver cells were characterized by degeneration, bal-
quent to serial passage in neonatal tamarins. Clini- looning, and cytoplasmic clumping. Unlike the
cal signs of infection were progressive and included case in lesions of hepatitis A, inflammation was
tremor, incoordination and ataxia, reduced tactile more evident in portal as compared to intralobular
res~onse, aggression, and impairment of vision; areas. Lesion development was closely associated
theIr.duration was about two weeks. Typical micro- with increases in serum AL T and isocitrate dehy-
SCOpIC lesions consisted of spongiform polioen- drogenase (SICD) levels. Electron microscopic ex-
cephalopathy of the cerebrum and spinal cord, and amination of hepatocytes of S. mystax and S. /a-
cerebellar spongiosis, with loss of Purkinje and biatus with acute hepatitis induced by inoculation
granular cells. with infected human sera demonstrated attached,
membrane-like structures in the cytoplasm [494].
Creutzfeld-Jacob disease (CJD). S. oedipus and S. fusci- They enclosed electron dense material between
collis (or nigricollis) were susceptible to infection them.

199
Potkay

Enterically-transmitted non-A, non-B hepatitis. Enterically Clostridium. Twenty-nine deaths in a C. jacchus col-
transmitted non-A, non-B hepatitis (ET-NANBH) ony were attributed to Clostridium perJringens A
is an emerging form of viral hepatitis with a particu- overgrowth following extensive prophylactic treat-
larly high incidence in parts of Africa and Asia ment against Shigella with gentamycin and furox-
[50,51]. Intravenous inoculation of S. mystax with one: Large numbers of the organisms were isolated
acute phase stool suspension from patients with from the gastric contents of 25 marmosets that were
ET-NANBH resulted in liver lesions characteristic examined [449]. Clinical signs were anorexia and
of acute viral hepatitis and elevated serum ALT intermittent diarrhea for three to five days before
and SICD levels. Virus-like particles (27-34 nm) death. The ventral abdominal and cervical subcu-
similar to those found in human cases were excreted ticular tissues were edematous and contained gas.
in early acute phase stools of infected tamarins. The gas-filled gastrointestinal tracts contained light
Because disease production was more consistent brown fluids, and the mucosa of the jejunum and
and the incubation period was shorter in M. Jascicu- ileum was hyperemic. Microscopically, the intesti-
laris and M. mulatta than in tamarins, the former nal lesions consisted of hyperemia, loss of mucosal
species were considered better models [517]. epithelium and thickening of the lamina propria.
Individual deaths, unassociated with antibiotic ther-
apy, may also result from C. perJringens [46]. C.
Marburg virus
perJringens was isolated from the throats of 8% of
None of 14 captive S. oedipus carried antibody recently imported Saguinus sp, but not from accli-
against this agent [260]. mated tamarins [108].

Encephalomyelitis Bacteroidaceae

A filterable, presumably viral agent was isolated Bacteroides. Bacteroides pseudotuberculosis roden-
from Callithrix sp with clinical signs of saliva- tium and Bacteroides aertrycke were associated
tion, convulsions, strabismus, and paresis [6]. It with deaths at parturition in two C. jacchus [308].
produced similar signs in marmosets and mice
inoculated intracerebrally. Microscopic findings Brucellaceae
including lymphocytic perivascular cuffing, micro-
hemorrhages, and glial proliferation. Gross lesions Bordetella. Bordetella bronchiseptica caused sudden
were absent. death in 16 marmosets, all but one of which was
less than one year old, in a breeding colony of C.
jacchus [27]. The colony had been established as
Bacterial diseases B. bronchiseptica-free three years earlier. Clinical
Bacterial infections are common in captive calli- signs were minimal and consisted of mucopurulent
trichids, and some are major contributors to illness nasal discharge and fever (I-2°C); some animals
and death. Much of the information available about became dyspneic when handled. At necropsy, vari-
the bacterial flora of captive species is derived from able pulmonary congestion and consolidation were
surveys of tamarins conducted soon after importa- noted, and six marmosets had fibrinopurulent vis-
tion [108,354]. Very little is known of the inci- ceral pleurisy and thickened pericardia. Micro-
dence of bacterial infection in free-living callitrich- scopic lesions were acute purulent bronchopneumo-
ids. Bacteria that have been identified are arranged nia and edema of the bronchial lymph nodes. Less
according to Bergey [34] and discussed below. frequently, rhinitis, fibrinopurulent pericarditis,
and necrotic laryngitis were observed. B. bronchi-
septica was isolated from the lungs of all animals
Eubacteriales that died; Proteus sp and Pseudomonas aeruginosa
were also isolated from several of them. Coloniza-
Achromobacteriaceae
tion of the nasal mucosa by B. bronchiseptica oc-
Alcaligenes. A. faecalis was isolated from the stools curred in 71 of 156 marmosets in this susceptible
of both recently imported (7%) and acclimated popUlation. Treatment with oxytetracycline halted
(4%) Saguinus sp [108]. the progression of clinical signs in adults, but did
not eliminate the organism from the nasal passages.
Bacillaceae An autogenous B. bronchiseptica vaccine has been
used in C. jacchus colonies, but there were no re-
Bacillus. Bacillus sp isolations from the throats of ports of its efficacy [69].
newly imported Saguinus sp were low (8%), and
there were none following a period of acclimatiza- Franciscella. Tularemia was observed in one C. j.
tion [108]. geoffroyi at a California zoo, and in four of nine

200
Callitrichid diseases
Saguinus nigricollis maintained in a Canadian zoo- observed in S. mystax and S. nigricollis shortly
logical garden [357]. Three of the tamarins were after importation [354).
found dead or moribund; ,one showed signs of de-
pression and responded to parenteral treatment with Enterobacter (Aerobacter). Enterobacter sp was com-
oxytetracycline, ampicillin, and B vitamins. Le- monly isolated from the throat and feces of newly
sions consisted of splenomegaly, enlargement of imported S. nigricollis and S. mystax, but signs of
mesenteric lymph nodes, slight hemorrhage into the disease were not observed (354).
intestines, and a fibrinous peritoneal exudate. Small
white spots in the spleen and liver were foci of Escherichia. Coliforms were routinely isolated from
caseous necrosis. Varying degrees of lymphadeni- the feces of Saguinus sp during quarantine, but the
tis, enteritis, acute glomerulitis, and pneumonitis isolation incidence of E. Jreundii diminished mark-
were also present. F. tularensis was isolated from edly in acclimated tamarins [108,354]. Among
the Franklin's ground squirrels (Spermophilus Saguinus, hemolytic strains of E. coli were consid-
Jranklinii) trapped near the primate facility. The ered to be important pathogens, causing a watery
agent was also identified in a ground suspension of diarrhea [274]. Lesions consisted of congestion,
fleas (Orchopeas sp) collected from the squirrels. edema, and necrosis of the mucosa of the ileum
The importance of rodent and vector control is ex- and colon. The efficacy of routine immunization
emplified by this outbreak, and the occurrence of against E. coli practiced in C. jacchus colonies has
tularemia in a veterinarian, bitten while examining not been described (69).
the sick tamarin, emphasizes the public health sig-
nificance of this disease. Klebsiella. Klebsiella pneumoniae is an important
pathogen in callitrichids [28,33,74,109,247,287).
Pasteurella. Because of its importance in other New Among newly arrived, wild-caught Saguinus sp,
World monkeys, Pasteurella multocida was consid- Klebsiella was isolated from the throats of 64% and
ered to be a potential pathogen in callitrichids was associated with pneumonia, septicemia, and
[247]. enteritis [\08]. The organism has also been recov-
ered from skin lesions [109]. Thirteen percent of a
Corynebacteriaceae Callithrix j. jacchus breeding colony succumbed to
Klebsiella sp infection in Brazil [60]. Clinical signs
Corynebacterium. Coryn. equi was isolated from a included diarrhea and hypothermia, and young ani-
pulmonary abscess in I of 15 wild-caught S. oedi- mals were affected more often than adults. Nec-
pus [452]. Clinical signs included anorexia, labored ropsy observations included gaseous distension of
respiration, weight loss, and general unthriftiness. the small intestine, which was also congested. The
Treatment with tetracycline (PolyoticTM, Soluble liver in some cases was enlarged and the surface
POWder American Cyanamid Co, Princeton, NJ), had diffuse yellow areas. All of the lesions exam-
parenteral fluids, and liquid diet was ineffective. ined histologically were characterized by intense
Histologically, the lesion was characterized as pyo- congestion with the presence of mono- and poly-
granulomatous bronchopneumonia and necrotic morphonuclear leukocytes, indicating that septice-
pleuritis. Granulomatous pancreatic serositis and mia was the cause of death. The outbreak was
fibrinopurulent epicarditis were also present. halted after instituting strict hygienic measures and
treatment with kanamycin, chloramphenicol, and
ErySipelothrix. Acute, fatal Erysipelothrix rhusiopath- cephalosporin-aminoglycoside intramuscularly for
iae infection was reported in an eight-month-old S. 8-12 days. An autogenous Klebsiella sp vaccine
nigricollis [235]. Clinical signs were depression, has been used in C. jacchus colonies, but there are
dehydration, weakness, and hyperthermia; pain was no reports of its efficacy [69].
elicited by abdominal palpation. Bacteria were ob-
served in skeletal and cardiac muscle, lymph nodes, Proteus. The incidence of Proteus sp isolation from
and kidneys, but not in the liver or lungs; there was the throats (28%) and stools (81 %) of newly im-
little or no tissue reaction. The source of infection
ported Saguinus sp was high [108]. Evaluations
was not identified, but the tamarin had been housed
conducted 3-12 months later showed a markedly
in the enclosure with chickens and other primates
reduced incidence of pharyngeal isolations (12%)
(Erythrocebus patas, Hylobates lar, and Saimiri
and a small decrease in fecal isolations (78%). In
sciureus). The organism was not found in samples
another study, Proteus sp was also found in S. mys-
of soil from the cage, water, or food.
tax and S. nigricollis with some regularity [354].
Enterobacteriaceae While it is often difficult to determine the role of
this genus as a cause of enteritis, P. rettgeri and P.
~itrobacter. A low incidence of Citrobacter sp isola- morgani have been identified as pathogens in cap-
hon from stool specimens and throat swabs was tive Saguinus [274 J.

201
Potkay

Serratia. This organism was isolated from the throats pulmonary congestion. Histologically, the periph-
of 0.80% of recently imported Saguinus sp [108]. ery of the ulcers were hemorrhagic, and the intesti-
nallamina propria contained mononuclear cells and
Salmonella. Numerous species of Salmonella have neutrophiles. Shigella sonnei was isolated from
been identified in fecal specimens from Callithrix 9.2% of the fecal samples tested, and from 44% of
sp imported into the United States. These species the animals necropsied. Containment and elimina-
include S. typhimurium, S. anatum, S. seftenberg, tion of the disease was accomplished by imposing
S. newington, S. oranienburg, and S. habana quarantine procedures and providing neomycin sul-
[265]. Salmonella was also isolated from the feces fate (Neobiotic™, Upjohn, Ltd, Crawley, Sussex,
of 19% of newly imported Saguinus sp [108], and England) (6 ml per 310 ml of drinking water) for
3% of S. nigricollis [354]. Salmonella species ob- ten days. S. sonnei was also found in 11% of 60
tained from normal tamarins were: S. derby, S. Callithrix sp, and was fatal in 7% of newly im-
stanley, S. st. paul, S. oranienburg, and Arizona ported S. mystax and S. nigricollis [354]. It was
sp. The types that were found associated with dis- identified as the cause of death in four C. jacchus
ease included S. california, S. heidelberg, S. oslo, maintained in a British zoo associated with gastro-
S. stanley, S. derby, S. thompson, S. javiana, S. enteritis and septicemia [153] and from one Cal-
panama, and S. typhimurium. Two isolates of Ari- lithrix sp imported into the United States [265].
zona sp were obtained from callitrichids during an Shigella fiexneri [103] was recovered from one
outbreak of shigellosis [85]. Salmonellosis may oc- Saguinus leucopus, which died with dysentery at a
cur as a mixed infection with Shigella. The results zoo [232]. No Shigella were isolated from a breed-
of a survey of 27 S. mystax from a breeding colony ing colony of 27 S. mystax in Peru [421].
in Peru were negative for Salmonella [421].
The primary clinical finding in salmonellosis Yersinia. Y. enterocolitica was reported in twelve
is enterocolitis, characterized macroscopically by wild-caught C. jacchus and C. j. penicillata main-
congestion, hemorrhage, and edema of the mucosa. tained in a Brazilian zoo for one to seven months
Microscopic lesions also include focal necrosis of [184,345] and in three C. jacchus, one C. ar-
the intestine and, sometimes, the liver and spleen gentata, and one S. oedipus in European zoos
[274]. [270,384]. Affected animals generally died acutely
In the laboratory, infections, particularly in and briefly showed signs of lethargy; profuse diar-
younger animals, may be associated with contami- rhea was observed in one. Typical findings at nec-
nation of commercial feed, and have been treated ropsy were splenomegaly, multiple splenic and he-
with kanamycin (KantrexTM, Bristol Laboratories, patic abscesses (approximately 0.5 em in diameter),
Division of Bristol-Meyers Co, Syracuse, NY), ulcers, and necrosis in the jejunum, ileum, and co-
chloramphenicol (ChloromycetinTM, Parke, Davis lon, and enlargement of the mesenteric lymph
& Co, Detroit, MI), and ampicillin (Omnipen TM, nodes. Histologically, there were large foci of
Wyeth Laboratories, Philadelphia, PA) [74]. The hepatic inflammation; bacteria were seen at the
frequency with which Salmonella can be isolated periphery of the lesions. Necrosis in the colon
from clinically normal callitrichids is of zoonotic was sometimes extensive. Y. pseudotuberculosis,
significance for individuals who handle them. thought to be introduced in contaminated feed,
caused the death of 6 of 35 S. labiatus in a breeding
Shigella. Shigellosis is an important pathogen in cal- colony [465]. Clinical signs and necropsy findings
litrichids and may occur as a mixed infection with were similar to those described for Y. enteroco-
Salmonella. An extensive outbreak of shigellosis litica.
involving a laboratory colony of 50 C. jacchus and
S. nigricollis has been described [85]. Acute or per-
Lactobacillaceae
acute illnesses were characterized by depression,
lethargy, anorexia, hunched posture, and bloody Streptococcus. Strep. (Diplococcus) pneumoniae was
diarrhea, and by subnormal temperatures and pale cited as a potential pathogen of callitrichids because
mucous membranes prior to death. Affected ani- of its ability to cause pneumonia and meningitis in
mals were generally in good condition, though de- other New World monkeys [247]. Recovery of
hydrated. Principal lesions were seen in the cecum Strep. sp from pharyngeal swabs of Saguinus sp
and colon. The cecum contained ulcers (0.5-3.0 shortly after importation and 3-12 months later,
mm) and pinpoint hemorrhages, and some animals respectively, was: ex Strep., 84% and 90%; 13
had small erosions and petechiae of the colon. Strep., 11 % and 3%; and 'Y Strep., 41 % and 45%
Blood and fluid feces were seen in the cecum, co- [108]. S. I. labiatus had poor antibody responses
lon, and rectum. Regional lymph nodes were edem- to experimental infection with Strep. pneumoniae
atous and sometimes hemorrhagic. Lesions in other (serotype 7F) and to pneumococcal capsular poly-
organs were mild, consisting mainly of hepatic and saccharide vaccine [73]. Preopsinization of Strep.

202
Callitrichid diseases
pneumoniae with human immune globulin or ad- acclimatized C. jacchus of both sexes [175]. Or-
ministration of the globulin 30 minutes prior to giv- ganisms were present in the throats of all 41 mar-
ing a lethal challenge wjth serotype 7F afforded mosets; 27% of prepucial and 26% of vaginal cul-
protection. tures were positive. Of 30 infants from infected
Streptococcus zooepidemicus septicemia was the family groups, 8% had mycoplasmas in their oro-
cause of death in S. labiatus and Callimico goeldii pharynges within 24 hours of birth, and all had the
housed in zoological exhibits [426]. Clinical signs organism by one week of age. Ureaplasms have
included abdominal distension, submandibular also been isolated from the kidneys and urinary
swelling, diarrhea, fever, and elevated white blood bladder of Saguinus sp and Callithrix sp [43]. Ex-
cell count. Lesions consisted of suppurative sub- perimental intravaginal inoculation of C. jacchus
mandibular and retropharyngeal lymphadenitis, with Ureaplasma urealyticum (strain G-37) of hu-
splenitis, and suppurative hepatitis. Beta-hemolytic man origin produced infections in four of six ani-
Strep. zooepidemicus was isolated from the liver, mals [473]. Organisms were recovered for 10-21
spleen, ascites fluid, and heart blood, as well as weeks, and although no frank vaginal discharge
from cultures of horse meat products and containers was observed, a polymorphonuclear leukocyte re-
used to feed three-banded armadillos, which were sponse was seen two to four weeks after inocula-
part of the exhibit. It was recommended that un- tion, and antibody titers increased fourfold.
cooked horse meat be routinely cultured and that
~trict sanitation practices be implemented when it Mycoplasma. Antibody against Mycoplasma pneu-
IS necessary to feed this product to exotic species. moniae was detected in I of 15 captive S. oedipus
at a zoo [260J. Experimental intravaginal inocula-
Enterococcus. The isolation rate of this agent from tion of S. mystax and C. jacchus with M. genitalium
~he throats of Saguinus sp was 3% among recently (Strain G-37) resulted in low-level infections of the
~mported tamarins, and 0% among acclimatized an-
genital tracts that persisted for at least two months
Imals [108].
and evoked serum antibody responses [474,475,
Micrococcaceae 483]. Intraoviductal inoculation in C. jacchus pro-
duced salphingitis and an antibody response [483].
Micrococcus. Twenty-three percent of recently im-
ported S. fuscicollis and S. oedipus carried this or- Neisseriaceae
ganism in their throats and continued to harbor it
for 3-12 months [108]. Neisseria. The incidence of Neisseria sp isolations
from the throats of Saguinus sp was 57% during
?~aphYlocOccus. S. oedipus and S. fuscicollis had pos- and 77% after quarantine [108].
ItIve throat cultures for coagulase positive (16%)
~nd coagulase negative (28%) Staph. shortly after Pseudomonadaceae
Importation; the incidence declined (to 12% and
Pseudomonas. A high incidence of Pseudomonas sp,
10%, respectively) after acclimatization [108]. isolated from rectal swabs (23%) and throat cultures
Staph. sp was isolated from the lungs of a Saguinus (II %) was reported in newly imported Saguinus sp
sp that died of bronchopneumonia [109].
[108], and from the same sites in S. nigricollis
[354]. The organism is considered to be an impor-
Actinomycetales tant cause of bronchopneumonia, particularly in de-
Mycobacteriaceae bilitated animals, and cannot be eliminated even
from conditioned colonies [74,108,265]. Empy-
Mycobacterium. Tuberculosis is uncommon in calli- ema, vegetative endocarditis, pancarditis, and sep-
trichids, which have been said to be highly resistant ticemia have been reported in association with
to infection [169,199 J. The disease has been seen Pseudomonas infection [I 09J. Pseudomonas sp was
at European zoos in two C. jacchus [143,245,484], also isolated from five callitrichids during an out-
two L. rosalia [90] and one C. penicillata [231] break of shigellosis (q. v.) [85]. Carbenicillin
that had resided in collections from 14 to 48 (Geopen TM, Roerg, Division of Pfizer Pharmaceuti-
months. Both avian and bovine types of M. tuber- cals, New York, NY), gentamicin (Garamycin™,
culosis were identified. Abdominal lesions were ob- Schering Corp, Kenilsworth, NJ), and colistin
served in two cases, and a pulmonary lesion in one. (Coly-Mycin™, Bristol Laboratories, Division of
The source of infection in one case was thought to Bristol-Myers Co, Syracuse, NY) have been used
be from raw eggs. to treat infections [74].
Mycoplasmataceae Legionellaceae
Ureaplasma (T-mycoplasma). Ureaplasmas were iso- Legionella. Aerosol infection of C. jacchus with Le-
lated from the throats of both newly captured and gionelia pneumophila, the agent of Legionnaire's

203
Potkay
disease, resulted in clinical signs consisting of fe- kanamycin) and sulfonamide treatment was unsuc-
ver, anorexia, and lethargy for one to six days [25]. cessful, but one tamarin responded within ten days
One of four marmosets had respiratory distress and to topical applications of emacridine lactate (Riva-
became moribund. Lesions were found only in the nol™, Chinosolfabrik der Riedel de Haen AG,
lungs and consisted initially of pinpoint hemor- Seelze, Germany).
rhages that became consolidated and affected two-
thirds of the lung tissue. Characteristic microscopic Leptospira
findings were bronchopneumonia involving ter-
Leptospira. Spontaneous leptospirosis has not been
minal and respiratory bronchioles; alveoli were
observed in New World primates, but experimental
edematous and contained fibrin, red blood cells,
Leptospira icteroides infections in S. oedipus and
and polymorphonuclear leukocytes. Within 10-17
S. o. geoffroyi were characterized by inappetence,
days, lesions began to resolve spontaneously. Re-
fever, jaundice, convulsions, and death [362]. Nec-
sults of a serologic survey of S. oedipus indicated
ropsy findings included minimal hemorrhagic le-
that 1 of 15 had antibody to L. pneumophila, but
sions in the lungs, heart, small intestine, and colon.
the significance of this finding was not clear [216].
Result of serologic surveys of 35 captive S. oedi-
pus, S. mystax, and S. nigricollis showed that only
Spirillaceae
one S. oedipus had antibody against L. bal/um
Campylobacter. Sixteen of 38 marmosets examined [341]. It was believed that this tamarin acquired the
in one colony harbored Campylobacter fetus subsp infection after importation, probably from exposure
jejuni in their intestinal tracts [262], and C. jejuni to infected wild mice.
was isolated from 10 of 15 S. mystax with diarrhea
in a Peruvian colony [421]. C. jejuni was also iso-
Rickettsial and chlamydial diseases
lated from one of three C. penicillata and none of
six Saguinus sp in a Brazilian zoo; there was no Rickettsiales
associated illness [149]. Sensitivity testing of C.
Rickettsiaceae
jejunilcoli obtained from captive S. oedipus indi-
cated that erythromycin was most effective, fol- Coxiella (Rickettsia) burnetti. Of 15 S. oedipus exam-
lowed by doxycycline and chloramphenicol, but ined at a zoo, 40% carried antibody against C. bur-
therapy should be based on the results of isolation nefti, the causative agent of Q-fever [260]. Anti-
and sensitivity testing [167]. body was not found in the sera of 55 newly
imported S. sp [108].
Spirochetales
Rickettsia akari. None of 23 captive S. oedipus carried
Treponemataceae antibody to this agent, which causes rickettsialpox
in man [260].
Borrelia. Naturally occurring infection of S. o. geof-
froyi with spirochetes, presumably Borrelia recur-
Rickettsia prowazekii. Antibody against the agent of
rentis, was studied in a relapsing fever area of Pan-
epidemic typhus, R. prowazekii, was absent in zoo-
ama [78]. The agent was morphologically similar
logical specimens of S. oedipus [260J.
to the human spirochete, and did not grow in cul-
ture. It produced transient infections in Cebus ca-
Rickettsia rickettsii. Antibody against this agent,
pucinus, Ateles geoffroyi, and Aotus trivirgatus,
which causes Rocky Mountain spotted fever, was
and more severe infection in Saimiri sp, rats, and
not demonstrated in a survey of newly imported
mice. Disease was produced in humans inoculated
Saguinus sp [108], or in wild-caught S. oedipus
with blood from infected monkeys.
residing at a zoo [260].
Noma. Noma (Cancrum oris, stomatonecrosis) was
Rickettsia typhi. In a survey of captive S. oedipus,
described in two captive S. oedipus [46J. Lesions
none had antibody against the causative agent of
consisted of ulcers that appeared suddenly on the
endemic (murine) typhus [260].
cheek and corner of the mouth and quickly involved
underlying soft tissue. Each animal had preexisting
gingivitis, periodontitis, and calculi on the canine Chlamydiales
and incisor teeth. Histologically, there was exten-
Chlamydiaceae
sive coagulation necrosis of the affected labial and
gingival tissue that extended into the maxilla. Nu- Chlamydia. Naturally occurring chlamydial infection
merous fusiform and spirilliform bacteria were ob- has not been reported in caIlitrichids, but the exper-
served, and micrococci, streptococci, and Proteus imental susceptibility of C. jacchus to Chlamydia
sp were isolated. Antibiotic (chloramphenicol and trachomati has been demonstrated [253,254,255].

204
Callitrichid diseases
Vaginal inoculation with strains 78 alpha (serotype most of the trypanosomas reported in callitrichids
DIG) and UW4 (serotype H) resulted in an acute are probably T. cruzi and T. minasense. T. cruzi
polymorphonuclear leucocytic reaction within three has been identified in wild C. jacchus, C. j. geof-
days, and the appearance of small numbers of in- froy, c. argentata melanura, c. j. penicillata, S.
tracytoplasmic chlamydial inclusions in epithelial midas niger, S. mystax, and L. rosalia in Brazil
cells from vaginal smears within eight to ten days. [92,99,100,112,124,306,337,406,456]; S. nigri-
Chlamydiae were isolated for 10-42 days, and IgM collis in Peru [124]; S. midas in French Guiana
and IgG antibody levels increased significantly [124]; Cebuella pygmaea, S. fuscicollis, S. mystax,
within 24-27 days of inoculation. Infections lasted S. oedipus, and S. /eucopus in Colombia [319];
only three to seven days in animals reinoculated S. geoffroyi in Panama [124]; and in captive S.
with the same or different strains; the anamnestic nigricollis, S. oedipus, S. fuscicollis, and S. /a-
~esponse was not serotype specific. The infection biatus [108,268] and Leontopithecus sp [268]. Nat-
In marmosets was similar to that produced by chla- ural hosts for T. minasense included: C. j. penicil-
mydiae in women. lata in Argentina and Paraguay [456); C. j. jacchus
and C. j. geoffroyi in Brazil [212,356,407]; S. oedi-
PSittacosis. Antibody against the agent of psittacosis pus in Colombia; S. nigricollis and C. pygmaea
Was not detected in a serologic survey of 22 captive in Peru [124]; and S. geoffroyi in Panama [178].
s. oedipus [260]. Undesignated trypanosomes have also been ob-
served in captive C. humeralifer [200J, S. o. geo.r
froyi, S. nigrico/lis, S. mystax [305], and C. jac-
Protozoan diseases
chus (83).
Infections by protozoans, particularly trypanoso- Isolates of T. cruzi were pathogenic for suckling
mas, are frequently seen in captive callitrichids, but mice. The time between infection and the appear-
clinical illness and mortality are rarely attributed to ance of parasites in the blood (prepatent period)
them. was short, followed by parasitemia, development
of tissue leishmanial forms, and variable mortality
Mastigophora [ 121 ,406), and they developed normally in the vec-
tor, Triatoma protracta [124]. Mice that recovered
Hexamitidae and Trichomonadidae from infection had a high resistance against reinfec-
tion by the Y strain of T. minasellse. T. cruzi, on
Giardia and Trichomonas. Giardia sp and Trichomonas
the other hand, was not pathogenic for mice and
sp are frequently cited as inhabitants of the intesti-
did not develop in T. protracta [124).
nallumen of call it rich ids [108,218,247,252). They
Although clinical signs of trypanosomiasis have
do not incite an inflammatory response, and while
not been observed in callitrichids, this may be re-
large numbers may be found in animals with diar-
lated to the paucity of surveys in which callitrichids
rhea, they are not necessarily the cause of the diar-
have been identified and examined in acute stages
rhea [55]. Giardiasis may be treated with quinacrine
[10 1]. Latent T. cruzi infections in animals that
or chloroquine; environmental sanitation is required
are stressed, however, may produce effects [124].
to prevent reinfection [156).
Lesions in affected callitrichids are usually inciden-
tal findings at necropsy and include foci of leish-
Trypanosomatidae
mania in the heart, liver. spleen. brain. and intes-
Trypanosoma. Chagas' disease (American trypanoso- tine [10 I). Focal infiltrations of monocytes were
miasis) is a major health problem in areas of Latin also seen in the livers of tamarins with heavy try-
America. The causative agent is the hemoflagellate, panosomal infections [109].
Trypanosoma cruzi, whose vertebrate hosts, in ad- The public health significance of T. cruzi infec-
dition to man, include several genera of neotropical tions in callitrichids is twofold. Since their rate
n?nhuman primates. Triatomid bugs act as interme- of natural infection is high and because they are
diate hosts, and infection may be acquired from commonly kept as pets in areas where triatomid
their bites or feces, or by ingesting them. Try- bugs exist. C. jacchus may be involved in the trans-
~anosomas are sometimes observed during rou- mission of trypanosomiasis to human beings [406].
tme examinations of callitrichid blood, but because Naturally infected animals are also potential
parasitemias are usually low, infections may be sources of infection to persons who work with them
ove~loo~ed unless parasites are sought or in vitro in laboratories and zoos [124).
cultIvatIOn or xenodiagnostic techniques are used.
Identification of Trypanosoma species is often dif- Leishmania. Leishmania brasiliensis was isolated
ficult. b~cause their morphologic and mensural char- from a wild S. geoffroyi in Panama using skin culti-
actenstIcs vary depending on the hosts from which vation techniques [178]. There were no lesions or
they are recovered. Using established criteria [ 124], clinical signs of disease. The agent produced typi-

205
Potkay

cal dermal lesions when inoculated into hamsters, infection in S. geoffroyi [427]. Clinical and patho-
and blood from the tamarin was infective for Phle- logic findings were not given. In other species,
botomus sanguinarius. Experimental infection with however, white, spherical cysts (approximately 1
L. brasiliensis resulted in nodule development at mm in diameter) are frequently found in the heart,
the injection site in seven of eight inoculated C. lungs, kidneys, tongues, skin, and skeletal muscle.
jacchus, ulceration in six of seven, and metastatic
lesions in three animals [91]. All developed posi- Besnoitia-like. Coccoid oocysts were described in a
tive skin tests and IgG antibody. single, Besnoitia-like, subcutaneous cyst in a S. oe-
dipus [388].
Sarcodina
Cryptosporidium. Oocysts of Cryptosporidium sp
Entamoebidae were identified in the feces of a captive S. oedipus
with diarrhea [225].
Entamoeba. Entamoeba coli has been identified in C.
jacchus, S. oedipus, S. fuscicollis, and S. nigri-
collis, but is apparently nonpathogenic [157,286]. Toxoplasmidae
It has been transmitted experimentally to man and
macaques, and strains of E. coli from the latter are Toxoplasma gondii. This intestinal coccidian parasite
infective for C. jacchus [313]. Entamoeba histolyt- is widely distributed throughout the world, and fe-
ica, however, may cause varying degrees of hem- lids are its final hosts. Although other vertebrates
orrhagic ulcerative colitis, typhlitis, and ileitis in serve as intermediate hosts, they are not necessary
callitrichids [113]. Infection with an unidentified for the parasite to complete its life cycle. In addi-
species of Amoeba (not histolytica or coli) was as- tion, certain insects can serve as transport hosts.
sociated with diarrhea and terminal lethargy in S. Oocysts are shed and subsequently develop into two
oedipus [168]. In macaques, the following drugs sporocysts containing four sporozoites each. Infec-
have been used to treat E. histolytica infections: tions are acquired by ingestion of sporulated 00-
carbasone (7.5 mg/kg for ten days via stomach cysts, ingestion of infected animals that contain
tube), diodopquin 0.2 mg/day for eight days by bradyzoites, or transplacental transmission.
stomach tube), fumagillin (50-125 mg/day for five Based on serologic surveys, toxoplasmosis ap-
to ten days), and emetine [55]. Use of these agents pears to be common among wild cebids in Brazil
has not been reported in callitrichids. [150,444), and spontaneous infections have been
described in five genera of captive Cebidae [20].
Results of surveys of C. jacchus, C. j. penicillata,
Sporozoa and C. j. geoffroyi maintained at Brazilian research
and zoological facilities [359], wild-caught S. oedi-
Eimeriidae
pus in Colombia [506) and both wild-caught S.
Eimeria and Isospora. Coccidiosis is not reported fre- mystax and S. fuscicollis and colony maintained S.
quently as a clinical entity in callitrichids. Eimeria mystax in Peru [421], however, were negative.
sp was seen occasionally in captive S. oedipus, S. Spontaneous fatal toxoplasmosis has been reported
fuscicollis, S. nigricollis [108] and C. jacchus in the United States in single specimens of S. oedi-
[157], and Isospora arctopitheci has been identified pus imported from Colombia [32], and in captive
in C. jacchus [417]. Experimental infection of S. L. rosalia and S. illigeri [20].
geoffroyi with the latter sporozoan produced a pre- Toxoplasma infections experimentally induced
patent period of six to eight days, and an oocyst in S. oedipus [505], S. o. geoffroyi [416] and C.
patency period of 17-55 days [217]. Hemorrhagic jacchus [255] resulted in severe and uniformly fatal
diarrhea occurred five days after infection, followed disease. Signs of illness occurred three to five days
by death two days later in 2 of 13 animals [367]. after infection by various routes and consisted of
I. arctopitheci was found only in epithelial cells of decreased appetite and sluggishness that progressed
the small intestine, particularly the jejunum; 00- to anorexia, severe depression, a crouched posture,
cysts were shed unsporulated. Histologic lesions in- coma, and death within 1-11 days. Some animals
cluded necrosis and subsequent loss of epithelial developed cough shortly before dying. Pathologic
cells at the tips of villi. changes consisted of splenomegaly, hepatic con-
gestion, and erosion or extensive duodenal ulcer-
Besnoitia. The coccidian parasite Besnoitia was orig- ation. Pulmonary involvement ranging from con-
inally classified as Sarcocystis because its parasitic gestion to bronchopneumonia was a consistent
cysts resembled those of the latter. Although natu- finding [32,416]. Microscopic lesions were associ-
rally occurring infections have not been reported ated with the development of rapidly multiplying
in nonhuman primates, experimental inoculation of tachyzoites in the liver, spleen, lung, intestines,
Besnoitia darlingi produced an acute, rapidly fatal lymph nodes, heart, kidneys, adrenals, and other

206
Callitrichid diseases
organs, and were characterized by focal necrosis, in the Callitrichidae [20,103,104,123]. The excep-
petechial hemorrhage, and the presence of inflam- tion was 1 S. o. geoffroyi of 2,330 examined in
matory cells. Some authors have concluded, based Panama that carried Plasmodium brasilianum. Cer-
on their own work and that of others, that catarrhine tain species, however, are susceptible to experi-
monkeys are more resistant to experimental toxo- mental infection with P. brasilianum and P. sim-
plasmosis than platyrrhini, and that resistance ap- ium, whose natural hosts are cebids, and to P. vivax
pears to be absent in the callitrichids [359]. Ex- and P. falciparum of man. Experimental infection
treme susceptibility of the latter group could with P. simium resulted in a mild parasitemia last-
account for failure to find seropositive animals in ing 8-22 days in C. aurita, and low parasitemias
nature. were observed in C. jacchus following infection
with P. brasilianum [102]. Prior passage of this
Hammondia. H. hammondi is a coccidian parasite of organism in Aotus and splenectomized C. jacchus,
the domestic cat and requires an intermediate host however, resulted in persistent (30 weeks), low
to complete its life cycle. It is antigenically and grade parasitemias and lymphocytosis [501]. Mar-
morphologically similar to Toxoplasma and, like mosets developed fever and anemia, ate less and
Sarcocystis, produces cysts principally in the skele- lost weight, but did not succumb to infections.
tal mUscle of its intermediate host [118]. It is not Two to 17 days after infection with P. brasilianum,
known if H. hammondi occurs naturally in nonhu- tamarins developed peak parasitemia which per-
man primates, but its infectivity for S. nigricollis sisted for 4-20 days [468]. P. falciparum infections
Was demonstrated experimentally. Following oral were induced in 4 of 32 S. geoffroyi [390]. The
administration of sporulated oocysts obtained from prepatent period was one to two days and the dura-
cats, antibody titers to T. gondii were low and tran- tion of patency was 4-15 days; a high parasitemia
sient. There were no clinical signs, and lesions- was observed in only one tamarin. P. knowlesi in-
small foci of necrosis and monocellular infiltration fection in two C. jacchus was associated with leu-
in the heart and skeletal muscles-were not sig- kocytosis due to an increase in mononuclear cells
nificant. H. hammondi was, however, isolated from [148]. Two of ten S. geoffroyi were susceptible to
cats fed infected tamarin tissue. P. vivax infection, having a one-day prepatent and
seven-day patent period [389], but this organism
Sarcocystidae
was not infective for C. jacchus [102]. Some strains
Sarcocystis. Numerous species of Sarcocystis have of P. vivax produce high levels of parasitemia that
been identified in a variety of wild and domestic persist for a month or more if they are first passaged
animals. Life cycles of those that have been studied in a host such as Aotus, and prior splenectomy or
are of the predator (final host)-prey (intermediate immunosuppression enhances susceptibility [520].
host) type in which the sexual stages are in the Splenectomized S. mystax developed hi?h levels. of
intestinal cells of the predator, and' asexual repro- parasitemia following passage of P. V1Vax (ASIan
duction occurs in the vascular endothelium and strain ONG/CDC) in Aotus [84). Infected blood
mUscles of the prey. Although the two-host cycle from these tamarins produced high parasitemias in
appears to be obligatory, monkeys may serve as S. fuscicollis for extended periods, and recrudes-
final or intermediate hosts for different species of cence occurred. Virulence of the Vietnam Palo Alto
Sarcocystis [330]. Sporulation of Sarcocystis 00- line of P. vivax in intact C. jacchus was increased
cysts (unlike those of Toxoplasma and Isospora) after passage in Aotus and splenectomized CaL-
occurs in the host's intestine. Meronts (sarcocysts), lithrix [342). Parasitemias were high and patency
which are formed during the asexual stage, have persisted for at least 74 ~a~s. Facial .edema ~nd
been described in skeletal muscle fibers of S. oedi- proteinuria were evident chmcally. P. VIVax, unhke
pus from Colombia [330[ and S. fuscicollis and P. falciparum, was infective for. Anopheles albi-
S. nigricollis from the upper Amazon region mans mosquitoes, which fed on mfected S. geof-
[108,264,358]. Sarcocystis was also identified in froyi [18).
cardiac muscle fibers of a captive-born L. chrysopy- Experimental simultaneous infection of C. jac-
gus in Brazil [29]. The inner part of the sarcocyst chus with P. brasilianum and Epstein-Barr virus
~all is produced by the parasite, and the outer por- (EBV) markedly increased the severity of the ma-
tIon by the host, but there is no inflammatory re- larial infection [499). Animals given EBV before
sponse around affected muscle fibers. Clinical signs Plasmodium developed high parasitemias; in those
hav~ ~ot been reported in association with San'o- receiving these agents in the reserve order the para-
CYStlS Infection.
sitemias resolved earlier. Animals with simultane-
Plasmodiidae ous infections had edema involving the face, neck,
and abdomen. Lassitude, shivering, anemia, and
Plas,:,odium. With one exception [17], naturally oc- proteinuria were evident, and four of six of them
CUrrIng malarial infections have not been reported succumbed. Pathologic changes included extensive

207
Potkay

renal tubular damage and proliferative glomerulo- ing degrees of alopecia, and treatment consisted of
nephritis. It was suggested that double infections in griseofulvin (12.5 mg/day).
people may be associated with the quartan malarial
nephrotic syndrome seen in the tropics, and that
Systemic mycoses
the marmoset may be a useful model for further
studies. Candida. The incidence of Candida sp isolation from
the throats of imported Saguinus sp was 30%, and
2% from acclimated tamarins; isolations from feces
Ciliata
were low (1 %) [108]. Glossitis and esophagitis as-
Balantidiidae sociated with Candida sp infections were also ob-
served in debilitated captive C. jacchus [69]. Clini-
Balantidium. Balantidium sp was reported in a single
cal signs of moniliasis were not reported in these
captive C. jacchus [271]. There were no associated
tamarins, but others have found the organism asso-
clinical or pathological findings.
ciated with ulcers in the mouth, esophagus, and
gastrointestinal tract [28,247], and Candida has
Other protozoan infections been reported as a cause of death.
Pneumocystis. P. carinii, first observed in C. jac-
chus, was more recently reported associated with Cryptococcus. Spontaneous cryptococcosis was diag-
interstitial pneumonia in C. aurita [383]. Few para- nosed at necropsy in three immature, captive S.
sitic cysts (5 to 7 mm in diameter) containing eight o. geoffroyi in Panama [467]. The tamarins were
intracystic nuclei were seen, and death was more emaciated and had severe, generalized pneumonitis
likely the result of coexisting bacterial infection and and splenomegaly and enlarged mesenteric lymph
helminthiasis. In a retrospective histologic survey nodes. Microscopically, plasma cells, lympho-
of the lungs of 441 S. oedipus and S. fuscicollis, cytes, and extravasated red cells were seen in the
50 tamarins (11.3%) were found to have P. carinii pulmonary alveoli. Cryptococcus (neoformans) was
infections [244,412]. The incidence was highest in present singly or in small groups in inflammed areas
7 -12-month-old colony-born animals and long- of the lungs and in germinal centers of the spleen.
term colony residents, but only two of the cases There was patchy loss of mucosa in the small intes-
were judged to be of possible clinical significance. tine, and the architectural structure of lymph nodes
It was suggested that pneumocystosis is probably was destroyed.
not common in wild tamarins. Infections may have Experimental infection of three S. o. geoffroyi
been acquired in captivity, or the conditions of con- with massive oral doses of Cryptococcus neo-
finement may have contributed to the infectivity of formans resulted in transient anorexia and list-
this agent. lessness [465]. Three days before death (19 and 32
days postinoculation) more profound clinical signs
Babesia. An unidentified piroplasma was reported in developed: irritability, muscular tremors of the
a captive C. jacchus that died of malnutrition and limbs, and paralysis which progressed to opisthoto-
secondary anemia [230]. nos. The principal necropsy finding was segmental
distension of the small intestine, and microscopi-
cally there were focal lesions of necrosis in the
Mycotic diseases brain, myocardium, and mesenteric lymph nodes.
Few mycotic infections were described in callitrich- The causative agent was cultured from the brain,
ids. It has been suggested that this may be related meninges, liver, spleen, and spinal cord.
to a lack of study and reporting of these conditions
[247].
Nutritional diseases
Although this is not a review of the nutritional re-
Dermatomycoses
quirements of callitrichids, it may be noted that
Piedraia. One imported Callithrix sp carried P. hor- their requirements are poorly understood and some-
tai, a common fungus in the tropics that affects the times difficult to meet. This seems apparent from
hair on the head [265]. Also called black piedra, the large numbers of diets that have been developed
it typically results in the formation of hard, brown and used in zoo and research environments [83].
to black nodules that surround the hair shafts [222]. Formulations varied and included numerous com-
binations of fresh fruits and vegetables, cereals,
Other. A fungus described as strictly endothrix and bread, eggs, dairy products, adult and larval in-
characterized by the presence of single or doubly sects, mice, reptiles and vitamin-mineral supple-
branched spores was detected in captive C. jacchus ments fed in precise quantities or ad libitum. Baked
and Saguinus sp [108,109]. The animals had vary- biscuits and commercially available pellets of vary-

208
Callitrichid diseases
ing hardness, pastes, commercial semi-soft prepa- chus was determined to be 15 mg/kg metabolic
rations, gruels and purified diets were also utilized. body weight, while that of S. fuscicollis. although
Many diets were formulated not only to provide not precisely determined, was considerably higher
nutrition, but also to enhance palatability and serve [162]. It was found that exposure to short-term
as an environmental stimulus for captive animals. stressors such as annoyance, flashing lights, and
Nevertheless, nutrition-related morbidity and mor- noise increased the requirement for this vitamin.
tality were often reported in callitrichids both on
a.rrival from source countries and after varying pe-
Avitaminosis D
~Iods following acclimatization [33,133,433]. Stud-
Ies to better elucidate nutrient requirements and re- The requirement of nonhuman primates for vitamin
lated considerations in the feeding of these species o to prevent rickets was first understood in the
are ongoing [23,24,40,82,83,133,161,165,276, 1930s and was recently reviewed [222). Subse-
370,414,420,470,471,513,523] . quently, it was found that New World primates re-
quire vitamin 03, which enhances calcium absorp-
Hypoglycemia tion better than vitamin 02, to maintain normal
bone metabolism [246]. Failure to supply vitamin
~a~tive callitrichids were reported to have a high D3 to growing animals results in rickets, and in
IncIdence of hypoglycemia, contributory factors adults, osteomalacia. Osteodystrophia fibrosa is
being their high metabolic rates and the frequency considered to be a descriptive term for these condi-
of feeding [74]. Early signs of hypoglycemia- tions [221. Formerly, rickets and osteomalacia were
muscle tremors and unsteadiness-could be re- commonly diagnosed in callitrichids, the clinical
versed by feeding fruits immediately, while for signs being lethargy, inappetence, weight loss,
more severe cases, 20% dextrose given by stomach skeletal deformities, pathological fractures (in
tube and insulin (1-2 units, intraperitoneally) was adults) and paralysis of the hind legs; death was
recommended. Small quantities of feed containing often the direct result of pneumonia [36,41,229,
sugar given several times a day were said to reduce 269,429,507). S. fuscicollis. experimentally de-
or eliminate the problem [74]. The results of a di- prived of vitamin D for 215 days, developed hyper-
etary study indicated that a liquid with a high sugar parathyroidism characterized by high parathormone
Content given in conjunction with a staple ration levels and partial skeletal demineralization (164).
Was acceptable to C. jacchus as a source of energy, The advent of diets with adequate vitamin D3, ap-
and that these marmosets gained more weight than propriate calcium-phosphorus ratios, and adequate
control groups [289). It was suggested that the protein has made the occurrence of rickets and os-
preparation resembled tree-exudated nectars that teomalacia rare, but has not eliminated it [66]. In
Callithrix utilize in the wild. the absence of such diets, supplementation with vi-
tamin D3 (500 IU/day) and 25% protein and expo-
sure to ultraviolet light was recommended to pre-
AVitaminosis C
vent occurrence [2061. Other studies indicated that
Experimental Vitamin C deficiency in C. jacchus the daily requirement for vitamin D3 in S. fusci-
was associated with loss of appetite, weight, and collis was 33 IU per animal [164], while that of C.
activity; swollen joints and puffy eyelids; muscle jacchus was 110 Iunoo gm body weight [460].
tenderness; anemia; and petechial and ecchymotic Daily oral administration of 1,000 IU of vitamin D3
hemorrhages in the skin of the face, abdomen, and was reported to cure C. jacchus with osteomalacia
extremities [I 15,295 [. Signs appeared within two within one month [206]. Normal circulating levels
to f?ur months and were progressive. Lesions of of I ex, 25-dihydroxyvitamin D3 were reported to
monbund marmosets (92- 167 days) were subperi- be four to ten times higher than in apes or catarrhini
osteal hemorrhages involving ribs and long bones and may be related to a reduced concentration of
and hemorrhages around joints, vertebral bodies, receptors for this metabolite in target tissues
Costochondral junctions, and in the muscles of the [3,434). C. jacchus has been recommended as a
extremities; acute or chronic pneumonitis was fre- model for studies of vitamin O-dependent rickets,
quently present. The teeth were loose, and micro- type 2 [460].
sCopically there were hemorrhages of the alveolar
segment of the periodontal ligament. In another
study C. jacchus fed a vitamin C deficient diet for Avitaminosis E
~our months showed no clinical signs of deficiency, High mortality (66%) among 157 imported S. /a-
ut had markedly elevated plasma cholesterol levels biatus was associated clinically with weight loss,
and decreased levels of circulating thyroid hormone rough hair coats, anemia, weakness, and lethargy;
[325]. in a few, incoordination or paralysis of the hind
The daily ascorbic acid requirement of C. jac- limbs was observed [28]. The tamarins were ob-

209
Potkay

tained in three groups at different times, and clini- Nicotinic acid deficiency
cal signs became apparent six to ten weeks after
S. oedipus fed diets devoid of nicotinic acid for
arrival. Laboratory findings varied between groups
52-104 weeks developed clinical signs of weak-
and over time, but hemolytic anemia, leukopenia,
ness, lethargy, diarrhea, and dermatitis [114,368].
and decrease in serum vitamin E levels were gener-
Necropsy findings were ulcerative enteritis, necro-
ally seen. At necropsy, emaciation, dehydrati?n,
tizing gingivitis, and ulceration of the tongue. Mi-
anemia, and atrophy of the lumbosacral an~ hmd
croscopically, there was significant loss of lingual
limb musculature were found in many ammals.
Bronchopneumonia was present in 20%, more than papillae and necrosis involving ~he gingiv~l epit~e­
lium and lamina propria, whIch sometImes m-
50% had splenomegaly, and livers were pale. Nu-
vo[ved the periodontal ligaments and was associ-
merous microscopic lesions were observed; more
ated with alveolar bone resorption. Tamarins fed
than 70% of the animals had swelling and the pres-
ence of pigment granules in hepatocytes, atrophy diets containing 5 mg of nicotinic acid did not de-
velop these signs and lesions.
of pancreatic acinar cells, coliti~, gastritis, a~d
nephrocalcinosis. Muscle necrosIs was seen ~n
57% and 15% had steatitis. Efforts to treat anemic Zinc deficiency
anim'als with parenteral vitamin E and seleni~m At varying intervals after importation, spontaneous
were unsuccessful. Vitamin E given per os and vita- zinc deficiency was observed in S. mystax that were
min E with selenium administered intramuscularly fed a commercial diet containing 150 mg/kg of zinc
to tamarins from the time of their arrival, however, [65]. Clinical signs were alopecia, sca[iness, and
was associated with a reduced incidence and sever- thickening of skin of the tail, perineum, limbs and
ity of anemia, muscle necrosis, and mo~ality as trunk; ulceration sometimes occurred. Addition of
compared with untreated groups. Among I~ported zinc (40 mg/kg) to the drinking water resulted in
and domestically bred C. jacchus. mortalIty a~d improvement of the condition of the skin and hair
morbidity characterized by Heinz body hemo}ytIc coat. Since deficiencies of trace elements can be
anemia and hemosiderosis were also associated related to dietary nutritional imbalances, vitamin
with low serum vitamin E levels [69). content of ingredients, source of dietary protein, or
absolute shortage of these elements, the cause of
zinc deficiency was not determined.
Folic acid deficiency
Provision of a folic-acid-free diet to C. jacchus re- Wasting
sulted in anorexia, loss of weight, alopecia, [assi-
The term "wasting marmoset syndrome" (WMS)
tude, diarrhea, and death in 59- [36 days [57,295).
was initially used to describe generalized weakness
Reduced white blood cell counts and granu[ocyto-
and failure to thrive in recently weaned marmosets
penia were also observed, as wer~ progressive s.to-
[308). Subsequent[y. its use expanded to include
matitis and inflammation of the lIps and ulceratIon
all callitrichids of all ages [277 ,35 [ ). Affected ca[-
of the mouth and intestines. Histo[ogic findings in-
litrichids were reported to have skeletal muscle at-
cluded altered cell maturation and impaired kerati-
nization. Affected animals had increased suscep- rophy. marked weight [os~, and a[ope~ia, e~pecially
of the tail. Associated sIgns sometImes mcluded
tibility to secondary infections. Develop~e~t of
weakness or paralysis of the hind legs, anemia, and
lesions and deaths were accelerated by admlmster-
chronic or intermittent diarrhea; the fur may appear
ing a folic acid antagonist (methotrexate) to th~se
wet or greasy. Among weanings, hypoa[bumin-
animals. Marmosets given diets supplemented wIth
folic acid developed no signs of deficiency or [e- emia elevated serum aspartate aminotransferase,
and ~nemia have been reported [308], and nephri-
sions.
tis, pancreatitis, hepatic lesions,. and pa~asitism were
observed in adults [49,376]. Hlsto[oglcally the gut
may appear normal, but thin [478], ~r there may
Histidine and arginine deficiency
be chronic colitis [351]. Changes m the fecal
In C. jacchus a reduction in dietary pro.tein to [e~s microflora of marmosets with WMS included a
than 6% led to coprophagy, as did dIets deVOId marked increase in the numbers of putrefactive or-
of histidine or arginine or both [163]. Marmosets ganisms (Bacteroides-jusobacte:ia) and Clostrid-
preferred soft, pasty feces, rejecting those that were ium, and significant decreases m the numbers of
firm. Consumption of diets that were free of these lactobacilli [299]. Populations of lactose nonfer-
amino acids was associated with weight loss, and menting organisms such as Proteus sp, Pseudomo-
it was suggested that either or both of them were nas aeruginosae and Alcaligenes jecalis were also
essential. found to increase.

210
Callitrichid diseases
WMS appears to encompass a variety of illnesses Spontaneous adenocarcinomas of the intestinal
~hat ~re not understood and that have no specifically tract have been diagnosed in at least five colonies
identifiable causes. That it is not a specific syn- of wild-caught and colony-bred S. o. oedipus [42].
drome or disease is suggested by the variety of fac- These neoplasms were found, for example, in 12
~ors ~hat have been put forth as causing or inftuenc- S. o. oedipus and one colony-bred S. juscicollis
mg its development; these include helminthiasis maintained in a large research colony for 13-74
~nd other infections, inadequate exercise, dietary months (average = 47.5 months) [311]. In all but
tnadequacies resulting from food formulation or the S. juscicollis, which had a mild-ileal neoplasm,
competition, and palatability of feed [351,385, the tumors involved the colon or cecum or both.
~34,478]. Likewise, recommended treatments have They were highly invasive, originated in multiple
tncluded providing a high protein diet [49,277, primary sites, and, in most cases, were associated
385,387,434], administering lactobacilli [479], with metastases to the paracolonic and mesenteric
modifying methods for feeding animals housed in lymph nodes. Microscopically, the tumors were
groups [471] and improving diet palatability [513]. characterized by PAS-positive epithelial cells that
disrupted or displaced the normal colonic mu-
Neoplastic diseases cosa, and invaded the submucosa, lymphatics, and
nearby lymph nodes. The immediate cause of death
Spontaneous neoplasms occur occasionally in calli- was intestinal obstruction in ten of these tamarins.
trichids and are described below. With few excep- The others died of ulcerative colitis, ascites, and
tions little information was available concerning anemia associated clinically with inanition and
them. For a discussion of neoplasia caused by vi- wasting. In other colonies, significant numbers of
ruses see Gamma herpesvirinae and Oncornaviri- S. oedipus died of adenocarcinoma of the colon,
nae. Among newly imported S. sp, one fibrochon- and there was a strong association between this neo-
droma of the larynx and one benign adenoma of the plasm and the presence of colitis [42,45,66,76,
adrenal cortex were seen [109]. Of five S. sp with 119,279,413]. A radiographic technique has been
tumors of the eyelids, one was examined and found described for use in identifying and following the
to be a melanized papilloma [59]. A squamous cell course of colonic tumors in such animals [75]. The
carcinoma originating in the skin below the in- similarities between colitis and adenocarcinoma of
tertragic notch of the ear was seen in an aged S. f. the colon in man and in S. o. oedipus suggested
leucogenys [411]. Associated clinical signs were that this species may serve as a model for gastroin-
facial palsy and paralysis of the orbicularis oculi testinal disease, a topic which was explored exten-
muscle. The tumor grew rapidly from a small, lo- sively at a recent symposium [77].
cal, slightly elevated lesion to amass that even-
tually involved the buccal cavity. Squamous cell
carcinomas involving the head have also been ob-
Diseases of specific organ systems
served in nine C. jacchus, as has been one reticu- Lesions of specific organs or systems described in
lum cell carcinoma [227]. Adrenal myelolipomas callitrichids are shown in Table II. They were not
[369] and a juxtarenal myelolipoma [451] were de- described as being associated with specific diseases
s~ribed in three aged S. oedipus and may have con- dealt with elsewhere in this review. Affected ani-
tnbuted to their poor body condition; the mass was mals were usually from zoological collections or
palpable through the abdominal wall of one. Neph- research colonies, and lesions varied from clinical
roblastoma [257], uterine tumor [348], and renal observations and incidental findings at necropsy to
papillary adenoma [47] were reported in individual causes of death. Data concerning total populations
S. oedipus, and thyroid adenocarcinoma was de- were not often available. Diseases for which a sig-
tected in one S. nigricollis [509]. nificant amount of information was available are
Leukemia was listed as the cause of death in a described briefly below.
C. jac:hus [168], lymphatic leukemia was diag-
nos~d m C. argentata, and S. midas [230,231] and
Oral pathology
mahgnant lymphoma was seen in C. jacchus [49].
Myeloproliferative disease in a three-and-one-half- The occurrence of dental and periodontal disease in
rear-Old S. o. oedipus was characterized by en- wild C. pygmaea, Callithrix sp, and Saguinus sp
arg~d lymph nodes, liver, and spleen [278]. Micro- has been extensively reviewed by species, and a
~cOpically, tissues of the gastrointestinal tract were reference list was published [222]. Missing, cari-
~nfiltrated by blast cells of undetermined origin and ous, and abscessed teeth were seen in 10-20% of
immature granulocytes, and these cell types largely the specimens studied, canines being most com-
~eplaced the lymphoid tissue of the lymph nodes, monly affected (18.1%). As might be expected, the
pleen, tonsils, and thymus. incidence of dental diseases increased with increas-

211
Potkay

ing age. Their occurrence appeared to be more looking, light colored diarrhea within ten days, and
common in animals obtained from certain areas and after 24-42 weeks, had altered serum magnesium
may have been related to the types and quantities and alkaline phosphatase levels, abnormal Ca: P ra-
of foods consumed. Infection of the roots of canine tios and evidence of osteomalacia [116]. Micro-
teeth was common in captive C. jacchus, usually scopically, the cytoplasm of the jejunal columnar
associated with broken or badly worn teeth [26]. epithelial cells was seen to have been displaced by
Clinically there was sudden swelling, abscessation, large vacuoles containing fat.
and external drainage of pus within 24-48 hours.
Occasionally, on the affected side, there was in-
creased lacrimation, conjunctivitis, and mucopuru- Colitis
lent nasal discharge, but affected· animals did not
evidence signs of pain or discomfort. Organisms Colitis was a common finding in colonies of
associated with the condition were Serratia sp, Pro- S. oedipus [66,76,311,373,419] and C. jacchus
teus sp, Eikenella corrodens. Diagnosis was based [66,419]. Microscopically it was characterized by
on clinical signs and radiography, and treatment abscesses of the crypts and inflammation in the lam-
consisted of extracting the affected tooth and treat- ina propria. Irregularities of the mucosal epithelial
ing with oxytetracycline. Crazing, the presence of and crypt morphology and a decrease in the number
discolored fine-lined fracture patterns of the dental of goblet cells were observed in advanced cases.
enamel, was consistently observed in L. rosalia and Cachexia was seen in tamarins with colitis, proba-
Saguinus sp, less frequently in Callithrix and not bly as a result of their reduced capacity to absorb
at all in Cebuella [222). It was usually seen in older nutrients. The colitis in S. oedipus was similar to
animals, but the relationship of this phenomenon to ulcerative colitis in human subjects [66], and was
dental disease is not known. often associated with colonic adenocarcinoma (see
Among captive callitrichids, periodontal disease under Neoplastic Diseases). Observations that the
with associated tooth loss was reported in C. j. incidence of colitis was high in all of the S. oedipus
jacchus [308,433), and dental calculi were fre- colonies studied, but not in colonies of related tam-
quently seen in C. jacchus, S. oedipus, S. fusci- arin species that were housed in a similar manner
collis and S. nigricollis [26,46,71,173). The maxil- suggested that the high risk borne by S. oedipu;
lary canines and premolars were most commonly likely had a genetic basis [373). It has also been
involved; calculi and plaque recurred about six shown that certain conditions of captivity such as
weeks after removal. Gingivitis [8,36,71) and mal- isolation, confinement, and low ambient tempera-
occlusion [433) have also been reported in captive ture can promote the occurrence of colitis in this
marmosets and tamarins. species [515). Diagnostic methods for this disease
Anomalies were rarely observed and included included colonoscopy and contrast radiography;
cleft palate in C. jacchus [231) and S. fuscicollis, examination of multiple biopsies gave a good as-
[283], supernumerary teeth, and congenitally miss- sessment of disease status [512). Treatment with
ing teeth. sulfasalazine (50 mg/kg/day, orally) resulted in in-
creased body weight and serum albumin levels and
diminished disease activity as determined histologi-
Bloat
cally in S. oedipus with acute colitis, but was inef-
Acute bloat (gastric dilatation) is usually associated fectual in those with chronic colitis [314).
with macaques, but has been reported in callitrich-
ids [74). Bloat has a rapid onset with minimal pro-
dromal signs, and death ensues unless the animal Idiopathic ulcerative ileocolitis with thrombocytopenia
is treated immediately by gastric lavage, restoration
Rapidly fatal focal ulcerative ileocolitis was re-
of blood volume, correction of acid-base imbal-
ported in five captive-born S. oedipus, aged 4-12
ance, and supportive therapy for shock. The etiol-
months [441). Clinical signs included diarrhea or
ogy of the disorder is not known, but its incidence
dark, tarry stools, weakness, inappetence, and pale
can us~ally be reduced by increasing the frequency
mucous membranes. Hematology revealed severe
of feedmg, and by offering small quantities of food
acute or nonregenerative hemolytic anemia and
during those parts of the day when the animals are
thrombocytopenia associated with widespread hem-
active. Gastric dilatation has also been reported in
orrhage. Other lesions, confined to the ileocolic
a.ssociation with infection by gas-producing bacte-
na [449] (See Clostridium under Bacillaceae.) junction, consisted of sharply demarcated ulcers
with pus and variable hemorrhage. Of the variety
of pathogenic bacteria isolated from these animals
Jejunal lipodystrophy
or their feces, strong consideration was given to
Saguinus oedipus, given a high cholesterol-high anaerobes and pathogenic strains of E. coli as the
coconut oil diet, developed voluminous, fatty- etiology of this condition.

212
Callitrichid diseases

Table II. Specific anatomical lesions observed in callitrichids


Lesion Species No. of cases· References

Integumentary
Alopecia Saguinus nigricollis 8/422 129
Dermatitis Callithrix jacchus 7/422 481
Ulceration Callithrix jacchus 481

Respiratory
Bronchopneumonia Callithrix jacchus, C. j. penicil/ata, C. 109,152,190,
humeralifer, Saguinus midas niger, 200, 201,
S. sp 202, 311
Empyema Cal/ithrix jacchus 410
Foam cells (alveoli) Cal/ithrix jacchus 9/422 4B1
Lymphoid cuffing Callithrix jacchus 27/422 481
Pneumonia Callithrix jacchus, Cebuel/a pygmaea, 74/355 35, 49, 74, 109,
Saguinus oedipus, S. fuscicollis, S. 5/78; 2/18 153,155,265,
nigricollis, S. sp, Leontopithecus 10/422; 1 275, 285, 287,
rosalia, "callitrichids" 481
Pneumonia, aspiration Saguinus oedipus 1/267 275
Pulmonary congestion, edema and Saguinus sp 109
hemorrhage
Pleuritis Saguinus sp, Cal/ithrix jacchus 1+ 69, 74, 109
Tracheiti's Saguinus sp 7 + /422 109, 481

Hematopoietic
Anemia Cal/ithrix jacchus, Saguinus sp, 175 + /422 69, 74, 168,
Leontopithecus rosalia, "calli- 230
trichids"
Reactive lymphoid hyperplasia Cal/ithrix jacchus 33/422 481
Thymic atrophy Callithrix jacchus 15/422 481
Splenic extramedullary hematopoiesiS Callithrix jacchus 18/422 481

Cardiovascular
Ascites Saguinus o. geoffroyi 198
Endocarditis Callithrix jacchus, Saguinus fuscicollis 1/18 45,49
Pericarditis Callithrix jacchus, Saguinus sp 109, 151, 155
Ventricular dilatation Callithrix jacchus 30/335 69
Myocardial fibrosis, fibrofuscinosis Cal/ithrix jacchus 15/335; 19/438 69, 486
Myocarditis Cal/ithrix jacchus, Saguinus mystax 9/483 385, 481
PUlmonary thrombosis Callithrix jacchus 1/335 69
Digestive
Dental abscess Callithrix jacchus 19/64 26, 227
Esophagitis Callithrix jacchus 4/335 69
ESophageal obstruction Callithrix jacchus 1 69
Gastritis Callithrix jacchus 4/335; 7/422 69, 481
Gastric trichobeozar Saguinus fuscicol/is 2 192
Gastroenteritis Saguinus mystax 25/49 385
Enteritis, acute and chronic Callithrix jacchus, Saguinus midas, S. 1/18; 63/422 1,29,156,
sp, Leontopithecus rosalia, L. 230, 481
chrysopygus, "callitrichids"
Enteritis Cal/ithrix jacchus 100/335 69
Enteritis, bacterial Cal/ithrix jacchus 7/178 74
Intestinal obstruction Cal/ithrix humeralifer 200
Intussusception Callithrix jacchus 428
Callithrix jacchus 197
TYPhlitis, acute gangrenous
Hepatic extramedullary hemato- Callithrix jacchus 42/422 481
poiesis
Hepatic mononuclear cell infiltrates Callithrix jacchus 15/422 481
Hepatic parenchymal cell necrosis Callithrix jacchus 8/422 481
Hepatitis, chronic Callithrix jacchus 9/335 69
Biliary hyperplasia Callithrix jacchus 4/335 69
Hepatic abscess Callithrix jacchus 1/335 69
Cholecystitis Callithrix jacchus 3/335; 27/422 69, 481
Hemosiderosis Callithrix jacchus 151/335 69
Pancreatitis Callithrix jacchus 46
Pancreat!~ fibrosis, exocrine atrophy Callithrix jacchus 35/336 69, 142
Pancreatitis, subacute to chronic Callithrix jacchus, "marmosets" 7/18 49,168,410
Peritonitis Callithrix jacchus, Saguinus sp, "calli- 7/18 1, 49, 74,
trichids" 414
Rectal prolapse Callithrix jacchus 2/335 69
Continued.
213
Table II. Continued
Lesion Species No. of cases" References

Urogenital
Cystitis Callithrix jacchus, Saguinus nigricollis 2/178 74, 410
Cystic ovarian follicles Callithrix jacchus 10/222 481
Renal extramedullary hematopoiesis Callithrix jacchus 40/456 481, 482
Metritis Callithrix jacchus 2+ 69, 151
Nephritis Callithrix jacchus, Saguinus mystax 4/178 74,385
Nephritis, chronic Callithrix jacchus 70/200 482
Nephritis, purulent Saguinus oedipus 1/267 275
Pyleonephritis Saguinus fuscicollis, S. oedipus, 43, 220, 410,
"callitrichids" 481
Glomerular fibrotic nephritis . Callithrix jacchus 307
Glomerular neph ritis, acute Callithrix jacchus 46
Renal tubular mineralization Callithrix jacchus 7/178 74, 482
Renal tubular necrosis, acute Callithrix jacchus 5/178 74
Renal tubular dilatation/casts Callithrix jacchus 89/456 481, 482
Tubulo-interstitial nephritis Callithrix jacchus 46
Interstitial nephritis Callithrix jacchus 2/335 69
Renal interstitial infiltrates Callithrix jacchus 284/456 481, 482
Nephrosis "callitrichid" 408
Testicular atrophy Callithrix jacchus 1; 33/195 69, 481
Obstetric conditions Callithrix jacchus, C. jx. C. j. peni- 3 233
ciliata, C. humeralifer
Musculoskeletal
Cleft lip and palate Callithrix jacchus, Saguinus fuscicollis 2 231, 283, 397
Ectrodactyly Callithrix jacchus 1 172
Diaphragmatic hernia Leontopithecus rosalia 8/90 401
Dwarfism Saguinus oedipus 1; 1/267 67, 275
Lobster claw deformity Callithrix jacchus 1 396
Myopathy Callithrix jacchus 116/335; 8/422 69, 481
Osteodystrophy Callithrix jacchus 30/335 69
Polydactyly Callithrix jacchus, Saguinus oedipus 2; 1/267 67, 275, 397
Scoliosis Saguinus fuscicollis 1 67
Septic arth ritis Callithrix jacchus 1/335 69
Syndactyly Callithrix jacchus, Saguinus nigricollis, 3 67,172,224
S. oedipus
Umbilical hernia Saguinus oedipus 2/267 275
Nervous
Meningitis Callithrix jacchus, Saguinus oedipus, 3 +; 4/267 69, 168, 275
"marmoset"
Meningoencephalitis, purulent Callithrix jacchus 46
Pachymeningitis Callithrix jacchus 405
Hydrocephalus Callithrix jacchus 2/235 69
Cerebral extramedullary hemato- Callithrix jacchus 10/483 481
poiesis
Cerebral hemorrhage Saguinus oedipus 12/267 275
Endocrine
Parafollicular cell hyperplasia Callithrix jacchus 44/422 481
Ectopic thymic tissue Callithrix jacchus 25/422 481
Thyroid enlargement Callithrix jacchus 19/335 69
Thyroiditis, chronic Callithrix jacchus 1/335; 48/422 69, 481
Adrenals; inflammatory cell infil- Callithrix jacchus 31/335 69
tration
Adrenals; extramedullary hemato- Callithrix jacchus 1071422 481
poiesis
Colloid gOiter Callithrix jacchus 9/422 481
Organs of Special Sense
Eye
Cataract Saguinus fuscicollis illigeri x 59
S. f. lagonotus, S. sp
Cellulitis, periorbital Callithrix jacchus 410
Conjunctivitis with blindness Callithrix jacchus 204
Obstructed meibomian ducts Saguinus o. oedipus, S. sp 59
Other: Anisocoria; corneal pig men- Callithrix j. jacchus. Cebuella pygmaea, 59
tation; distichiasis; entropion; ec- Saguinus f. fuscicollis, S. f. lagono-
tropion; iris cyst; keratitis; lagoph- tus, S. f. leucogenys, S. f. nigri-
thalmos; lens pigmentation; optiC collis, S. f. nigrifons, S. o. oedipus
disc ectasis
Other
Neonatal conditions Saguinus oedipus 9, 56/156 10, 272
--------
"Number of cases reported, or number of cases/total population.
Callitrichid diseases
Atherosclerosis Helminth parasites
Spontaneous atherosclerosis is rare in callitrichids Internal parasitic infections are common in calli-
[12,45,49,79]; it has been induced in S. oedipus by trichids (Tables III, IV, and V). The following dis-
feeding a 5% cholesterol, 23% lard diet for 47-73 cussion is restricted to those which are particularly
weeks [117]. Atheromas were found distributed common, injurious to their hosts, or of public
through the aortas of tamarins that ate this diet for health significance.
69-73 weeks· all animals had atherosclerotic le-
sions of the c;ronary and lingual arteries and arteri- Trematoda
oles, and blood cholesterol levels were markedly
elevated. C. pygmaea was also reported to develop Trematodiasis appeared to occur almost exclusively
hYpercholesterolemia when maintained on a diet of in tamarins, there being only one report of infection
eggs and milk [443]. in Callithrix (Table III). Life cycles of the digenetic
flukes are complex and largely unknown. They
may, depending on the species, require intermedi-
Thyroiditis ate hosts, which could include insects, mollusks,
amphibians, reptiles, or fish. Infection of the final
~hronic thyroiditis has been observed at necropsy host is acquired by ingesting either intermediate
In 10-60% of colony born C. jacchus [295,481]. hosts in nature or feed contaminated with trematode
The incidence appeared to be lower in wild-caught cercariae. Diagnoses of trematodiasis based on the
Callithrix and Saguinus, however [295]. Lesions observation of eggs in feces are generally not de-
varied from minor to extensive lymphocytic infil- finitive; examinations of adult trematodes is prefer-
trations with follicular destruction. The findings able [285].
Were incidental and their significance was un- The biliary tract was most commonly reported
known.
as a site of fluke infection. The genera involved
were Athesmia and Platynosomum, the average
Mesangial nephropathy number of flukes per host being 11 and 5, respec-
tively [388]. Flukes were usually found at nec-
Inflammatory renal lesions, which occurred in more ropsy, sometimes causing distension of the biliary
than 90% of the members of a callitrichid colony, tract. Microscopically, their presence may be asso-
Were directly related to the deaths of 10-20% of ciated with biliary epithelial hypertrophy and hy-
them [43,44]. The species involved were S. oedi- perplasia, pericholangial fibrosis, and a mixed in-
pus, S. fuscicollis, S. labiatus, S. mystax, S. bi- flammatory cell reaction [246].
color, L. rosalia, Callithrix j. jacchus, C. j. geof- While several flukes (Neodiplostomum, Phaner-
f~oYi, C. penicillata, and C. pygmaea. Clinical opsolus, and Echidnostoma) inhabit the small intes-
Signs were nonspecific, consisting of transient or tine, the incidence of infections was low and no
Continuous hematuria, proteinuria, and urinary clinical or pathologic findings have been reported.
Casts. Histologically, the typical lesions were mes- S. f. illigeri was susceptible to experimental in-
angial sclerosis, proliferation, and sclerosis of fection with Schistosoma mansoni cercariae [110].
BOwman's capsule, and glomerular sclerosis. In the Their subcutaneous administration produced high
mesangium, lesions were strongly associated with (31 %) infection nites and lesions, which included
IgM. deposits, which appear to have occurred ac- hepatosplenomegaly, necrosis, and hemorrhage of
cordIng to classical complement activation path- the intestine and ascites. In animals infected percu-
:vays. There did not appear to be any genetic or sex taneously, infection rates were low (2.6%) and le-
Influence on the frequency or occurrence of this sions consisted of hepatic granulomas. Adult Schis-
progressive disease. tosoma were recovered from the inferior mesenteric
veins.
Obesity
Cestoda
S. fuseicollis and S. oedipus whose body weights
e~ceeded 460 g and 450 g, respectively, were con- Tapeworms were occasionally found in the small
sidered to be obese [48]. In these animals, the most intestines of imported tamarins; marmosets were
frequently found lesions were acute pancreatic ne- seldom affected (Table IV). Of these worms,
crosis and steatonecrosis. These findings, and the the most commonly reported were Atriotaenia
~bservation that affected tamarins had glycosuria and Paratriotaenia, while Bertiella, Raillietina,
hut not .ketonuria, led to the speculation that they and Hymenolepis were observed infrequently. The
ad an insulin resistant diabetes similar to human number of parasites was small, averaging about five
tYpe II diabetes. per host, and no apparent pathology was associated

215
Table III. Trematode parasites of callitrichids

Parasite Host Habitat Location References


Trematoda
Dicrocoeliidae
Athesmia (Heterolecithodes) Saguinus geoffroyi, S. fuscicollis, Gall bladder, bile ducts Panama Prov., Panama; 28, 86, 87,
foxi S. nigricollis, S. labiatus, S. New Orleans, LA; Oak 205, 206,
oedipus, S. leucopus, S. sp Ridge, TN; Coving- 285, 286,
ton, LA 388, 476
Platynosomum amazonensis Saguinus fuscicollis, Callithrix Gall bladder, bile ducts Oak Ridge, TN 87, 285,
jacchus 388
Platynosomum marmoseti Saguinus nigricollis Gall bladder, bile ducts Oak Ridge, TN 87, 285
Platynosomum sp Saguinus sp, Leontopithecus sp Gall bladder a 87, 286
Zonorchis gOliath Saguinus geoffroyi, Leonto- Bile ducts Panama Province and 286, 476
pithecus sp Canal Zone, Panama
Dicrocoelium sp Saguinus sp Liver Chicago, IL 108
Diplostomidae
Neodiplostomum tamarini Saguinus nigricollis, S. fusci- Small intestine Oak Ridge, TN 87, 285
collis
Neodiplostomum sp Saguinus sp, Leontopithecus sp Intestine 86, 108
286
Lecithodendriidae
Phaneropsolus orbicularis Saguinus fuscicollis, S. sp Intestine 86, 285,
388
Phaneropsolus sp Saguinus fuscicollis, S. sp Small intestine Oak Ridge, TN 87, 286
Echidnostomatidae
Echidnostoma aphylactum Saguinus geoffroyi Small intestine Panama Prov., Panama 476
Trematodes Saguinus nigricollis Liver, biliary tract Oak Ridge, TN 358
------ .------------- - ------------ - -

aGeographic location was not reported.

Table IV. Cestode parasites of callitrichids

Parasite Host Habitat Location References


Cestoda
Anaplocephalidae
Atriotaenia (Oochoristica) Saguinus nigricollis, S. tamarin, Small intestine Brazil; Colombia; 16,87,108,
(Matheovataenia) S. bicolor, S. midas, S. sp, Guyana; Peru 120,286,
megastoma Callithrix argentata melaura, 452
Leontopithecus sp
Bertiella mucronata Saguinus leucopus, Callithrix Small intestine Minas Gerais, Brazil 16,388
nigrifrons
Davaineidae
Para trio taenia oedipomi- Saguinus oedipus Small intestine New Orleans, LA 458
datus
Para trio taenia (Oochoristica) Saguins fuscicollis, S. leucopus, Small intestine Oak Ridge, TN 74, 87, 286,
sp S. illigeri, S. oedipus, S. sp 388
Raillientina sp Saguinus nigricollis, S. sp Small intestine Chicago, IL 74, 108
Diphyllobothriidae
Diphyllobothrium erinacei Saguinus sp Subcutaneous 166, 222
(larvae)
Spirometra mansonoides Saguinus geoffroyi Subcutaneous in Panama Prov., Panama 388, 476
(larvae) scapular region
Spirometra rep tans (larvae) Callithrix argentata Subcutaneous South America 120, 456
Spirometra sp (larvae) Saguinus fuscicollis, S. nigri- Subcutaneous in Loreto, Peru 87, 388, 437
collis, S. oedipus, S. illigeri, scapular and lumbar
S. mystax, S. sp, Callithrix sp region, axilla
Hymenolepididae
Hymenolepis cebidarum Saguinus nigricollis, Callithrix Intestine Minas GeraiS, 16, 120, 286
nigrifrons (?) Brazil; Colombia;
Peru
Vampirolepis sp Callithrix sp 355
Cestodes Callithrix jacchus, Saguinus oe- London Zoological 196, 197,
dipus, S. nigricollis, S. sp Gardens, England 205, 206
Cestode larvae Saguinus labiatus Subcutaneous Covington, LA 28
aHabitat was not reported.
bGeographic location was not reported.

216
Table V. Helminth parasites of callitrichids
Parasite Host Habitat Location References
----~ --- - .. _ - - - - - - - ------.~

Nematoda
Oxiuridae
Enterobius callithrieis Caflithrix jaeehus, Cecum, large intestine London Zoological 432, 447,
Saguinus oedipus Gardens, England; 518
South America
Enterobius vermieularis Cebuella pygmaea 518
Enterobius sp Callithrix jaeehus, Small intestine London Zoological 197, 286
Cebue/la pygmaea, Gardens, England;
Leontopitheeus sp
Primasubulura jacehus Callithrix jaeehus, Cecum, small intestine, Oak Ridge, TN: 87, 108,
Cebue/la pygmaea, colon Brazil; South 111, 388
Saguinus labiatus, America
S. fuscieo/lis,
S. leueopus, S. oedipus,
S. mystax
Subulura jaeehus Callithrix penicillata, Cecum, large intestine Panama Prov., 61,64
C. jaeehus, C. argentata Panama; Rio de 243, 456,
C. aurita, Saguinus Janeiro, Brazil; 476,518
geoffroyi, S. oedipus, Colombia; Loreto,
S. bieolor, Cebue/la Peru; Mato Grosso,
pygmaea Brazil
Subulura distans Callithrix jacehus, C. Intestine, cecum London Zoological 456, 486
argentata, Saguinus Gardens, England;
bicolor Mato Grosso, Brazil
Subulura sp Caflithrix jaeehus, London Zoological 191, 286
Leontopitheeus sp, Gardens, England
Cebue/la pygmaea
Trypanoxyuris eallithrieis Callithrix jacehus, Colon Panama Prov., 245, 251,
Saguinus nigrieollis Panama; Brazil; 476
South America
Trypanoxyuris (Enterobius) Saguinus oedipus Colombia 386
minutis
Trypanoxyuris oedipi Saguinus oedipus Colombia 251
Trypanoxyuris tamarini Saguinus nigrieollis, Cecum, colon Oak Ridge, TN; 87, 108
S. fuscieollis Peru; South 245, 251
America
Trypanoxyuria sp Callithrix jaechus, Large intestine South America 286, 388
Saguinus fuseieollis,
S. iIIigeri,
S. oedipus, S. sp,
Leontopitheeus sp
Spiruroidea
Protospirura murieola Callithrix jaeehus, Stomach South America 388
Saguinus fuseieollis
Pterigodermatites nyetieebi Leontopitheeus r. Small intestine, colon, Washington, DC 346
rosalia cecum, rectum, stomach
Pte.rygodermatites sp Saguinus oedipus Small intestine Topeka, KS 300
SPlfura guianensis Saguinus fuscieollis, Esophagus, stomach Panama Prov., 87, 243,
(== tamarin) S. mystax Panama; Loreto, 358, 388,
Peru; South 476
America
b
SpJrura sp Saguinus sp 286
Tnehospirura leptostoma Callithrix jacehus, Pancreatic ducts Brazil; Colombia; 28, 29, 30
Saguinus oedipus Oak Ridge, TN; 69,87
Covington, LA; 376, 440
Macclesfield,
England; Sisseln,
Switzerland
Triehospirura sp Cebuella pygmaea, 286
Callithrix sp
Gnathostomatidae
Gnathostoma weinberg Saguinus sp French Guiana 456
b
Gnathostoma sp Leontopithecus sp, 286, 456
Saguinus sp
PhYSalopteridae
Physaloptera sp Saguinus geoffroyi, Stomach Panama Prov., 286, 456,
Callithrix jacchus, Panama; Brazil 476
Leontopithecus rosalia,
Cebuella sp
Retieularia sp Cebuella, sp, 286
Leontopitheeus sp
Continued.
217
Table V. Continued

Parasite Host Habitat Location References

Metastrongylidae
Angiostrongylus costaricensis Saguinus mystax Ileum, intestinal Iquitos, Peru 437
mesentery
Filariopsis (Filaroides) Callithrix jacchus, Lung Rio de Janeiro, 403, 446,
barretoi Saguinus nigricollis Brazil 518
Filariopsis (Filaroides) Cebuella pygmaea Lung Leticia, Colombia 301, 403
cebuellae 498
Filariopsis (Filaroides) Callithrix jacchus, Lung 498, 518
gordius Saguinus nigricollis
Filaroides sp Saguinus fuscicollis, Lung Upper Amazon River 87, 285,
Cebuella pygmaea basin; Oak Ridge, 358, 388
TN; South America
Metastrongyles Saguinus oedipus New Orleans, LA 206
Trichostrongylidae
Longistriata dudia Saguinus fuscicollis Duodenum, jejunum South America 388
Longistriata sp Saguinus fuscicollis, Small intestine Oak Ridge, TN 87, 286
S. sp
Molineus vexillarius Saguinus fuscicollis, Duodenum, jejunum Oak Ridge, TN 87, 108,
S. leucopus, S. oedipus, 388,518
S. nigricollis
Molineus tortulosus Saguinus oedipus Colombia 388
Molineus elegans Saguinus mystax Small intestine Loreto, Peru 243
Molineus sp Saguinus sp b c 286
Pithecostrongylus (Cooperia) Cebuella pygmaea 286,518
alatus
Rhabditidae
b
Strongyloides stercoralis Cebuella pygmaea, 455, 518
Saguinus m. midas
Strongyloides sp Saguinus oedipus, Small intestine New Orleans, LA; 87, 205,
S. fuscicollis, S. sp Oak Ridge, TN 206, 286
Strongylidae
Oesophagostomum sp Saguinus oedipus New Orleans, LA 205, 206
Ancylostoma sp Saguinus sp c 286
Ascarididae
Ascaris sp Saguinus sp 286
a
Ascridids Peritoneal cavity, Colon and Darien 476
large and small Provs., Panama
intestines
Thelaziidae
b
Riticularia alphi Callithrix jacchus, 518
Leontopithecus rosalia
Onchocercidae
Dipetalonema caudispina Saguinus midas niger, Blood South America 68,122,
S. midas, S. bicolor, 456, 496
S. mystax, Leonto-
pithecus rosalia
Dipetalonema gracile Callithrix jacchus, C. Microfilariae-blood; Loreto, Peru; 19, 28, 87
argentata, Saguinus Adults-serous Colombia; Oak 108,122,
fuscicollis, S. mystax, cavities and adjacent Ridge, TN; Para, 205, 243,
S. nigricollis, S. midas connective tissues, Brazil; Covington, 385, 388
niger, S. bicolor, S. subcutaneous LA; French Guiana
midas, S. labiatus
Leontopithecus rosalia,
L. r. chrysopygus
Dipetalonema zakii Leontopithecus rosalia Intermuscular Eastern Brazil 77, 134
connective tissue
Dipetalonema sp Saguinus nigricollis, Microfilariae-blood; Upper Amazon River 358, 437
S. mystax Adult-peritoneal basin
cavity, subperitoneal
connective tissue and
lymphatics
Tetrapetalonema panamensis Saguinus oedipus, Microfilariae-blood South America 68
S. midas niger
Tetrapetalonema (Mansonella, Saguinus oedipus, Microfilariae-blood; Loreto, Peru; 19,68,122,
Dipetalonema) marmosetae S. fuscicollis, Adults-subcutaneous Panama Prov., 144, 338,
S. geoffroyi, in subcapsular Panama; Colombia; 425, 518
S. midas niger, connective tissue, South America
S. nigricollis intermuscular fascia,
and serous cavities
Tetrapetalonema mystaxi Saguinus m. mystax Microfilariae-blood; Brazil 126
Adults-subcutaneous
in subscapular
connective tissues
Continued.
Callitrichid diseases

Table V. Continued

Parasite Host Habitat Location References


Tetrapetalonema tamarinae Saguinus midas niger, Blood and tissues Loreto, Peru; 68, 108,
S. nigricollis Colombia, South 122
America
Tetrapetalonema zakii Leontopithecus rosalia 518
Tetrapetalonema sp Saguinus nigricollis Microfilariae-blood; Upper Amazon River 358
Adults-subcutaneous basin
tissue, intermuscular
fascia of back
Parlitsoma sp Leontopithecus sp 286
Setaria sp Saguinus sp 286
Filariasis Callithrix jacchus, Blood, peritoneal London Zoological 69, 152,
Saguinus iIIigeri, cavity Gardens, England; 154
S. midas niger Macclesfield,
England
Microfilariae Callithrix jacchus, Blood, lymphatics London Zoological 193,194,
C. penicillata, Gardens, England; 195, 199,
Saguinus geoffroyi, Brazil; Guyana 203, 206,
S. oedipus, S. mystax, 221, 305,
S. tamarin, S. midas, 379,380,
S. m. midas, 381, 382,
Leontopithecus rosalia 416, 456,
518
Nematodes Callithrix jacchus, Cecum, colon, lung Upper Amazon River 196, 358
Saguinus fuscicollis basin; London
Zoological Gardens,
England
Nematode larvae Callithrix jacchus, South America 388
Saguinus fuscicollis,
S. iIIigeri, S. oedipus
Acanthocephala
Prosthenorchis elegans Callithrix j. jacchus, Lower ileum, cecum, Rio de Janeiro and 28,74,
C. j. geoffryi, proximal colon Para, Brazil; Oak 87, 108,
C. humeralifer Ridge, TN; Loreto, 205, 206,
chrysoleuca, Peru; New Orleans, 243,311,
Cebuella pygmaea, LA; Colombia; 312, 338,
Saguinus fuscicollis, Panama; South 358, 385,
S. leucopus, S. oedipus America; USSR 388, 410,
geoffroyi, S. midas ni- 425, 456,
ger, S. o. oedipus, 518
S. labiatus, S. mystax,
S. nigricollis, S. m.
midas, S. illigeri,
Leontopithecus r. rosalia
Prosthenorchis lenti Saguinus oedipus Proximal colon Panama(?); Espirito 312, 476
geoffroy;, Callithrix Santo, Brazil
"jacchus geoffroyi
Prosthenorchis sigmoides Callithrix jacchus, Small intestine Rio de Janeiro, 312, 518
C. humeralifer Brazil
chrysoleuca,
Leontopithecus rosalia,
Saguinus sp
Prosthenorchis spirula Callithrix j. jacchus, Ileum, cecum Estado do Rio, 120,312,
Cebuella pygmaea, Brazil . 388, 456,
Saguinus mystax, S. 518
midas niger, S. o. oedi-
pus, Leontopithecus
rosalia
Prosthenorchis sp Callithrix jacchus, C. sp, Ileum, cecum Para and Espirito 155, 194,
Saguinus fuscicollis, Santo, Brazil; 197, 286,
S. geoffroyi, S. oedipus, London Zoological 312, 388,
S. mystax, S. sp, Gardens, England; 402
Cebuella pygmaea, South America;
Leontopithecus rosalia Philadelphia
Zoological
Park, PA
Acanthocephalan larvae Callithrix jacchus, Subcutaneous tissue South America 388
S. fuscicollis, S. oedipus

"Host was not reported.


bHabitat was not reported.
cGeographic location was not reported.

219
Potkay

with their presence. Intestinal cestodes were con- though the numbers of parasites per host were
trolled by treatment with niclosamide (Yomesan ™ , high.
Chemagro, Division of Baychem Corp, Kansas Physaloptera and the spirurids, Spirura and Pro-
City, MO) [74]. tospirura, were found attached to the mucosa of
Larval forms (spargana or plerocercoids) of Spi- the lower esophagus and stomach. Their presence
rometra and Diphyllobothrium were occasionally may be associated with lesions ranging in severity
seen in subcutaneous and retroperitoneal tissues and from inflammation and fibrosis to perforation. Ex-
in the abdominal cavities of tamarins. The adults ceptionally large numbers may occlude the esopha-
are intestinal parasites of carnivores, and the first gus [274,375], although the average number of par-
stage larvae (procercoids) are found in animals such asites per infection was seven for Spirura and one
as crustaceans, frogs, and snakes [120,274). Spar- or two per animal for Protospirura and Physa-
gana are found in small numbers (one to four), loptera.
encapsulated by connective tissues and cause little Pterygodermatites were observed attached to the
inflammatory response. Sparganosis was also de- submucosa of the small intestine and may also be
scribed in S. f illigeri having nodules in its thoracic found in its tunica muscularis and the pancreatic
cavity [180]. They consisted of fibrous cysts whose ducts. Clubbing of the intestinal villi and the forma-
walls, infiltrated with lymphocytes and plasma tion of a necrotic pseudomembrane were seen mi-
cells, surrounded intact and degenerating cestode croscopically. Severe infections were manifested
larvae and an aggregation of inflammatory cells. by diarrhea, weakness, hypoproteinemia, and ane-
Numerous viral particles were present in the cyto- mia; hundreds of parasites may be present. Some
plasm of the larvae; the proliferative nature of the of these spirurids require intermediate hosts such as
spargana was thought to have been related to the cockroaches (for Pterygodermatites) , crickets, or
viral infection. other insects to complete their life cycles, or infec-
Infection with larval forms of Taenia (cysticer- tion may be by skin penetration [166,521). Ham-
cosis) was occasionally observed in Saguinus sp sters, and perhaps other rodents, may serve as pos-
and was characterized by the presence of cysts con- sible reservoir hosts [521]. When it is not possible
taining single scolices [274). Various mammals to eliminate intermediate hosts from the callitrich-
serve as definitive hosts, and ingestion of eggs shed ids' environment, regular testing and treatment for
in feces results in cysticercosis. parasites should be considered. Mebendazol (Tel-
Hydatid disease (echinococcosis) was rarely seen min Paste™, Pitman-Moore, Washington Crossing,
in caIlitrichids [274). Hydatid cysts contain numer- NJ; 40 mg/kg per os) [346] or mebendazol (Meben-
ous daughter cysts, brood capsules, and scolices. vet™ 5%, Janssen; 10 mg/kg given twice subcuta-
The characteristic cyst wall is a nonnucleated lami- neously four days apart) [320] as well as ivermectin
nated structure delineated by a fibroid capsule laid (Ivermec™, Merck Sharp and Dohme-GUET;
down by the host. Final hosts of Echinococcus mul- 0.2 mg/kg per os) [320) have been used success-
tilocularis, observed in S. oedipus, are canids fully to treat and control Pterygodermatites infec-
[ 166]. Diagnosis of somatic cestodiasis is usually tions.
made at necropsy. Clinical signs have not been re- Trichospirura leptostoma infections in C. jac-
ported in affected tamarins, nor has treatment been chus produced mild to severe chronic pancreatitis
described. characterized by periductal fibrosis, ductular prolif-
eration, and atrophy of the exocrine pancreas [376].
The wasting disease-like syndrome present in af-
fected animals was thought to be the result of mas-
Nematoda sive infections [30]. Cockroaches (Blatella german-
Numerous species of nematodes occur in wild- ica and SupeUa longipalpa) harbored larvae and
caught callitrichids and those raised in captivity may be capable of serving as intermediate hosts.
(Table V). Cecal worms (Primasubulura and Subu- Adult and larval Filaroides occur in the alveoli
lura) and Trypanoxyuris were commonly present and terminal parts of the bronchioles. These meta-
in recently captured animals. Primasubulura was strongylids were found in masses (3-8 mm in di-
located primarily in the large intestine, parasites ameter) and were often evident as dark, slightly
being found in the cecum and small intestine when elevated lesions on pleural surfaces. They were
infections were heavy [Ill]. The numbers of para- sometimes associated with purulent pneumonitis
sites ranged from 4 to 981, and clinical signs in- [388), but were not commonly encountered. Filari-
cluded inappetence, flatulence, and severe diarrhea. opsis was, in a few cases, located in the bronchi-
Treatment with mebendazol (40 mg) for two con- oles, alveolar ducts, and alveoli, forming fibrous
secutive days was successful. Neither lesions nor nodules visible as brownish-yellow spots on the
clinical signs associated with Subulura or Try- pleural surface [403].
panoxyuris infections have been reported, even Infections by Angiostrongylus were also appar-

220
Callitrichid diseases

ently rare. Adult worms were found within mesen- Acanthocephalans


~eri.c arteries; their degenerating eggs and larvae
The most common and serious helminth infections
I~clted the development of large (0.75-2.5 cm in
encountered in caIlitrichids were caused by thorny-
diameter) weIl-encapsulated granulomas. Micro-
headed worms, Prosthenorchis elegans, and, less
?ranulomas were associated with eggs and larvae
frequently, P. spirula (Table V). Inhabitants of the
In the kidneys, liver, lungs, and heart. Slugs and
distal ileum, cecum, and proximal colon, they at-
fresh water snails serve as intermediate hosts for
tach to the muscular waIls by their proboscises and
~etastrongylids. A ngiostrongylus , unlike Filaro-
produce inflammation, necrosis, and fibrosis. Ab-
Ides. and Filariopsis, is also a parasite of man; in-
scesses at the site of attachment were often visible
fectIOns are acquired by ingesting intermediate
through the serosal surface, ranging from a few
hosts or vegetables contaminated with infective lar-
millimeters to more than a centimeter in diameter.
vae [437].
Mesent.eric lymphadenitis was commonly associ-
?f the trichostrongylids, Molineus and Longi-
ated with acanthocephalid infections, and spleno-
:trzata were most commonly encountered. AI-
megaly occurred when large numbers were present.
hough the number of parasites per host averaged
Local or general peritonitis may be present, and
above seven, heavily infected animals may harbor
perforations can lead to fatal peritonitis and septice-
dozens. The pathogenicity of and treatment for
mia. Specific clinical signs have not been reported,
these parasites have not been described. Infections
although affected animals may be depressed or in-
probably result from ingesting infective larvae or
appetent. The number of worms per infection aver-
thro~gh skin penetration by larvae. Although Stron-
aged from eight [388] to more than 30 [120J. Exam-
g~lOl.des was said to be a common parasite of calIi-
inations of feces for eggs often give variable results
tnchlds, there were few specific reports of its occur-
because eggs may not be shed continuously, and
rence. It has been postulated that infections are
may not be reliable diagnosticaIly unless many tests
ac~uired at compounds where animals are held
are performed [351]. Capsules containing 0.1 gr
pnor t~ e.xport [388], or they may be acquired later
calomel, 0.05 gr santonin, and 2.0 gr milk-sugar
In captlVlty. The route of infection is oral or skin
followed by 1 teaspoon of castor oil per os were
pen~tration by larvae [166]. S. stercoralis is patho-
reported to be an effective treatment [54,205,294],
gemc for people. Oesophagostomum has been ob-
as was carbon tetrachloride [227], but these results
served only in tamarins housed in proximity to
have not been confirmed. The newer broad spec-
Macaca, which commonly harbor these nodular
trum anthelmintics, thiabendazole (25-35 mg/kg
~orms; infections are acquired by ingesting infec-
oraIly for four days) and mebendazol (15 mg/kg
tIve larvae.
orally for two days, or 3 mg/kg oraIly for ten days)
There was a high incidence of infection by one .
were said to be effective, but supporting data were
~r ~~re .s~ecies of fil.arial worms in wild-caught
not given [187]. More recently developed drugs
al~Itnchlds. Adult DIpetalonema were found in
such as ivermectin have apparently not been evalu-
pentoneal and pleural spaces where they may be
ated. Cockroaches and certain beetles serve as in-
~sSociated with inflammation and adhesions, or
termediate hosts, and unless they can be eliminated,
In subcutaneous tissues. Adult Tetrapetalonema
fou infections may become permanently established in
fa . ~ d In
. the subcutaneo~s tissue and intermuscular'
captive callitrichid colonies [459] .
. SCIa of the back and In subscapular connective
tIssue, evoke little inflammatory response. Adults
of these genera are generaIly present in smaIl (two Arthropod paraSites
~o four) numbers. Microfilariae are seen often
In Iarge numbers, in the vascular beds of' many There are few reports of parasitism by arthropods,
organs. Based on morphologic and histochemical although reduviid bugs, mosquitoes, midges, and
chara
. ctenstIcs,
" . . representing eight spe-
mlcrofilanae sandflies are known to transmit certain viruses
c~s ?f filarids have been described, but it has been and parasites such as Trypanosoma, Dipetalonema,
~orsslble to cor:relate o.nly fi~e. of .these with adult and Leishmania that have been identified in caIli-
bloillS [68]. ~Icrofilanal actlVlty In the peripheral trichids.
si od .has a dlU:nal peak that suggests that transmis-
on. IS by WInged, blood-sucking arthropods-
Mites
fosSlbly mosquitoes or midges-that bite most
requ.ently during daylight hours [122]. Infections Several species of mites (Table VI) parasitize cal-
~e diagnosed by finding microfilariae in peripheral Iitrichids, but the incidence of acariasis is rare.
C~o? sa~ples, at necropsy or histopathologically. Demodicosis in as. geoffroyi was characterized by
.mcal signs have not been reported in affected alopecia, cutaneous erythema, and papule forma-
ammals, nor have treatment regimens been evalu- tion on the head, tail, and limbs [226]. Microscopi-
ated and reported. caIly, there was focal degeneration and inflamma-

221
Potkay

tion of the skin around hair follicles, which collis, but most authors are of the opinion that fleas
harbored mites identified as Demodex sp. Ronnel do not normally parasitize callitrichids. Callithrix
(1 % solution) (EctoraI™, Pitman-Moore, Washing- sp was reported as a host for Amblyomma cajen-
ton Crossing, NJ) and rotenone ointment (Good- nense in Brazil [II]; Amblyomma sp, Ornithodorus
winal Ointment™, Goodwinal Products Corp, Hun- talaje, and O. rudris were associated with S. o.
tington Station, NY) were effective in treating the geoffroyi [78,125]; and immature Amblyomma sp
condition. Other cutaneous mites parasitizing calli- was reported from L. r. rosalia [511].
trichids may also produce moderate to severe der-
matitis [136,137] with hyperkeratosis and dermal Midges
crusting [293], but the significance of Mortelman-
Culicoides espinolai and C. minasensis were re-
sia found in nasal passages is unknown [121].
ported to bite C. penicillata and man [145,146].
Lice
Pentastomes
Pediculus I. lobatus infection of captive S. nigri-
Porocephalus clavatus nymphs are commonly
collis weddelli was considered to be the result of
found in tamarins (S. fuscicollis, S. nigricollis, and
close contact with infected Ateles paniscus [242).
S. mystax) and less frequently in marmosets (c.
Two mallophagan lice, Gliricola pinto and Har-
jacchus), which serve as intermediate hosts of this
risonia uncinata, were described from museum
pentastome [28,66,87,196,274,358,384,431). P.
specimens of C. h. humeral(fer, and are thought to
crotali and P. subcylindricum have also been re-
be contaminants or accidental infections [242]. It
ported from L. r. chrysopygus in Brazil (455). Eggs
is unlikely that either anopluran or mallophagan lice
from adult P. clavatus are passed in the feces of
parasitize callitrichids in nature.
definitive hosts (large snakes such as boas) [304];
they hatch after ingestion by the intermediate host,
Fleas and Ticks
and the larvae migrate into internal organs where
Ctenocephalides f. felis was reported from C. j. they develop into infective nymphs. The nymphs
penicillata and S. o. geoffroyi, and unidentified are wingless and legless, and have an annulated
fleas were listed as being associated with S. nigri- appearance. They are found in semitransparent

Table VI. Parasitic mites of callitrichids

Name Host References


Demodicidae
Demodex sp Saguinus oepidus geoffroyi 226
Trombiculidae
Euschoengastia sp Leontopithecus r. rosalia 511
Eutrombicula alfreddugesi Saguinus oedipus geoffroyi 53, 511
Eutrombicula goeldii Saguinus oedipus geoffroyi 53
Microtrombicula brennani Leontopithecis r. rosalia 185,511
Pseudoschoengastia bulbifera Saguinus oedipus geoffroyi 53
Speleocola tamarina Leontopithecus r. rosalia 186,511
Listrophoridae
Listrocarpus hapalei Callithrix jacchus 141
Listrocarpus cosgrovei Saguinus fuscicollis 87, 141
Rhyncoptidae
Rhyncoptes anastosi Saguinus o. oedipus, S. sp, 139,511
Leontopithecus rosalia
Rhycoptes recurvidens Saguinus nigricollis, 292
Leontopithecus rosalia
Lemurnyssidae
Mortelmansia duboisi Callithrix j. jacchus 138, 286
Psoroptidae
Cebalgoides cebi Saguinus o. oedipus 136
Fonsecalges johnjadini Callithrix j. geoffroyi 136
Fonsecalges saimiri Saguinus nigricollis, 87, 140
(= Dunnalges lambrecchti) S. fuscicollis
Other
Mites Saguinus nigricollis 358
Mite eggs (in fecal specimens) Saguinus sp 108
.. --- - ----- - ----- - - ._-----

222
Callitrichid diseases
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