key: cord-0962374-uwrwlkx8
authors: Kramer, Joshua A.
title: Diseases of the Gastrointestinal System
date: 2018-11-23
journal: The Common Marmoset in Captivity and Biomedical Research
DOI: 10.1016/b978-0-12-811829-0.00013-3
sha: 56631120062929a9022a2e3dbc80735f46ae8ac6
doc_id: 962374
cord_uid: uwrwlkx8

In captivity, gastrointestinal diseases are the most common clinical finding in common marmosets. Clinical signs may be due to a host of etiologies and typically manifest as weight loss, diarrhea, changes in eating habits, and/or abdominal distension. Proper recognition of clinical signs and identification of the underlying cause(s) is important to maintain the health of the individual animal and colony as a whole.

In captivity, gastrointestinal (GI) diseases are widespread and the most common clinical finding in common marmosets [1e6] . Clinical signs may be due to a host of etiologies and typically manifest as weight loss, diarrhea, changes in eating habits, and/or abdominal distension. Proper recognition of clinical signs and identification of the underlying cause(s) is important to maintain the health of the individual animal and colony as a whole.

Marmosets are broadly characterized as frugivores, insectivores, and exudivores; and their GI system is adapted to meet the needs of this diverse diet [7] . Their teeth and bone structure allow them to gouge tree bark to eat edible plant exudates including gum, sap, and latex [8] . This gouging behavior not only exposes the sappy interior but also stimulates the plant to produce gum, thus resulting in a long-term food source [9, 10] . To better digest the gums, marmosets have a large cecum for their body size, which enables efficient fermentation. They may also be able to preferentially retain liquids (i.e., gums) in the cecum while sending solid food to the colon, and their cecum has extensive folds and pockets that may allow for retention of bacteria to repopulate the upper colon when needed [11] .

Marmosets in captivity are generally fed a commercial marmoset diet supplemented with fruit, vegetables, and insects or other sources of protein, such as eggs. Due to limitations in caging and diet formulation, the diet fed to captive marmosets likely does not recapitulate their natural diet, which can lead to nutrient deficiencies, secondary metabolic disorders, or inflammatory disease of the GI system. Care should be taken to avoid feeding diets high in simple sugars, such as glucose. While palatable, these diets can lead to secondary clinical problems, as noted below. While it was historically common to feed mouse pups to marmosets, this should be avoided due to the risk of disease transmission.

Additional detail on marmoset nutrition, including vitamin requirements, is discussed elsewhere in this volume. However, it should be noted here that marmosets have a dietary requirement for vitamin D3 due to a reported end-organ resistance [12] . Inadequate D3 levels in feed can result in osteomalacia or other bone pathology. This is covered in additional detail elsewhere in this volume.

Because clinical signs of GI disease are readily apparent to caretakers, veterinary staff are often tasked with identifying the potential causes of diarrhea in marmosets. Every investigation should begin with a thorough cageside examination to better understand the animal's temperament, activity level, and overall appearance. From there, a physical examination should be performed and include evaluation of the oral cavity and abdominal palpation. Veterinary staff should become familiar with the normal characteristics of marmosets including the thickness of the gut loops, liver size, and mesenteric lymph node size. Given their small size, it may be possible to perform a basic examination on awake, restrained animals. However, sedation enhances the ease through which abnormalities can be detected on abdominal palpation and reduces the risk of injuries to staff or animals.

In some cases a physical examination may allow proper diagnosis of a condition. However, additional diagnostics may be required. Radiography and ultrasonography are both readily available and easy to perform and can provide useful diagnostic information. Again, the clinician should become familiar with what is normal utilizing healthy animals as a baseline. There are also published resources available to describe normal radiographic and ultrasonographic anatomy [13, 14] .

Infectious causes of GI disease are not uncommon. Fecal bacterial culture is important when considering bacterial causes of GI diseases and many viruses can be identified through PCR or other techniques. Fecal flotation, sediment analysis, or direct examination are useful to identify parasites and protozoa.

More advanced diagnostics such as colonoscopy and biopsy may also be considered and can provide useful diagnostic information for some bacterial, viral, neoplastic, or inflammatory conditions. Intestinal biopsy with or without colonoscopy is easily performed utilizing pinch biopsy forceps with an opening measuring approximately 4 mm. Liver biopsy can be obtained percutaneously or via a small paracostal incision.

In those institutions maintaining colonies of marmosets, consideration should be given to longitudinal tracking of colony health. Tracking body weight and body condition scores is a simple method that can provide useful long-term data on colony health. More complex analyses of body composition, such as EchoMRI or DEXA scans, can also be used and may be simple to perform in marmosets trained to cooperate. This is covered in more detail elsewhere in this book. These modalities can provide useful information to track changes in fat, lean mass, and bone composition over time to evaluate changes in colony health and may be able to identify subtler changes.

Finally, necropsy of index cases also serves as a useful diagnostic tool, especially in larger colonies. A complete and thorough necropsy provides valuable diagnostic information that may not be obtained through other methods. Necropsy examination should be performed by a trained pathologist or person familiar with normal marmoset anatomy and abnormal tissues should be submitted for histopathologic evaluation. Additionally, in the event of an epizootic, euthanasia of affected animals may help limit the spread of the agent, thereby preserving the health of the remainder of the colony.

The GI tract is large and encompasses different organ systems, each of which has its own spectrum of common diseases. Each system will be covered individually below. In addition, specific detail on the multisystemic manifestation of some diseases may be found in other chapters of this manuscript.

Examination of the oral cavity should be a part of every physical examination. Traumatic injuries to the teeth are common and should be identified and treated appropriately to prevent continued oral pain or ongoing pathology.

Marmosets have a symmetrical upper and lower tooth arcade with two incisors, one canine, three premolars, and two molars. Detailed descriptions of the order of tooth eruption have been published [15, 16] . They are specially adapted to eat plant exudates and in the wild may spend up to 30%e67% of their time foraging for exudates. To aid in this endeavor, they use specially adapted teeth [8] .

Tooth damage is a common source of morbidity in captive marmosets. Any damage that exposes the root cavity may lead to bacterial infection and a resultant abscess. A common cause of damage is tooth fracture as a result of handling, but wear from enrichment devices, cage material, or other sources may also lead to dental wear and eventual exposure of pulp cavity.

Marmosets with damage to upper teeth present with facial swelling on their cheek, lateral to the nares and below the eye ( Fig. 13.1 ). This is sometimes associated with oculonasal discharge. Damage to lower teeth is less common but can result in abscess formation on the chin or upper neck. Swelling often begins as a red discoloration, progressing rapidly to abscess formation and purulent exudate. Bacterial isolates from the lesions vary, and bacteria may invade the maxilla which will be evident radiographically [17] . Treatment often requires removal of the affected tooth to allow drainage (Chapter 10 of this volume, figures 10 and 11) with subsequent antibiotic treatment to prevent osteomyelitis, damage to the orbit or globe, or sepsis.

literature, but one would presume that dietary factors including reduced mechanical cleaning of teeth due to reduced tree gouging behavior may play a role. A variety of bacterial isolates may also be present. Periodic dental examinations during routine preventive health assessments along with prophylactic cleaning should be performed to prevent gingivitis and periodontal disease.

While marmosets may be susceptible to a wide range of oral viral pathogens, by far the most important are herpes infections. These agents can cause significant morbidity and mortality, which can greatly affect captive colonies. Care should be taken to avoid infection by strictly separating callitrichids from other species of New World monkeys.

Etiology: Human herpesvirus 1 (HHV-1) (herpes simplex virus) has been identified as the cause of outbreaks of vesicular stomatitis in common marmosets. In all cases, animals have been exposed to a caretaker with recrudescent herpesvirus lesions several days earlier.

Clinical signs: HHV-1 infection is rapidly progressive and animals may die within 1e4 days [18] . Clinical signs include ulcerative lesions on the tongue, gingiva, and lips, which are associated with anorexia, weakness, and hypersalivation. More rarely, signs may progress to include more fulminant signs such as seizures [18, 19] .

Pathology: Pathology findings are consistent with the clinical signs and include vesicular and ulcerative lesions of the oral and esophageal mucosa. Inflammatory exudate and intranuclear inclusion bodies are associated with these lesions. Animals that live longer may develop meningoencephalitis [19] .

Prevention and control: Due to the potential for this virus to spread from animal to animal within a colony, suspected cases should be euthanized immediately and submitted for pathologic examination. Contact animals should be quarantined and observed closely for clinical signs to prevent the spread of disease to other animals in the group. Caretakers with suspect clinical signs should be assigned alternative work duties to prevent exposure of the colony.

Etiology: Herpesvirus tamarinus is an alphaherpesvirus related to Herpes simplex whose natural host is the squirrel monkey [20] . Spider monkeys and some animals in the genus Cebus may also be latent carriers [21] . Though rarely a source of disease in squirrel monkeys, it causes ulcerative and vesicular stomatitis in aberrantly infected callitrichids [22] .

Clinical signs: The disease course and clinical signs are similar to that noted for Herpes simplex, with a short incubation period and relatively rapid progression to death. In addition to stomatitis, infection is associated with hepatosplenomegaly, ulcerative gastroenteritis, and multifocal necrosis in the adrenal glands, liver, and lymphoid tissue.

Pathology and diagnosis: Clinically apparent oral vesiculation and ulceration should cause a high level of suspicion, and diagnosis can be achieved by biopsy or through viral isolation from saliva. Biopsy will show ulcerative and vesicular lesions with suppurative inflammation, viral syncytia, and intranuclear viral inclusion bodies.

Prevention and control: Treatment with antiherpetic drugs has not been reported, and consideration should be given to euthanize infected animals, and potentially their contacts, to limit the spread of the agent and prevent an epizootic. Because of the risk of this virus, there should be strict separation of callitrichids from other New World primate species. Suspected cases should be euthanized for a diagnostic evaluation including necropsy and histopathology, and contact animals should be quarantined and closely observed.

Candida albicans can infect marmosets but is generally only associated with disease in debilitated animals in whom it may cause thrush [23, 24] . Thrush is characterized by a white discoloration and proliferation on the tongue and in the esophagus. Lesions are most common in the upper GI tract but may be present in other regions as well. Oral nystatin wash or fluconazole may be effective, and treatment aimed at eliminating the cause of debilitation or immunosuppression should be initiated.

In general, neoplastic diseases of the oral cavity are rare in nonhuman primates, including common marmosets. There is, however, a report of oral and nasopharyngeal squamous cell carcinoma affecting eight animals (4.9%) in a single colony [25] . These tumors were locally invasive with expansion into the jaw and/or palate, retrobulbar space, or base of the cranium. While a similar incidence of this specific neoplasm has not been reported elsewhere, it should be included as a differential diagnosis for oral proliferative lesions.

As in other primate species, marmosets should be provided a balanced diet containing essential nutrients II. DISEASES AND CLINICAL APPLICATIONS DISEASES OF THE ORAL CAVITY AND ESOPHAGUS and vitamins. With respect to oral health, vitamin C and niacin are both essential to maintain the integrity of the oral mucosa.

Vitamin C is required to cross-link collagen and therefore an essential dietary nutrient in species lacking gulonolactone oxidase, including marmosets. Deficiency (scurvy) affects multiple species of primates. Marmosets have been reported to have a relatively high requirement for vitamin C and to develop clinical signs after approximately 10 weeks of absolute restriction.

Clinical signs include weight loss, altered gait, and gingival hemorrhage. At necropsy, animals may have hemorrhages around joints and in muscles. Histologically, there was prominent hemorrhage around the periodontal ligament despite not having the characteristic gingivitis that plagues other species of primates [26e29].

To prevent this disease, animals should be fed a commercial diet with adequate levels of vitamin C. Care should be taken to monitor the shelf life and refrigerate diets according to the manufacturer's recommendations to prevent loss of vitamin C over time and secondary nutritional deficiency. Animals that develop clinical signs should be treated with dietary supplementation of at least 500 ppm and by injection of vitamin C, but marmosets may be refractory to treatment [27] .

Other nutrient deficiencies may also manifest as oral disease including vitamin A [30] , folic acid [31] , and niacin [32] deficiencies. Vitamin A deficiency causes aberrant epithelialization and keratinization of the oral mucosa. Folic acid deficiency causes impairment of keratinization and secondary ulceration, which results in weight loss and anorexia. When the related species Saguinus oedipus was fed a diet deficient in niacin, animals developed ulcerative stomatitis, ulcerative enterocolitis, and ulcerative and atrophic glossitis [32] . Clinical signs included anorexia and weight loss as a result of the extensive oral and intestinal lesions. Prevention of all of these syndromes can be accomplished through provision of a well-balanced diet.

Though rare, clinicians should be cognizant of potential congenital malformations in marmosets that are aborted near full gestational age or that die soon after birth. Recently, one marmoset breeding colony in the United States had three cases of cleft palate. In all cases, animals developed to full term. One was still-born, one died perinatally, and one lived to 4 days old but eventually died. No other malformations were present [33] . There has also been a single case report of cleft palate in an aborted brown-mantled tamarin fetus [34] . In another report, a single animal was born with cleft lip and cleft palate, microphthalmia, and polydactyly. The animal was born at full term but euthanized after being rejected by its parents. Together, this triad of congenital malformations suggests 13 trisomy [35] .

Diseases affecting the stomach and intestine of marmosets are the cause of significant morbidity and mortality in marmoset colonies around the world. Often the presenting complaint is diarrhea. Utilization of a scoring system to track diarrhea longitudinally may prove useful, and such systems have been published [36] . Clinicians should become familiar with the common causes of diarrhea and weight loss and pursue diagnostic tests as appropriate to each case.

Scientific reports of bacterial enterocolitis in common marmosets are surprisingly rare. Marmosets are likely as susceptible to a similar variety of GI pathogens as other primates, including humans. If a bacterial disease is identified, care should be taken to ensure overall colony health by identifying and treating subclinical carriers in addition to those animals with recognizable clinical signs. In addition, many of these pathogens are zoonotic risks, highlighting the need for personal protective equipment and strict sanitation.

Etiology: Escherichia coli is a Gram-negative bacillus that includes a diverse array of serotypes and pathogenic subtypes. Enteropathogenic E. coli positive for the attaching and effacing locus have been responsible for outbreaks of hemorrhagic diarrhea in common marmosets and related species [37e40]. In two reports, E. coli was positive for the attaching and effacing (eae) gene, negative for shiga toxin production, and were identified as serogroup O26. This serogroup is associated with outbreaks of diarrhea and hemolytic uremic syndrome in man and thus represents a potentially serious zoonotic threat to caretakers [38] .

Clinical signs: Clinical signs in infected animals include weakness, lethargy, dehydration, and voluminous watery diarrhea that progresses rapidly to include hemorrhage [39, 40] . Individual cases, or, commonly, outbreaks of diarrhea, should cause a high index of suspicion. Anecdotally, some animals may present with red-tinged urine as well.

Pathology: Intestinal biopsies or samples of intestine from necropsy will show mucosal erosion, adherent bacillary bacteria, and a cobblestone appearance to the mucosa. This attaching and effacing lesion is pathognomonic and may aid in the rapid diagnosis of infection.

Diagnosis: Diagnosis can be made through fecal culture on MacConkey agar, and E. coli culture should be specifically requested from the diagnostic lab. If E. coli is cultured, serotyping can be pursued to identify the exact etiology and relative risk to humans.

Prevention and control: Prevention of the introduction and spread of disease should be accomplished through washing of fruits and vegetables fed to animals, hygiene of caretakers, and strict use of personal protective equipment. Treatment should be initiated based on bacterial sensitivity results, but empirical selection of enrofloxacin dosed orally or parenterally is normally effective.

Etiology: Klebsiella pneumoniae is a Gram-negative bacillus that has been associated with outbreaks of fatal peritonitis and GI disease in common marmosets [1, 2, 41, 42] and other New World primates [43] .

Clinical signs: In marmosets, clinical signs include anorexia, mesenteric lymphadenopathy, diarrhea, and peritonitis.

Pathology: At necropsy, animals generally have ulcerative colitis and fibrinopurulent peritonitis with bacterial septicemia and dilated colonic crypts ( Fig. 13 .

Diagnosis: Diagnosis is readily made through culture, and sensitivity testing should be performed as bacteria may harbor resistance genes.

Prevention and control: Treatment with enrofloxacin should be rewarding unless the particular strain is resistant. Consideration should be given to screening contact animals with nasopharyngeal and/or rectal cultures and treating any animals identified as carriers with an appropriate antibiotic.

Etiology: Shigella sp. are common pathogens of laboratory primates. Shigellosis is highly contagious and inoculation with as few as 10 organisms may cause infection [44] . Shigellosis is less commonly reported in marmosets than in other nonhuman primate species, but infection with Shigella sonnei has been reported [23, 37] .

Clinical signs: Clinical signs include depression, lethargy, and dehydration due to ongoing hemorrhagic diarrhea. Facial edema, likely due to fluid imbalance, may also be seen.

Pathology: At necropsy, animals will have necrotizing, hemorrhagic, and ulcerative typhlocolitis, similar to the pathology of other nonhuman primates with shigellosis.

Diagnosis: Diagnosis is made through fecal culture. However, laboratory misdiagnosis is not uncommon, and there is some difficulty in distinguishing E. coli and Shigella [44] . In an outbreak situation, consideration should be given to utilizing alternative diagnostic modalities such as PCR to properly identify the etiologic agent.

Prevention and control: In the cited report, treatment with neomycin was effective; however, one should consider utilizing enrofloxacin or trimethoprime sulfamethoxazole, which is utilized with success in other species including man [44] . Due to the risk to other animals and zoonotic potential for this pathogen, care should be taken to isolate infected animals, utilize rigid personal protective equipment practices, and properly sanitize the environment. Treated animals should be cultured or examined by PCR following cessation of therapy to identify any residual carriers. These animals should undergo further treatment until cultures and/ or fecal PCR show elimination of the carrier state.

Helicobacter sp.

Various species of Helicobacter have been isolated from marmosets including Helicobacter jaachi, Helicobacter callitrichis, and others [45e47]. Due to the nature of the surveys conducted, a correlation with any specific clinical sign or disease syndrome is not possible. In one survey [45] , identification of Helicobacter sp. histologically was not associated with pathologic changes in the stomach.

Etiology: Clostridium perfringens is an anaerobic sporeforming, rod-shaped bacterium associated with gas gangrene in a variety of species. There are scant reports of Clostridium perfringens causing anorexia, diarrhea, gas gangrene, and death in marmoset colonies including one in which 29 animals died due to gastric dilation following antibiotic treatment for shigellosis [48, 49] . 

Clinical signs: Animals may develop facial swelling and facial erythema. Death is often rapid and sudden, and the GI tract is distended by gas.

Pathology: The intestines, in addition to gas, contain watery brown-gray fecal material and may also have areas of necrosis and mucosal sloughing. Bacteria can be identified in GI contents. In addition, organisms may be identified circulating in the blood and within various tissues, including muscle, bile ducts, liver, lungs, and kidney.

Prevention and control: Given the rapid clinical course, animals may die without premonitory clinical signs. If a diagnosis is made, treatment with antibiotics such as clindamycin, rifampin, or tetracycline should be considered. Prophylactic treatment of other potentially exposed animals may help prevent additional deaths due to this disease.

Clostridium difficile may also be associated with disease but is rarely reported. A high index of suspicion should occur if animals develop diarrhea following antibiotic therapy. Affected marmosets develop bloody diarrhea, weakness, and collapse. Antibiotic therapy alters the normal gut microbiota and allows proliferation of toxin-producing C. difficile. At necropsy, lesions range from mild mucosal edema to pseudomembranous colitis. Transmural cecal and colonic necrosis may also be seen [50e52].

Yersinia enterocolitica is a Gram-negative coccobacillus that causes gastroenteritis in humans. Y. enterocolitica and its relative Y. pseudotuberculosis have been reported in other species of primates; and while rarely reported in marmosets, it can cause diarrhea [3, 53, 54] . The most prominent pathologic change is hepatic necrosis, but there may also be necrosis in the small and large intestines. Diagnosis can be achieved through histologic findings of index cases, fecal culture, or PCR. Treatment may be unrewarding but should include supportive care and aggressive antibiotic therapy with fluoroquinolones or trimethoprimesulfamethoxazole.

Mycobacteria sp.

Atypical mycobacterial species, including Mycobacterium kansasii and Mycobacterium gordonae, can be isolated from the GI tract including stomach fluid and feces [55] . While not associated with clinical GI disease, bacteria are associated with mesenteric lymphadenitis, and enlarged abdominal lymph nodes can sometimes be palpated. Perhaps most importantly, atypical mycobacteria can cause positive reactions to tuberculin skin tests in marmosets and therefore must be distinguished from Mycobacterium tuberculosis infection.

While parasitic diseases were very common historically, changes in husbandry including the use of antiparasitic drugs and effective pest control have reduced their burden in many marmoset colonies.

Etiology: Giardia is a flagellated protozoan parasite. Clinical signs: Giardia sp. has been identified as a common organism in the feces of marmosets but is not generally associated with immediate clinical signs. It may be more common in animals <1 year of age [36, 56] .

Diagnosis: Diagnosis can be accomplished through ELISA of fecal specimens, and testing of colonies may show a high prevalence of infection despite a lack of appreciable clinical signs. Direct examination of fecal flotations can also be used but is less sensitive than immunoassays. Organisms can also be identified histologically as small crescent-shaped or teardrop-shaped organisms with paired nuclei in the lumen (Fig. 13.3) . Regardless of the diagnostic methodology chosen, multiple samples should be sampled over the course of several days due to intermittent shedding.

Prevention and control: Eradication with two doses of oral tinidazole was effective at eliminating the disease and this was associated with weight gain 1 year later. This suggests that elimination of Giardia sp. from colonies is worthwhile to improve the overall colony health and may help reduce the incidence of unexplained 

13. GASTROINTESTINAL DISEASE weight loss, which is generally associated with inflammatory bowel disease (IBD) [36] .

Isospora arctopitheci can infect marmosets. Parasites invade the small intestinal epithelium and, while most infections remain subclinical, may cause clinical signs including bloody diarrhea. In severe infections, animals may die between 3 and 7 days post infection. Oocysts can be identified on fecal flotation or sedimentation. At necropsy animals will have small intestinal lesions characterized by sloughing of the intestinal epithelium. Sporocysts, macrogamonts, and microgamonts are usually visualized in epithelial cells at the distal end of intestinal villi, especially the jejunum. Mice serve as an intermediate host; and therefore, feeding of mouse pups to marmosets should be avoided [57e59].

Prosthenorchis elegans attaches to the wall of the ileum where it forms a fibrous nodule and is associated with inflammation near the site of attachment. In some animals, there may be adhesions between the ileum and adjacent structure, abscess formation, or septic peritonitis resulting from partial rupture of the ileum [60, 61] . Depending on the degree of inflammation and adhesion formation, animals may present with no clinical signs or they may present with abdominal turgor, lethargy, weakness, or signs of sepsis.

Entamoeba coli may be present in the GI tract but is not often associated with disease and is considered, like in other primate species, nonpathogenic in most cases.

Cryptosporidium parvum is a known pathogen of a variety of species and has been reported in symptomatic and asymptomatic marmosets [56, 62] . On histology, small, round, blue organisms are seen at the luminal surface ( Fig. 13.3) . Treatment with paromomycin has proven effective.

Morbilliviruses Etiology: Morbilliviruses are RNA viruses associated with disease in a variety of species. The most common Morbillivirus is measles virus, which is the cause of significant morbidity and mortality in primates.

Clinical signs: In Old World monkeys, it is associated with a multisystemic disease centered on the skin, lymphoid system, brain, and lung. Unlike Old World primates and man, callitrichids infected with either measles or the closely related Paramyxovirus saguinus usually develop a GI syndrome characterized clinically by diarrhea, dehydration, and progressive lethargy. However, upper eyelid edema, a skin rash, and pneumonia can also be seen [63] .

Experimentally infected mustached tamarins generally succumbed within 2 weeks of infection [64] . Outbreaks have been reported in several species of callitrichids with up to a 100% mortality in some species [63, 65] . In these situations, death may occur as soon as 8 h after onset of clinical signs and not all animals will show clinical signs.

Pathology: Gross pathology findings include hemorrhagic gastroenteritis and colitis and variable pneumonia. Histologically, there is multifocal necrotizing gastroenterocolitis and/or bronchointerstitial pneumonia depending on the tropism of the specific virus. Large syncytial cells containing intranuclear and intracytoplasmic viral inclusions may be present in the gut, bile ducts, pancreatic ducts, renal tubules, bronchial epithelium, or hepatic cords; and there may be necrosis of lymphoid tissue, which is typical of morbillivirus infection.

Prevention and control: Based on these reports and clinical knowledge of the disease in man, every effort should be made to prevent entry of measles virus into research colonies. Contact with personnel should be limited to those who have been vaccinated and/or screened for positive antibody titers. If an outbreak does occur, affected animals should be quarantined and consideration should be given to culling affected animals early to help limit the spread of disease.

Vaccination is a common practice in colonies of macaques and other Old World primates. Marmosets have been successfully vaccinated [64] . While routine vaccination does not appear to be a common practice, vaccination with the human measles or canine distemper-measles vaccine should be considered to protect colony health in an epizootic. Treatment of affected animals, if attempted, should include rehydration, supportive care, and antibiotics to treat and prevent secondary infections.

Etiology: Ateline herpesvirus 2 and 3 (Herpesvirus ateles) is a gammaherpesvirus in the genus Rhadinovirus related to EpsteineBarr virus (EBV) whose natural host is the spider monkey [66e68]. When experimentally inoculated in common marmosets, it causes Hodgkin's-like lymphoma, which may manifest as GI disease due to proliferation of neoplastic lymphocytes in the gut and abdominal lymph nodes.

Saimiriine herpesvirus 2 (Herpesvirus saimiri) is a closely related herpesvirus whose natural host is the squirrel monkey. In squirrel monkeys, it is not generally associated with disease but can persistently infect marmoset lymphocytes and cause malignant transformation [66,67,69e71] .

Clinical signs: For both agents, disease has been reported to start approximately 2e3 weeks postinoculation and may prove fatal by 3e4 weeks; but longer courses with slower-growing lymphomas have also been described. Disease is characterized by a mild-to-moderate leukocytosis, circulating neoplastic cells visible on blood smears, generalized lymphadenopathy, and hepatosplenomegaly. Animals may also have upper respiratory disease including nasal discharge.

Pathology: At necropsy, there is diffuse lymphoma affecting multiple organs that can include those noted above plus kidney, adrenal gland, tonsils, and lung. Aggressive cases may also be associated with extensive hemorrhage and necrosis in vital organs. Treatment has not been described though animals have been vaccinated using an attenuated viral strain. Vaccination successfully protected animals from subsequent challenge [72] .

Prevention and control: Because of the risk of this virus, there should be strict separation of New World primate species. Suspected cases should be euthanized for a diagnostic evaluation including necropsy and histopathology, and contact animals should be quarantined and closely observed.

Human herpesvirus 4 (EBV) causes mononucleosis, lymphoma, and nasopharyngeal carcinoma in people. While infection to callitrichids has been documented, common marmosets seem relatively resistant to lymphoma development following EBV infection [73, 74] . However, some strains may be more or less oncogenic, and EBV/HHV-4 should be considered as a differential diagnosis for malignant lymphoma in the marmoset [69] . Animals that do progress to lymphoma have a more protracted course than with Herpesvirus ateles or saimiri with lymphoma developing 4e8 weeks post infection.

Finally, Callitrichine herpesvirus 3 (CalHV3) has also been associated with GI lymphoma, although an etiologic relationship has not been established. Animals develop clinical signs including inappetence, diarrhea, and weight loss and often have palpable abdominal masses. At necropsy, B cells invade the gut and cause enlargement of mesenteric lymph nodes. While seroprevalence may be as high as 60% in some colonies, the incidence of GI lymphoma may be low [75e77]. Currently it is not clear whether CalHV3 is the etiologic agent responsible for these lymphomas or if it is detected in these lesions because of their high B-cell content.

Experimental infection with the SARS coronavirus has been reported and resulted in diarrhea associated with mild diffuse colitis. At necropsy, animals had colonic crypt hyperplasia [78] . Experimental yellow fever infection has been associated with hemorrhagic diarrhea and melena, with findings of hemorrhagic gastroenteritis at necropsy [79, 80] .

The most common GI tumor of common marmosets is small intestinal adenocarcinoma [81e83]. Tumors generally originate in the proximal jejunum but may also be present in the distal jejunum or ileum. Metastasis to the mesenteric lymph nodes is common and has also been reported in the lung and kidney.

Not surprisingly, the most common clinical signs are diarrhea and weight loss, though animals may also present with abdominal bloat. At necropsy, there is focal thickening of the small intestine with or without stricture. In man, gastric carcinomas have been associated with EBV infection and with Helicobacter sp. infection. Neither was identified as a potential cause for small intestinal adenocarcinomas in the largest report to date [83] . Based on these results, small intestinal carcinoma should be considered as a differential diagnosis in cases of diarrhea for which another underlying cause cannot be identified.

GI lymphoma is not uncommon and may be associated with a viral cause including Callitrichine herpesvirus 3, Herpesvirus saimiri, Human herpesvirus 4 (EBV), or Herpesvirus ateles as described above.

Reports of other proliferative diseases in common marmosets are exceedingly rare. There is a single case report of an inflammatory fibroid polyp in the duodenum of a common marmoset [84] .

Etiology: No discussion of GI disease in common marmosets would be complete without the discussion of IBD. In marmosets, this condition has historically been called marmoset wasting syndrome (MWS). In reality, the historical MWS is most likely a group of distinct disease entities that present with similar clinical signs but diverse etiologies and associated pathology [41] . Because MWS lacks diagnostic specificity, its use should be discouraged and marmoset diseases causing significant weight loss or wasting should be referred to by their etiology or associated morphologic changes. IBD is a known entity and will be described further.

Clinical signs: Clinical signs for both small and large intestinal IBDs are apparently similar in marmosets. Clinically, IBD animals present with diarrhea, weight loss, alopecia, and a failure to thrive. Bloodwork may show hypoproteinemia, anemia, and elevated liver enzymes [85] . As the condition progresses, animals may develop muscle atrophy and weakness, including a characteristic facial appearance with prominence of the cranium and ears.

Pathology: Simplistically, there are two general pathologic patterns of IBD. Historically, IBD in callitrichids has been associated with chronic colonic inflammation in which the lamina propria is expanded by lymphocytes [1, 4, 60, 85, 86] . While most associated with tamarins [1, 60] , this has also been shown to commonly affect adult common marmosets [1, 2, 4] . Other reports discuss a chronic lymphocytic enteritis (CLE) centered on the small intestine ( Fig. 13.4) . Histologically, the lamina propria of the jejunum is expanded by lymphocytes and villi are blunted [2, 41, 86, 87] .

A specific entity of IBD has been recognized in some common marmoset colonies characterized by a CLE accompanied by progressive weight loss. In this form of IBD lymphocytic infiltrates comprising CD3/CD56positive cells efface the normal architecture resulting in fusion and blunting of villous tips accompanied by crypt hyperplasia. Intense lymphocytic infiltration of the epithelium is observed consistent with an immune-mediated response to environmental or potentially host antigens [41] . Treatment with prednisone and dietary withdrawal of gluten had no effect on the clinical disease. Elimination of Giardia within the colony was associated with a marked reduction in incidence of the disease, suggesting that environmental triggers may initiate a self-perpetuating immunemediated disease.

Differential diagnosis: Despite the high prevalence of the disease and associated morbidity and mortality, the definitive cause of IBD/CLE has yet to be identified. Weight loss and wasting are nonspecific signs in marmosets and may be associated with a number of clinical entities. These findings have been associated with parasitic infection [36,88e90] , gluten sensitivity [91] , dietary protein deficiency [92, 93] , vitamin E deficiency [23] , stress, and gliadin hypersensitivity [94, 95] . In one survey of zoos, no fewer than 10 causes were proposed by survey respondents [96] . In some cases, subsequent investigations have contradicted previous assertions [97] .

As noted earlier, wild marmosets obtain a large percentage of their calories from tree exudates and neither this method of foraging nor the nutritional content of the exudate are exactly recapitulated in current marmoset diets. Additional investigations into dietary factors would be worthwhile. Recent reports of gluten sensitivity including elevations in anti-Gliadin antibodies and positive response to food trials eliminating gluten indicate that dietary factors, specifically incorporation of cereals into the diet, may play a role in the development of IBD [91, 94, 95] . Furthermore, in one 

experiment, wild-caught Saguinus sp. monkeys were biopsied at baseline then placed in a standard cage and fed a commercial diet. They developed characteristic colonic inflammation during the course of captivity, which would seem to implicate food and/or stress [98] .

Diagnosis: Regardless of the cause, IBD poses a unique threat to captive marmoset colonies and represents a significant cause of mortality [99] . Diagnosis is often made through identification of clinical signs but gut biopsies can also prove useful. Recently, calprotectin and matrix metalloproteinase 9 have been identified as possible biomarkers of disease in marmosets [100, 101] . Additionally, hypoalbuminemia (<3.5 g/ dL) and weight loss (<325 g) together are negatively correlated with outcome [102] .

Prevention and control: Treatment should be supportive. Some success has also been reported in treating animals with glucocorticoids. Due to the possible side effects of this and effects on research, long-term glucocorticoid therapy may not be possible in many situations but could be considered for individual cases [103] . Elimination of other causative factors such as parasitic infections should be pursued and animals should be fed a nutritious and balanced diet formulated for their species.

While IBD is a major source of mortality in animals <6 years of age, amyloidosis is more common in older animals [99] and in one survey affected 17% of animals overall. Amyloid was identified as AA or reactive amyloid that originates from the N-terminal fragment of the serum amyloid A (SAA) protein [104] . Animals with reactive amyloidosis tend to be older (6.75 years of age) compared with animals that die of other causes and present with weight loss with or without diarrhea and hepatosplenomegaly. Organs affected include, in decreasing order of frequency, the small intestine, liver (Fig. 13.5) , adrenal glands, kidney, stomach, colon, and spleen. In some animals, diagnosis can be confirmed through use of rectal biopsy or percutaneous liver biopsy.

Bacterial liver disease in marmosets is uncommon but has been reported both naturally and experimentally. Histologically, amyloid is identified as extracellular amorphous eosinophilic material, which expands hepatic sinusoids and/or the lamina propria of the small or large intestine. Hematoxylin and eosin, 400x. Images courtesy of Keith Mansfield, Novartis Institute for Biomedical Research and Charles Bailey, Johns Hopkins University.

Etiology: Clostridium piliforme is a rod-shaped, flagellated, anaerobic, spore-forming bacillus that is the causative agent of Tyzzer's disease. Tyzzer's disease can infect a wide range of laboratory animals and has been reported in both marmosets and tamarins.

Clinical signs: Animals appear to be most susceptible at an early age and may die suddenly without premonitory clinical signs.

Pathology: Affected animals have classic lesions of Tyzzer's disease including dissemination of bacteria to heart, liver, and/or GI tract with resultant multifocal hemorrhagic necrosis in these locations [105, 106] .

Diagnosis: Unfortunately, antemortem diagnosis is difficult because the organisms do not grow in culture.

Prevention and control: Treatment has not been reported but is often unrewarding in other species. Tetracyclines may be attempted.

Etiology: Francisella tularensis, the causative agent of tularemia, has been described as both a natural and experimental infection [107e109].

Clinical signs: Clinical signs of infection may include lethargy, ataxia, and fever, but animals may also present more acutely or die suddenly. Following experimental aerosol exposure, animals generally succumbed within 1 week of infection.

Pathology: At necropsy, animals will have multifocal hepatic necrosis, necrotizing enteritis, bronchopneumonia, lymphadenitis, and splenitis, which are consistent with disease in other species.

Diagnosis: In suspected cases, serology may be beneficial to help diagnose the disease but necropsy and histopathology may be beneficial as well.

Prevention and control: Limiting contact of free-ranging marmosets to possible hosts such as rodents and other small mammals should limit spread of this disease.

Leptospira borgpetersenii has rarely been reported in Wied's marmosets and presumably could infect common marmosets as well. Expected clinical signs include diarrhea, weight loss, and jaundice, and bloodwork shows hyperbilirubinemia. Diagnosis can be confirmed through serology or at necropsy where animals will have renal and/or hepatic lesions. Leptospiral organisms may be noted with a silver stain or immunohistochemistry [110] .

Other potential pathogens include Yersinia enterocolitica, which causes miliary hepatic necrosis [53] , and Burkholderia mallei (glanders), which induces hepatic necrosis when introduced experimentally [111] .

As in the stomach and intestines, parasitic disease of the liver and gallbladder are rare in marmosets. The most common parasites are Platynosomum sp. and Toxoplasma gondii. While modern pest control measures and use of antiparasitic agents have reduced the likelihood of transmission by reducing contact with host species, infection is still possible; and one should be familiar with these agents as potential causes of clinical disease.

Platynosomum sp.

Etiology: The trematode flukes Platynosomum amazonensis, Platynosomum marmoseti, and Athesmia foxi may infect callitrichids including common marmosets [61, 90, 112, 113] .

Clinical signs: These parasites reside in the gallbladder and bile ducts, and clinical signs manifest primarily as weight loss. With a severe infection, one would expect to see hyperbilirubinemia and icterus.

Pathology: At necropsy, there is dilation of intrahepatic bile ducts, thickening of the gallbladder, and black discoloration of the bile. Flukes may be grossly visible as small black foreign bodies within the gallbladder or bile ducts. Histologically flukes are associated with portal fibrosis and significant cholestasis.

Prevention and control: This parasite can be treated with 60 mg/kg praziquantel, and care should be taken to control cat, snail, lizard, and toad populations, which can all serve as intermediate or paratenic hosts [90] .

Etiology: Toxoplasma gondii has also been reported in callitrichids and other New World monkeys [114e117] .

Clinical Signs: Experimental infection results in rapid death between 1 and 12 days post infection. Clinically, one would expect to see fever, along with elevations in liver enzymes associated with infection. The organism also commonly infects the kidneys, muscles, heart, lymph nodes, spleen, and lung, which can result in kidney failure, pneumonia, and myocarditis, which may be presenting complaints as well.

Pathology: Infection is prominent in the liver where it is associated with multifocal to coalescing inflammation and necrosis, which can be extensive.

Diagnosis: Diagnosis may be made from blood smears, though organisms may be present in blood only late in the disease. Due to the acute nature of the disease, treatment in marmosets has not been described but includes trimethoprimesulfamethoxazole or pyrimethamine þ sulfadiazine þ leucovorin in other species.

Etiology: Lymphocytic choriomeningitis virus (LCMV) is a member of the family Arenaviridae. Disease has been reported in a variety of species, and marmosets are highly susceptible to infection. Originally termed callitrichid hepatitis virus, it was later discovered that this transmissible agent is actually a variant of LCMV [118e121] .

Clinical signs: Marmosets are most commonly exposed following ingestion of infected rodents, and disease has been associated with the feeding of newborn mice to marmosets [19] , though wild mice may also serve as a reservoir [122] . Approximately 1e2 weeks following exposure, animals may present as weak and anorexic, jaundiced, or with unexplained hemorrhage. Sudden death without identification of premonitory clinical signs may also occur. Animals often have elevated liver enzymes.

Pathology: The most common and prominent pathologic finding is multifocal hepatic necrosis with Councilman (acidophilic) bodies and mononuclear inflammation. Animals may also have necrosis in the spleen, lymph nodes, adrenal cortex, and intestinal tract.

Diagnosis: Diagnosis can be made through serology or, more likely, based on characteristic histopathologic findings and use of immunohistochemistry or other molecular techniques to identify infection.

Prevention and control: Care should be taken to avoid infection by controlling the wild rodent population and avoiding the use of mice as food enrichment for marmosets. If disease is suspected, animals should be isolated to avoid spread within the colony, and euthanasia of infected animals and contacts should be considered. Thorough sanitation of the environment is required, and an evaluation of pest control measures should be undertaken to reduce or eliminate the rodent population.

Hepatitis C is a cause of significant morbidity in human populations and is responsible for hundreds of thousands of human deaths annually. Marmosets are susceptible to infection with GB virus B, the most closely related virus to hepatitis C virus, and therefore serve as a useful animal model of hepatitis C [123] .

Infected animals develop hepatic pathology similar to that seen in humans with hepatitis C, which include multifocal nonsuppurative hepatitis, formation of lymphocytic nodules, and piecemeal necrosis, which progress to portal fibrosis over the course of approximately 5e6 months. Steatosis may also be present. Progression occurs despite clearance of the virus from plasma [124, 125] . These changes are associated with concomitant changes in plasma insulin and glucagon levels consistent with metabolic dysregulation [126] . While acute experimental infection is not associated with notable clinical signs, one may see an elevation in serum ALT, ALP, and/or LDH clinically.

Etiology: Marmosets are susceptible to yellow fever, and the virus may occur naturally in wild populations [127e129] . Experimental inoculation of Callithrix jacchus may cause disease depending on the specific strain used for infection. In an experiment in which multiple strains were inoculated into common marmosets, the Africanorigin Asibi strain resulted in low mortality, whereas South American strains such as O.C., J.Z., J.F., Martinez, and A.C. Bolivian strains resulted in high mortality with an average survival time of 5e9 days post infection [79, 128] .

Clinical signs: Clinically one would expect to see weakness, lethargy, and potentially icterus. Depending on the strain, liver enzymes may be elevated and clotting times may be abnormally long.

Pathology: Gross pathologic changes are somewhat dependent on strain but generally include icterus, splenomegaly, and congestion or hemorrhage of the stomach. Histologically, there is steatosis and multifocal random hepatic necrosis, which may be associated with intranuclear viral inclusion bodies in hepatocytes. Councilman bodies may also be present.

Prevention and control: Unless a facility was importing primates from South America, introduction of this agent into a facility would not be expected. However, as global temperatures rise, the endemic range of mosquitoes harboring this virus (Aedes aegypti) could change and lead to an enhanced probability of transmission in some captive settings. As such, measures to control the mosquito population and to limit contact with other infected animals or humans should be implemented to prevent transmission of this virus.

In addition to these important viruses, marmosets may also be infected experimentally with other pathogens that result in hepatic disease.

Not surprisingly, marmosets are susceptible to Lassa virus, the causative agent of Lassa fever. This virus is an arenavirus closely related to LCMV and results in lesions similar to those seen in this important human disease, including hepatocellular necrosis with lesions similar to those described for LCMV above [130] .

Marmosets are also experimentally susceptible to Junin virus, the causative agent of Argentine hemorrhagic fever, another arenavirus. Animals present with anorexia, weight loss, and/or neurologic symptoms. Anemia develops over the course of 1e3 weeks, and leukopenia and thrombocytopenia may also be evident [131, 132] . Gross lesions include multifocal hemorrhage in the mouth, pharynx, and esophagus. Histologically, there is multifocal hepatic necrosis along with meningoencephalitis, interstitial pneumonia, and lymphocytic depletion [133] .

Marmosets have been used as models to study Marburg virus and Ebola virus. Infection with both results in weight loss, anorexia, fever, and depression. Animals may show hemorrhage from mucosal surfaces and dyspnea. Animals generally succumb to disease within 7e10 days. Pathologic findings are typical of filovirus infection and include hepatocellular necrosis along with a host of other pathologic changes such as splenic necrosis, lymphoid necrosis, and disseminated intravascular coagulation [134e136] .

Other species of callitrichids, including several species of Saguinus, have been experimentally infected with hepatitis A virus. Animals developed elevated liver enzymes, histopathologic changes in the liver consistent with hepatitis A virus infection, and developed circulating antibody titers. The incubation period was approximately 3e5 weeks [137] .

Marmosets commonly develop nonalcoholic fatty liver disease (NAFLD), which sometimes progresses to nonalcoholic steatohepatitis (NASH). In one report, hepatomegaly was present in 18% of marmosets and was identifiable on physical examination and radiographs [138] . NAFLD and NASH are important human diseases, and marmosets may serve as a useful animal model for these conditions.

Marmosets with fatty liver disease are more likely to have high total body weight and body condition scores and are generally more likely to be female than male. Bloodwork findings are reported to include an elevated GGT and triglycerides.

At necropsy, animals will have markedly enlarged livers which, in severe cases, can extend down to the pelvic region. Histologically, there can be both macrovesicular and microvesicular steatosis, which is associated in some cases with inflammation and fibrosis ( Fig. 13.6 ). Management of NAFLD/NASH is not discussed in the literature, but dietary intervention may prove worthwhile (Table 13 .1). FIGURE 13.6 Marmosets develop fatty liver, which sometimes progresses to nonalcoholic steatohepatitis. Fatty liver is often characterized histologically as macrovesicular steatosis in which hepatocytes contain large, clear, intracytoplasmic fatty inclusions on HE staining (top left). These vacuoles stain with oil red O indicating they are fat (top right). Sometimes, marmosets progress toward nonalcoholic steatohepatitis (NASH), which is characterized by interstitial fibrosis and a ballooning degeneration (Trichrome stain, bottom left). Some of these marmosets also develop diabetes, and histologically animals have large pancreatic islets (bottom right).

Etiology: Though far less common than it once was, the nematode Trichospirura leptostoma causes chronic pancreatitis [139, 140] .

Clinical signs: Infected animals have clinical signs including weight loss, muscle wasting, and anemia. Though not reported, one would expect elevated amylase on serum chemistry. Amylase >800 IU/L should raise the level of suspicion for pancreatitis [141] .

Pathology: The parasite infects the pancreatic ducts where it is associated with moderate-to-severe ductular fibrosis and blockage of the ducts. Fibrosis expands into exocrine pancreatic tissue.

Diagnosis: Parasite eggs can be identified in feces using formalin sedimentation.

Prevention and control: Treatment of suspected cases is best accomplished with 50 mg/kg fenbendazole for 14 days. Ivermectin at 200e500 mg/kg may also successfully kill the parasite but is less effective [139] .

The German cockroach (Blattella germanica) and brown-banded cockroach (Supella longipalpa) are intermediate hosts. Initial reports of infection in wildcaught marmosets suggested that this parasite did not cause high morbidity, whereas later reports of laboratory samples indicated a higher incidence of disease. One possible explanation for this dichotomy is that some animals experience a rapid infection due to cockroach infestation, which overloads the body's ability to manage the infection. As such, pest control measures should be implemented to prevent infestation and reduce the risk of transmission to marmoset colonies.

Successfully treated animals may show remarkable weight gain and improvement in clinical signs after treatment. The clinical signs together with marked weight gain post treatment have led some to speculate about this parasite's relationship to MWS [88, 89] . While it is clear that the parasite causes wasting and characteristic clinical signs that are readily reversible with treatment, it is unlikely that it is the cause of MWS which, as noted above, is associated with chronic inflammation of the intestines and is still present in colonies despite eradication of this agent.

Marmosets can develop insulin-resistant diabetes, and this condition is partially dependent on the diet they are fed. Marmosets fed a common, commercially available diet, which has glucose as a main ingredient (32% added glucose), readily develop obesity and prolonged hyperglycemia. Animals fed a high-fat diet also developed hyperglycemia and obesity, though these changes were both less dramatic and delayed by w6 months [142] . Animals in both groups developed vascular pathology consistent with atherosclerosis and islet hyperplasia consistent with insulin resistance. As noted above, diet is critically important in maintaining healthy marmosets. While palatability is obviously important, the selected diet should be well balanced without unnecessary added sugar.

Animals with insulin resistance or overt diabetes may present with clinical signs including polyuria/polydipsia, anorexia, vomiting, and weakness [143] . Animals may be obese but begin to lose weight as the disease progresses. Laboratory findings are characteristic of diabetes in other species and include hyperglycemia, hypertriglyceridemia, and glycosuria. Glycosylated hemoglobin (HgbA1c) is also a useful diagnostic tool and is elevated in animals with persistent hyperglycemia. Animals that are euthanized with diabetes will initially show islet hyperplasia at necropsy (Fig. 13.5 ), but this may progress to islet atrophy as disease progresses.

Dietary management is possible to delay the progression of disease but may prove unrewarding in the long term. Anecdotally, oral hypoglycemic agents such as metformin may be used to treat animals with some success. Insulin therapy could be considered on a case by case basis but is likely not feasible in a research setting due to the intensive care and frequent injections that are required and secondary physiologic changes that would alter the animal's usefulness experimentally.

In addition to developing diabetes naturally, marmosets should also be considered as an animal model for diabetes given the readiness with which they develop insulin resistance and hyperglycemia following a change in diet. Interestingly, marmosets are resistant to diabetes induction with streptozotocin due to altered expression of the GLUT2 glucose transporter in their islets limiting the usefulness of this specific model [144] . However, their islet anatomy and structure are similar to those of humans, making them a potentially useful animal model for an important human disease [145, 146] .

Effect of various biological factors on spontaneous marmoset and tamarin colitis. A retrospective histopathologic study

Spontaneous pathology of the common marmoset (Callithrix jacchus) and tamarins (Saguinus oedipus, Saguinus mystax)

Diseases of the Callitrichidae: a review

Chronic colitis in common marmosets (Callithrix jacchus) and cotton-top tamarins (Saquinus oedipus)

Studies on the dentition of the marmoset

A survey of the pathology of marmosets (Callithrix jacchus) under experiment

Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet

The functional morphology of the anterior masticatory apparatus in treegouging marmosets (Cebidae, Primates)

Gummivory and gut morphology in two sympatric callitrichids (Callithrix emiliae and Saguinus fuscicollis weddelli) from western Brazilian Amazonia

Vegetable exudates as food for Callithrix spp. (Callitrichidae): exploratory patterns

Digestion in the common marmoset (Callithrix jacchus), a gummivore-frugivore

The mechanism of end-organ resistance to 1 alpha,25-dihydroxycholecalciferol in the common marmoset

Radiographic anatomy of the thorax and abdomen of the common marmoset (Callithrix jacchus)

Transcutaneous ultrasonography of the abdomen in the normal common marmoset (Callithrix jacchus)

A comparison of tooth eruption patterns between two colonies of young marmosets (Callithrix jacchus)

Dental development in the cotton ear marmoset (Callithrix jacchus)

Canine tooth root infection as a cause of facial abscess in the common marmoset (Callithrix jacchus)

Fatal Herpes simplex infection in a group of common marmosets (Callithrix jacchus)

Spontaneous herpes simplex virus infection in common marmosets (Callithrix jacchus)

Herpesvirus tamarinus and its relation to herpes simplex virus

Veterinary pathology

Overt herpes-T infection in squirrel monkeys (Saimiri sciureus)

A survey of the pathology of marmosets (Callithrix jacchus) derived from a marmoset breeding unit

Bacterial and mycoplasma flora of a laboratory colony of the common marmoset (Callithrix jacchus)

Spontaneous neoplasms of the marmoset (Callithrix jacchus). Oral and nasopharyngeal squamous cell carcinomas

Studies on the biology of the periodontium of marmosets. VII. The effect of vitamin C deficiency on the marmoset periodontium

Ascorbic acid requirement and assessment of ascorbate status in the common marmoset (Callithrix jacchus)

Eruption gingivitis associated with scorbutism in macaques

Vitamin C deficiency in captive nonhuman primates fed commercial primate diet

Studies on the biology of the periodontium of marmosets. XI. Histopathologic manifestations of spontaneous and induced vitamin A deficiency in the oral structures of adult marmosets

Studies on the biology of the periodontium of marmosets: 8. The effect of folic acid deficiency on the marmoset oral mucosa

Studies on the biology of the periodontium of marmosets. XIII. Histopathology of niacin deficiency stomatitis in the marmoset

Personal communication: Mejia A. Cleft palate in marmosets

Cleft palate in a marmoset: report of a case

Congenital malformations in a common marmoset (Callithrix jacchus) similar to human 13-trisomy syndrome

Treatment of giardiasis in common marmosets (Callithrix jacchus) with tinidazole

An outbreak of shigellosis in laboratory marmosets and tamarins (Family: Callithricidae)

Molecular serotyping of Escherichia coli O26:H11

Enteropathogenic Escherichia coli and ulcerative colitis in cotton-top tamarins (Saguinus oedipus)

Hemorrhagic typhlocolitis associated with attaching and effacing Escherichia coli in common marmosets

Clinical care and diseases of the common marmoset (Callithrix jacchus)

Septicemia and peritonitis in a colony of common marmosets (Callithrix jacchus) secondary to Klebsiella pneumoniae infection

Klebsiella pneumoniae infection in a New World nonhuman primate center

Identification of Helicobacter sp. in gastric mucosa from captive marmosets (Callithrix sp

Isolation and characterization of a novel Helicobacter species, Helicobacter jaachi sp. nov., from common marmosets (Callithrix jaachus)

Helicobacter callitrichis sp. nov., a novel Helicobacter species isolated from the feces of the common marmoset (Callithrix jacchus)

Acute gastric dilatation in common marmosets (Callithrix jacchus)

A case of nontraumatic gas gangrene in a common marmoset (Callithrix jacchus)

The comparative pathology of Clostridium difficile-associated disease

Five spontaneous deaths associated with Clostridium difficile in a colony of cotton-top tamarins (Saguinus oedipus)

Antibiotic associated pseudomembranous enterocolitis in new world primates (abstract)

Yersiniosis in zoo marmosets (Callithrix jacchus) caused by Yersinia enterocolitica 4/O:3

Yersinia enterocolitica infections in non-human primates

Colonization with nontuberculous mycobacteria is associated with positive tuberculin skin test reactions in the common marmoset (Callithrix jacchus)

Survey of Cryptosporidium and Giardia spp. in a captive population of common marmosets

Apicomplexa: eimeriidae) in the primates and the scandentia

Biology of Isospora spp. from humans, nonhuman primates, and domestic animals

Endogenous development of Isospora arctopitheci Rodham, 1933 in the marmoset Saguinus geoffroy

An analysis of the association of gastroenteric lesions with chronic wasting syndrome of marmosets

Spontaneous infectious diseases of marmosets

Successful treatment of cryptosporidiosis in 2 common marmosets (Callithrix jacchus) by using paromomycin

An epizootic of measles in a marmoset colony

Fatal measles infection in marmosets pathogenesis and prophylaxis

A paramyxovirus causing fatal gastroenterocolitis in marmoset monkeys

Experimental infection of Callithrix Jacchus marmosets with herpesvirus ateles, herpesvirus saimiri, and Epstein Barr virus

Latent infection and malignant lymphoma in marmosets (Callithrix jacchus) after infection with two oncogenic Herpesviruses from primates

Herpesviruses saimiri and atelesetheir role in malignant lymphomas of monkeys

Overview of viral oncology studies in Saguinus and Callithrix species

Susceptibility of common marmosets (Callithrix jacchus) to oncogenic and attenuated strains of Herpesvirus saimiri

Susceptibility of common marmosets (Callithrix jacchus) to oncogenic and attenuated strains of herpesvirus saimiri

Herpesvirus saimiri: protective effect of attenuated strain against lymphoma induction

Persistent Epstein-Barr virus infection in the common marmoset (Callithrix jacchus)

Hematologic and immunologic responses in common marmosets (Callithrix jacchus) infected with Plasmodium knowlesi and Epstein-Barr virus

An Epstein-Barr-related herpesvirus from marmoset lymphomas

Fatal lymphoproliferative disease associated with a novel gammaherpesvirus in a captive population of common marmosets

Complete genomic sequence of an Epstein-Barr virus-related herpesvirus naturally infecting a new world primate: a defining point in the evolution of oncogenic lymphocryptoviruses

Pneumonitis and multiorgan system disease in common marmosets (Callithrix jacchus) infected with the severe acute respiratory syndrome-associated coronavirus

The susceptibility of marmosets to yellow fever virus

Etiology of yellow fever: III. Symptomatology and pathological findings in animals experimentally infected

Gastrointestinal tumors observed in nonhuman primates at the German primate center

Adenocarcinoma of the small intestine in a common marmoset (Callithrix jacchus)

Small intestinal adenocarcinoma in common marmosets (Callithrix jacchus)

Inflammatory fibroid polyp in the duodenum of a common marmoset (Callithrix jacchus)

Clinical pathologic changes in two marmosets with wasting syndrome

Spontaneous lesions detected in the common cotton-eared marmosets (Callithrix jacchus)

Aging phenotypes of common marmosets (Callithrix jacchus)

The parasite Trichospirura leptostoma associated with wasting disease in a colony of common marmosets, Callithrix jacchus

Trichospirura leptostoma: a possible cause of wasting disease in the marmoset

Histopathology findings in common marmosets (Callithrix jacchus Linnaeus, 1758) with chronic weight loss associated with bile tract obstruction by infestation with Platynosomum (Loos, 1907)

The influence of gluten on clinical and immunological status of common marmosets (Callithrix jacchus)

Chronic tubulointerstitial nephritis and wasting disease in marmosets (Callithrix jacchus)

Dietary habits relating to 'wasting marmoset syndrome' (WMS)

Callitrichid nutrition and food sensitivity

IgA-gliadin antibodies, IgA-containing circulating immune complexes, and IgA glomerular deposits in wasting marmoset syndrome

Results of a preliminary survey into wasting marmoset syndrome in callitrichid collections

Susceptibility of tamarin (Saguinus labiatus) red blood cell membrane lipids to oxidative stress: implications for wasting marmoset syndrome

The marmoset as a model of aging and age-related diseases

Detection of calprotectin and apoptotic activity in the colon of marmosets with chronic diarrhea

Serum matrix metalloproteinase 9 (MMP9) as a biochemical marker for wasting marmoset syndrome

Serum albumin and body weight as biomarkers for the antemortem identification of bone and gastrointestinal disease in the common marmoset

The use of glucocorticoids in marmoset wasting syndrome

Systemic AA amyloidosis in the common marmoset

Naturally occurring Tyzzer's disease in cotton-top tamarins (Saguinus oedipus)

Spontaneous Tyzzer's disease with the central nerve involvement in a newborn common marmoset

Characterization of lethal inhalational infection with Francisella tularensis in the common marmoset (Callithrix jacchus)

Establishment of lethal inhalational infection with Francisella tularensis (tularaemia) in the common marmoset (Callithrix jacchus)

Re-emergence of Francisella tularensis in Germany: fatal tularaemia in a colony of semi-free-living marmosets (Callithrix jacchus)

Leptospirosis in Wied's marmosets (Callithrix kuhlii)

Use of the common marmoset to study Burkholderia mallei infection

Two new species of Platynosomum (Trematoda: Dicrocoeliidae) from South American monkeys

Sobre o parasitismo por Primasubulura jacchi em Callithrix penicillata (Primates, Callitrichidae)

Spontaneous acute toxoplasmosis in a marmoset monkey

Susceptibility of the marmoset, Marikina geoffroyi, and the night monkey, Aotus zonalis, to experimental infection with Toxoplasma

Pathology of toxoplasmosis in captive new world primates

Sero-epidemiological survey for brucellosis, leptospirosis, and toxoplasmosis in freeranging Alouatta caraya and Callithrix penicillata from Sao Paulo State

Pathology and immunohistochemistry of callitrichid hepatitis, an emerging disease of captive New World primates caused by lymphocytic choriomeningitis virus

A common-source outbreak of callitrichid hepatitis in captive tamarins and marmosets

Callitrichid hepatitis: epizootiology of a fatal hepatitis in zoo tamarins and marmosets

Isolation of an arenavirus from a marmoset with callitrichid hepatitis and its serologic association with disease

First outbreak of callitrichid hepatitis in Germany: genetic characterization of the causative lymphocytic choriomeningitis virus strains

Development of a GB virus B marmoset model and its validation with a novel series of hepatitis C virus NS3 protease inhibitors

GB virus B infection of the common marmoset (Callithrix jacchus) and associated liver pathology

Acute liver damage associated with innate immune activation in a small nonhuman primate model of Hepacivirus infection

Metabolic dysregulation in Hepacivirus infection of common marmosets (Callithrix jacchus)

Surveillance for sylvan yellow fever activity in Panama (1957e1961)

Susceptibility of marmosets to different strains of yellow fever virus

The isolation of yellow fever virus from wild-caught marmosets

Lassa virus infection in experimentally infected marmosets: liver pathology and immunophenotypic alterations in target tissues

Junin virus infection of Calithrix jacchus: haematological findings

Argentine hemorrhagic fever: a primate model

Junin virus infection of Callithrix jacchus: pathologic features

A small nonhuman primate model for filovirus-induced disease

Experimental respiratory Marburg virus haemorrhagic fever infection in the common marmoset (Callithrix jacchus)

Experimental respiratory infection of marmosets (Callithrix jacchus) with Ebola virus Kikwit

Experimental infection of marmosets with hepatitis A virus

The common marmoset as a model for the study of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis

Diagnosis and treatment of Trichospirura leptostoma infection in common marmosets

Trichospirura leptostoma gen. et sp. n. (Nematoda: Thelazioidea) from the pancreatic ducts of the white-eared marmoset Callithrix jacchus

Serum amylase values in callitrichids

Differential contribution of dietary fat and monosaccharide to metabolic syndrome in the common marmoset (Callithrix jacchus)

Islet hyperplasia in callitrichids

Differential expression of GLUT2 in pancreatic islets and kidneys of New and Old World nonhuman primates

Ultrastructural analysis, zinc transporters, glucose transporters and hormones expression in New world primate (Callithrix jacchus) and human pancreatic islets

Islet microarchitecture and glucose transporter expression of the pancreas of the marmoset monkey display similarities to the human