Authors: Valverde Celia R., Christe Kari L.
Categories: Article
Source: The Laboratory Primate
A high quality radiograph requires optimal radiographic density, adequate contrast, minimal patient motion and proper patient positioning (Owens, 1999). High quality radiographs must be obtained for accurate interpretation and assessment. A radiograph exposure technique chart is essential for consistent high-quality radiograph production. Most poor quality radiographs are due to operator error or inadequate techniques (Ewers, 2000; Stender, 1990). Since radiograph exposure technique charts are based on anatomic thickness (in centimeters), formulating a chart for small primates is relatively easy. As thickness decreases it becomes easier to visualize the different densities within that thickness (Ferron, 1967). However, as mass increases radiograph exposure technique charts must be tailored precisely to the anatomical study (Ferron, 1967). In addition, short exposure times (1/60 or 1/120 seconds), fast film screen systems and effective patient restraint, eliminate most motion artifacts. Nonhuman primates require either physical or chemical restraint for proper patient positioning. Unfortunately, this restraint may also alter the radiographic technique or quality.
The thoracic cavity in the rhesus monkey extends from the thoracic inlet to the 14th thoracolumbar segment dorsally and just caudal to the 7th sternebrae ventrally (Silverman and Morgan, 1980a). The adult rhesus macaque thorax is wedge-shaped, deep sagitally, and broader dorsally than ventrally. The macaque's thorax is more elongated craniocaudally than the dog's thorax.
The costodiaphragmatic angle is sharp; the right costodiaphragmatic angle is sometimes located more caudally than the left (Silverman and Morgan, 1980a).
The mediastinum is complete. The thymus is bilobed in the macaque; therefore, the thymic “sail sign” may be visualized on both sides of the mediastinum in young animals. The mediastinum in the adult macaque is concave bilaterally on the frontal radiograph and is similar to the cat's mediastinum. Irregularities of the paravertebral mediastinal stripe on the frontal projections are considered an abnormal finding and are usually caused by mediastinal lymphadenopathy (Silverman and Morgan, 1980a).
All routine thoracic examinations of nonhuman primates should be performed on sedated patients, restrained in the upright position by an acceptable restraint device. Radiograph positioners have been well described in the literature (Ferron, 1966; Silverman and Morgan, 1980a; Silverman et al., 1983).
A routine thoracic study should include erect lateral and ventrodorsal views. The relatively greater depth of the costodiaphragmatic recesses in macaques, as compared with those in human beings and dogs, increases the importance of the lateral projection. The caudal extent of the costodiaphragmatic recesses cannot be fully evaluated on the frontal projections due to the superimposition of the cranial abdominal organs.
The trachea of the adult rhesus monkey is flattened transversely and is approximately 9.5–11 cm long and 0.9 cm wide. There are approximately 27 cartilaginous C-shaped tracheal rings. The dorsal portion of the trachea is incomplete and is formed by an elastic membrane. The right bronchus extends in a near straight line from the trachea, whereas the left bronchus comes off at a distinct angle (Silverman and Morgan, 1980a).
Dorsal tracheal deviation on the lateral projections and irregularity of the paravertebral mediastinal stripe on the frontal projections are the most accurate signs of hilar lymphadenopathy (Silverman and Morgan, 1980a).
The macaque lung most closely resembles the dog lung in that they both have a thick pleura, minimal interlobular septation, and similar arrangement of vessels. Pulmonary lobation in the rhesus monkey is similar to that in the dog and cat. The left lung is divided into two cranial and caudal. The cranial lobe is subdivided into cranial and caudal segments. The right lung is divided into four cranial, middle, caudal, and accessory. Bronchi in macaque lungs are developed to at least three generations before the first bronchiole is reached. The bronchi open into short (2–3 mm) terminal bronchioles that are only developed to a single generation and lined by pseudostratified columnar epithelium.
Frequently there is no intermediate bronchiole in rhesus macaque. Other macaque species have terminal bronchioles that are developed to 3–4 generations and lined by simple cuboidal epithelium (Silverman and Morgan, 1980a).
The pulmonary parenchyma of macaques has an accentuation of the interstitial densities resulting in diminution of the distinctiveness of pulmonary bronchovascular markings. It is important not to overemphasize the significance of the interstitial pattern and diagnose interstitial pulmonary disease. The accentuation of the interstitial pattern may reflect a normal pulmonary parenchyma of nonhuman primates, or may be secondary to pulmonary acariasis (Pneumonyssus siminicola) (Silverman and Morgan, 1980a).
Angulating the x-ray beam 15 degrees caudally, for the ventrodorsal projection, can enhance evaluation of the caudal portions of the lungs.
Artifactual densities or normal densities can be confused with thoracic pathology, e.g. obliteration of the cardiac silhouette by pericardial or sternal fat deposits and the presence of nipple shadows resembling “coin lesions.”
Planimetry is a radiographic technique utilized to determine the total lung capacity in nonhuman primates. The technique has been described in anesthetized baboons (Harris et al., 1971). The authors reported an excellent correlation between total lung capacity and radiographic lung area. This correlation was better for young than aged baboons (Bennett et al., 1995).
Air sacs are not found in all species of nonhuman primates. When present, the air sac acts as a resonator modifying sound (Hilloowala, 1976). New World primates such as howler monkeys (Allouatta sp), titi (Callicebus sp) and owl monkeys (Aotus sp) have a varying degree of laryngeal air sac development. Old World primates have cervical laryngeal air sacs that communicate with the laryngeal lumen via a central ostium at the base of the epiglottis (Lowenstine, 2003).
Great apes have well-developed laryngeal air sacs which are large in the siamang, gibbons, orangutans, and gorillas. These air sacs have paired openings from the lateral saccules and extend along the ventral neck, beneath the clavicles and into the axilla. In orangutans and gorillas, the apparatus extends along the thoracic wall. Air sacculitis is often an extension of chronic respiratory infections. Air sacculitis due to gram negative organisms such as Pseudomonas is common, especially in orangutans. Radiographic signs may include increased soft tissue density of the cervical and intermandibular areas, thickening of the mucosa of the perilaryngeal air sacs and the presence of exudate (Baer et al., 1994).
Bronchointerstitial pneumonia is one of the major causes of morbidity and mortality in nonhuman primate species. The differential diagnosis for interstitial pneumonia is quite extensive and includes bacterial (Streptococcus sp, Staphylococcus sp, Pseudomonas aeruginosa, Klebsiella pneumoniae, Bordetella sp, Francisella tularensis, Proteus mirabilis), parasitic (Filarioides sp, Filariopsis sp), protozoal (Toxoplasma gondii, Pneumocystis carinii), fungal (Histoplasma capsulatum, Coccidiomyocoides immitis), and viral agents (measles, other paramyxoviruses, influenza viruses).
Tuberculosis is the most common disease producing mediastinal lymphadenopathy in nonhuman primates. Irregularity of the paravertebral mediastinal stripe on the frontal projections and dorsal trachea deviation on the lateral projections are the most accurate signs of hilar lymphadenopathy. In contrast to human beings, pulmonary tuberculosis in nonhuman primates rarely shows any nodular calcification. Most commonly the tubercles undergo extensive caseation necrosis. Extra-pulmonary sites of infection may not be readily apparent on radiographs. Differential diagnosis of pulmonary tuberculosis includes lung mite infestation (Pneumonyssus simicola), nocardiosis, and deep mycosis such as histoplasmosis, or coccidioidomycosis (Silverman and Morgan, 1980a).
Radiographic findings of cocciodiomycosis include the formation of numerous multiloculated cavities that arise from conducting airways and evidence of severe diffuse pulmonary parenchymal disease. Serial thoracic radiographs provide an excellent indication of the extent of infection and the progress of the disease (Converse et al., 1962; Breznock et al., 1975).
Lung mite (Pneumonyssus simicola) infestation is usually a subclinical disorder seen in virtually all wild and imported wild-caught rhesus. It may persist in subsequent generations of captive-born group housed macaques. Treatment with ivermectin can eliminate the infection, but the lesions of chronic bronchiolitis, bronchiectasis, and pigmentation may persist as an incidental finding (Lowenstine, 2003). The typical radiographic manifestation of pulmonary acariasis in rhesus macaques consists of an increased nonstructured interstitial pulmonary density, increased thickness and density of the bronchial walls, increased peribronchial density, pleural thickening, pleural adhesions, indistinct pulmonary vasculature and cavitary pulmonary lesions. Follow-up radiographs usually demonstrate minimal or no progression of the peribronchial and interstitial densities in uncomplicated cases. Pleural thickening is a prominent radiographic finding; the interlobar fissures are thickened and irregular, differing from their normal thin, smooth appearance. Pleural adhesions are common. Cavitary pulmonary disease consisting of bullae and subpleural blebs can be extensive. The most frequent complication of pulmonary acariasis is pneumothorax. Because, of the complete separation of the mediastinum of the macaque, unilateral pneumothorax occurs frequently (Silverman and Morgan, 1980a).
The cardiovascular system of most nonhuman primates is similar in anatomy and physiology to that of human beings, and the domestic dog (Bonakdarpour et al., 1967). The major mediastinal branches of the aortic arch in the macaque and dog are the brachiocephalic branch and right and left subclavian arteries. The vertebral and carotid arteries originate from the brachiocephalic trunk.
Angiography is a radiographic contrast study using iodinated contrast media and sequential radiographs to visualize the cardiovascular system (heart, arteries, and veins). With the advent of ultrasonography and color Doppler, contrast procedures to examine the cardiovascular system have been reduced to the diagnosis of the more complex congenital defects and associated conditions. Angiography, in conjunction with pressure measurements, is essential in examining cardiac lesions to determine the severity of the functional and anatomical defects.
Selective angiography is the placement of an indwelling catheter, near the suspected lesion, for delivery of a contrast media. Selective angiography requires specialized equipment (e.g. catheters, contrast material, an automated contrast injector, a rapid film recording device, and fluoroscopy). Nonselective angiography is less accurate in demonstrating lesions than selective angiography. Its use is limited, although it can be adequately performed with routine radiographic equipment (Owens, 1999).
Arterial angiography can be performed, usually through catheterization of the femoral or carotid artery through a small surgical incision (cutdown). A catheter can be advanced to the area of interest. The advancement of the catheter can be monitored using fluoroscopic technique or through serial injections of an iodinated contrast material. Lateral and ventrodorsal projections should be evaluated. The assessment of the arterial, capillary and venous phases of angiography can be performed.
Angiographic studies have been used to provide a comparison between nonhuman primate and human vascular anatomic variations and collateral pathways, such as the angiographic anatomy of the external carotid artery system in the rhesus monkey (TerBrugge et al., 1989) and the coronary artery distribution in bonnet monkeys (Macaca radiata) (Buss et al., 1982). Placental radioangiography, as a method for the study of uteroplacental blood flow, was described in the pregnant rhesus monkey (Kato et al., 1987). Clinical applications of the arterial angiogram have been described for the diagnosis of dissecting arterial aneurysm secondary to arteriosclerosis (Boorman et al., 1976), congenital arteriovenous fistula in a rhesus macaque (Rosenberg et al., 1983), and for the diagnosis of atrial septal defect in a Sumatran orangutan (Greenberg et al., 1999).
This is a major cause of morbidity and mortality in the owl monkeys (Aotus sp). A prominent feature of this condition is ventricular dilation and myocardial hypertrophy, primarily of the left ventricular chamber, left ventricular free wall and the interventricular septum. Thoracic radiographs are used as an ancillary diagnostic tool. Findings might include cardiomegaly, vascular dilation and pleural and/or pericardial effusion. Echocardiography is the imaging modality of choice. Differential diagnosis includes viral myocarditis (Cocksackie B virus, encephalomyocarditis caused by picornaviruses) and parasitic infection (Toxoplasma gondii in New World primates, particularly squirrel monkeys; Trypanosoma cruzi in Southern American monkeys) (Baer et al., 1994).
Chronic myocardial interstitial fibrosis is a common finding in many species of primates, especially great apes in which sudden cardiac death is common (Lowenstine, 2003).
Nonhuman primates are used extensively as experimental models for atherosclerosis. Atherosclerosis can be readily induced in many species. Naturally occurring atherosclerosis is seen in captive primates and is also reported in free-ranging animals, but is usually mild and limited to the formation of fatty streaks (Lowenstine, 2003). Atherosclerosis has been associated with coronary artery disease, cardiomyopathy, dissecting aortic aneurysms, and congestive heart failure.
Spontaneously occurring aortic aneurysms have been described in the gorilla and squirrel monkey (Saimiri sp), howler (Allouatta sp), capuchin (Cebus sp), patas (Erythrocebus patas), African green (Chlorocebus aethiops), spider monkeys (Atelles sp) and pygmy chimpanzee (Pan paniscus). Diagnosis of aortic aneurysm can be made on the basis of a radiographic examination, sonography, abdominal palpation and ascultation of bruits. Definitive diagnosis may require angiography or computerized tomography (Baer et al., 1994; Lowenstine, 2003).
All routine abdominal examinations of nonhuman primates should be performed on sedated or anesthetized patients. A routine abdominal study should include lateral and ventrodorsal views. A foam pad placed underneath the animal is helpful with correct positioning and comfort since, nonhuman primates have prominent sacral bones with protruding tails.
Abdominal organs are difficult to visualize on nonhuman primate abdominal radiographs. The lack of intra-abdominal fat reduces organ resolution and gastrointestinal contents obscure organ visualization. The abdomen is also the thickest part of the body and therefore, a higher kVp must be used to attain adequate radiation penetration. Moreover, motion artifact can present a major problem when imaging the gastrointestinal tract.
An esophagram is performed using positive contrast media to evaluate esophageal location and morphology. Fluoroscopy is the optimum technique for the assessment of esophageal motility and function. One should obtain lateral and ventrodorsal projections of the cervical region and thorax, and a right ventrodorsal oblique projection of the thorax. Sedation and anesthesia are not recommended because esophageal motility will be altered. Esophagrams can outline potential strictures, esophageal foreign bodies, megaesophagus, and trauma to the esophagus.
Tarsiers, New World and Old World monkeys have a flask-shaped simple stomach. The rhesus stomach is positioned lower and more horizontally than in humans, due to the shape and size of their liver (Hartman et al., 1933). The stomach structure of colobines (Colobus and Presbytis) differs from any other primate and resembles that found in ungulates, with a pseudoruminant anterior fermentation area in a large multichambered stomach. The stomach is large and sacculated, though not truly compartmentalized. The sacculations are produced by reduced longitudinal muscle bands. The size of the stomach and colon tend to be proportionally larger in folivorous nonhuman primates. These animals also tend to be larger in stature to accommodate for their sizeable gastrointestinal tract. The colobine stomach may constitute up to a quarter of the adult body weight and up to half for a semi-weaned infant. The Pongidae stomach is indistinguishable from human beings.
Gastrography is a radiographic contrast study of the stomach using negative, positive, or double contrast techniques for evaluation of gastric morphology, function and the rate of gastric emptying. If gastrointestinal perforation is suspected barium should not be used; an iodinated contrast medium should be used instead. Full strength iodinated contrast (240-300 mg Iodine/ml) should be diluted 50 with water (Wallack, 2003). Ideally, no sedation or anesthesia should be used in a functional study, although it can be used for a morphologic evaluation of the stomach.
Pneumoperitoneography can be used in combination with gastrointestinal positive contrast studies; both the mucosal and serosal surfaces are visualized (Silverman et al., 1975).
Trichobezoars are relatively common in many species of primates (Keller et al., 1982; Lapin, 1963; Mook, 2002). Trichobezoars are formed from plant fibers, hair, and mucus. Clinical signs may be subtle such as anorexia, vomiting, weight loss and occasionally the stool may contain hair.
Gastrointestinal ulceration occurs most commonly in newly captured, stressed or geriatric nonhuman primates (e.g. African Green monkeys, squirrel monkeys, macaques). Nonhuman primates on NSAID therapy are at risk of developing gastrointestinal ulcers.
Acute gastric dilation/bloating is seen almost exclusively in indoor-housed macaques and baboons, but has also been reported in callitrichids (Cicmanec, 1977). Clinical signs are enlarged abdomen differentiated from colonic distention, discomfort, distress and shock. Microcardia and a narrowed caudal vena cava are observed due to hypovolemia and decreased venous return. Death ensues unless the animal is treated immediately. The etiology is unknown though it often associated with management changes in feeding. Clostridium perfringens in the feed has also been associated with acute gastric distention (Newton et al., 1971).
Prosimians have no sigmoid flexure, taenia (bands) or haustra (saccules) in the colon. Also, the length of the cecum, relative to that of the colon and rectum, is far greater than in other primate groups. New World monkeys have no sigmoid flexure or haustra in the colon. Old World monkeys are mostly hindgut fermenters. They have a cecum but lack a vermiform appendix; the colon has taenia, haustra, and a sigmoid flexure. Hominids have a colon well developed with taenia, haustra, and a cecum with a vermiform appendix. Valvulae conventes are present in some higher primates and humans (Goldberg et al., 1982).
A UGI is a radiographic study using positive contrast media to provide functional and morphological evaluation of the small intestine. Barium sulfate suspension of 30% weight/volume provides adequate mucosal coating and contrast for radiographic visualization. Iodinated gastrointestinal contrast media should be used in animals with suspected perforation. However, ionic and nonionic iodinated media are less sensitive for the detection of mucosal lesions and may not demonstrate a perforation or a fistula. In addition, nonionic iodine contrast is hypertonic, drawing fluid into the intestinal lumen, diluting the contrast media further, and dehydrating the patient. Also, iodine has a faster transit time than barium so lateral and ventrodorsal projections should be made more frequently (usually every 10–30 minutes) until the contrast is seen in the large intestine (Owens, 1999). The transit time to the colon is variable, depending on the animal's age, temperature, problem and the type and length of anesthesia, making interpretation difficult.
This is an abdominal radiographic study, using retrograde infusion of negative contrast, positive contrast or double contrast, for the morphologic assessment of the large intestine.
Pneumocolon is used to discriminate between a normal gas filled large intestine and a gas dilated small intestine and to identify large bowel strictures and intraluminal and intramural masses.
Double contrast barium enema is used to evaluate the colonic mucosa, wall thickness or identify strictures and/or intraluminal and intramural masses.
A linear foreign body may cause the intestines to appear “plicated” on abdominal radiographs. An intestinal linear foreign body injury was reported in a cynomolgus macaque; the ulceration, perforations and septic peritonitis were attributed to the ingestion of sisal rope used for environmental enrichment (Hahn, 2000).
Intestinal perforation can occur as a result of intestinal foreign body, intestinal neoplasia or abdominal trauma.
Rocks in the cecum are common radiographic findings of nonhuman primates housed in outdoor corrals with gravel or a rocky substrate.
Enterocolitis is the most common cause of morbidity and mortality in nonhuman primate species. The differential diagnosis includes bacterial (Campylobacter sp, Salmonella sp, Shigella sp, Yersinia sp, enteropathogenic E. coli, Clostridium sp, Mycobacterium aviumintracellulare complex), parasitic (Giardia, Balantidium coli, Cryptosporidium sp, Entamoeba histolytica, Trichuris trichiura, Strongyoides, Strongyles and cestodes), fungal (Candida albicans), and viral agents (rotaviruses, coronaviruses, paramyxovirus).
Marmoset wasting syndrome is a poorly understood disease of callitrichids. The etiology is probably multifactorial, including low dietary protein and zinc content, feeding behavior, gastrointestinal tract infection and malabsorption. Clinical signs are nonspecific but include alopecia, diarrhea, chronic colitis, weight loss and anemia. It has been postulated that their dietary protein requirement is greater than that of other primates.
Megacolon of cynomolgus macaques (M. fascicularis) has been reported. Indoor-housed cynomolgus macaques appeared bloated but not in pain. Gastrointestinal signs included diarrhea, mucus in the stool, anorexia, and failure to pass stool, with repeated episodes of extreme abdominal distension and accumulation of gas and feces in abnormally enlarged colons. Intra-abdominal adhesions were noted in all animals. Most of the animals had a history of a prior obstetric surgery. Abdominal radiographs confirmed abnormal dilation and positioning of the colon. Conservative management with stool softeners was palliative; a partial colectomy was curative (Eisele et al., 1991).
Diverticulosis is commonly seen in geriatric nonhuman primates. It is most severe in the descending and sigmoid colon. Severe diverticulosis can lead to diverticulitis and ultimately rupture through the intestinal wall causing focal or generalized peritonitis.
Intestinal adenocarcinoma is the most common malignant neoplasm in rhesus macaques and a significant cause of morbidity and mortality in the geriatric population (Valverde et al., 2000). Typical presenting signs are weight loss, microcytic anemia and fecal occult blood positive. Anorexia, constipation and obstruction occur quite late in the disease course. Metastases to the liver and mesenteric lymph nodes can occur. Diagnosis is achieved by abdominal palpation, ultrasonography, contrast radiography, or exploratory laparotomy. Naturally occurring colonic adenocarcinoma is highly prevalent in the cotton-top tamarin (Saguinus oedipus) (Lowenstine, 2003).
Rectal prolapse is commonly seen in animals that are stressed or have recurrent gastroenteritis. Rectal prolapse can self-reduce or be manually reduced. Nonreducible or severely traumatized rectal prolapses require surgical resection.
The rhesus liver is primitive with a left and right lateral lobe placed dorsally, and a single large ventrally placed central lobe (Hartman and Straus, 1933). The caudal border of the liver does not extend beyond the costal arches and the caudal liver margins should be sharp.
Hepatitis The differential diagnosis for hepatitis is quite extensive and includes bacterial, viral (Hepatitis A, B, C, D, E, G, TT, Callitrichid hepatitis due to lymphocytic choriomeningitis virus in callitrichids and owl monkey, GBV-A-like flavivirus of tamarins) or parasitic (schistosomiasis, trematodiasis).
Amyloidosis appears more disseminated in Asian macaques then in African or New World nonhuman primates. Macaques are prone to systemic amyloidosis following chronic inflammatory processes (i.e., retroviral infections or chronically implanted devices (Lowenstine, 2003). Systemic amyloidosis usually involves the liver and spleen and may or may not include the gastrointestinal tract or kidneys. Animals with severe amyloidosis are usually debilitated and cachectic with sparse, dry hair coats and marked hepatomegaly. Animals with disseminated amyloidosis can live for extended periods of time without severe clinical problems but the condition is irreversible.
Hepatic lipidosis/fatal fasting syndrome has been reported in four macaque species (M. arctoides, M. fascicularis, M. mulatta, and M. radiate) and one African Green monkey (Chlorocebus atheiops) (Christe and Valverde, 1999). The disease is characterized by rapid weight loss (0.1 kg/day) in obese animals, with anorexia and lethargy often being the only presenting clinical signs. The liver grossly appears enlarged with rounded edges, pale and friable. The kidneys may also be enlarged, pale and soft.
The macaque pancreas is located just behind the stomach along the transverse axis (Hartman and Straus, 1933).
Pancreatitis is uncommonly diagnosed antemortem. However, it should be included in the differential list for anorexia and abdominal pain. Pancreatitis is more commonly noted in obese and diabetic monkeys. Radiographic findings may include an increased soft tissue radiopacity and diminished contrast in the right cranial abdomen, the stomach antrum is displaced to left, the proximal duodenum is displaced to right, the transverse colon is displaced caudally and focal mineralization of pancreas may be seen (uncommon).
Peritoneography is a radiographic contrast study of the peritoneal cavity using negative or positive contrast media to outline the peritoneal surface of the diaphragm, abdominal wall and serosal surfaces of the abdominal viscera. It is especially useful in assessing the integrity of the diaphragm or abdominal wall for congenital or acquired hernias. It enables the evaluation of the liver lobes and masses associated with the liver and adrenals.
Proper needle placement is confirmed by aspirating for air, urine or blood (manifestations of improper needle placement). Also, moving the tip of the needle gently from side to side ensures that the needle does not enter the retroperitonium or a solid abdominal organ.
Contrast agents are rapidly absorbed from the peritoneal cavity and excreted by the kidneys; a radiograph at 45 minutes post-injection can also demonstrate the renal collecting system. Pneumoperitoneography has shown no serious side effects and the CO2 is usually absorbed into the body tissues within 1–2 hours (Hoffman et al.) Pulmonary function must be monitored during the procedure. If the gas media used was room air, it should be removed at the end of the procedure.
Diaphragmatic hernias cause a cranial displacement of the diaphragm. They are not related to normal anatomical openings, but are usually, defects in one or more leaflets and the central tendon. Diaphragmatic hernias have been found in many different species such as golden lion tamarins, squirrel monkeys, and a pregnant baboon (Bush et al., 1980; Hendrickx and Gasser, 1967; T-W-Fiennes, 1972).
Inguinal hernias are relatively common. They are most common in males and may progress to an inguinoscrotal hernia. Omentum is most commonly herniated, although intestines may herniate as well. Using positive contrast peritonography on 100 human patients, the accuracy of the herniogram was 97% compared to only 59% with physical exam (James et al., 1975).
Perineal hernia is the result of weakened uterine and perineal ligaments from multiple births and a vertical posture. The bladder frequently herniates into a subcutaneous position in the perineal region, usually during the last trimester of pregnancy. It will often reoccur with each pregnancy.
Peritonitis\Ascites\Hemoabdomen are commonly associated with ruptured hollow viscera. Radiological signs of peritonitis include localized or general loss of abdominal detail and failure to visualize the serosal surfaces of the abdominal viscera. Free abdominal gas is usually associated with rupture of gastrointestinal tract; but a small amount of gas is usually undetectable. If gas is present, the serosal surface of the bowel may be more distinct. Also, since gas tends to rise, it may be visible radiographically adjacent to the diaphragm; the highest point in abdomen is the left side, between the diaphragm and the liver. In chronic peritonitis there may be marked abdominal effusion.
The spleen lies in the upper left quadrant of the abdomen just under the diaphragm. It is triangular in shape and more elongated than a human spleen.
Nonhuman primate kidneys are flattened and slightly irregular in outline. The cranial pole is sharper than the caudal pole and the left kidney is slightly larger then the right. Both kidneys are firmly attached to the dorsal abdominal wall near the thoracolumbar junction (Silverman and Morgan, 1980b). The left kidney is located more caudally and ventrally than the right, similar to the renal orientation in the dog and cat, but opposite to the human (Gray, 1959).
Nonhuman primates have unipyramidal kidneys, apart from spider monkeys (Ateles sp). Spider monkeys have multipapillary kidneys like humans, pigs, cattle and elephants. It is difficult, therefore, to opacify the renal collecting system of the spider monkey.
Survey radiographs do not identify the renal location or contour well in nonhuman primates, due to the paucity of abdominal fat.
Intravenous pyelography is also known as Excretory Urography (EU), or Intravenous Urography (IVU). It is a radiographic study done after intravenous injection of an iodinated contrast media to visualize the renal structure and the collecting system. Sequential radiographs highlight the renal vasculature (vascular phase), parenchyma (nephrogram phase), renal collecting ducts and ureters (pyelogram phase) as the contrast media is excreted by the kidneys and passes through the renal collecting ducts and ureters into the bladder. An IVP must not be performed in a dehydrated or severely renal compromised patient.
Cystography is a contrast study of the urinary bladder used to evaluate its position, morphology, integrity, distensibility, wall thickness and for intraluminal or intramural lesions (tumor, calculi, polyps).
Positive contrast cystography is optimal for evaluating bladder wall integrity and bladder position. Mural masses may be seen if the projection is tangential to the lesion.
Double contrast cystography provides the best mucosal detail and is optimal for the assessment of urinary calculi and intramural masses.
Pneumocystography highlights the bladder wall, but is the least preferred technique due to the risk of air embolism.
A positive contrast study of the urethra that evaluates the location, morphology and integrity of the urethra.
Renal cysts of varying sizes and numbers are commonly noted in nonhuman primates. Until they compose or compress more than 50% of the renal tissue, or are within the renal medulla, they are generally not clinically significant.
Glomerulonephritis is seen fairly frequently in all nonhuman primates but the callitrichids are especially prone to develop IgM/IgA nephropathy. Immune complexes directed toward parasitic and dietary antigens are hypothesized to play a role (Lowenstine, 2003). Glomerulonephritis has been a major cause of death and is a frequent cause of end stage renal disease in New World primates, especially in owl monkeys, squirrel monkeys, and other cebids. Owl monkeys have an increased incidence and severity of glomerulonephritis with advancing age (Jones et al., 1993a).
Hydronephrosis is a dilatation of the renal pelvis and calyces, leading to flattening of the renal papillae and atrophy of the renal cortex. Hydronephrosis is a frequent result of urinary tract obstruction (e.g., sequelae of endometriosis, tumors, renoliths).
Urolithiasis. The renal pelvis and calyces are sites for formation and accumulation of calculi. Renoliths may be well tolerated, but in some cases they lead to severe hydronephrosis. In the advent of pyelonephritis, renoliths can become a nidus of infection. Urolithiasis is rare in nonhuman primates while nephrocalcinosis is more common (Faltas, 2000; Silverman and Morgan, 1980b).
Obstructed bladder occasionally occurs in rhesus males during the breeding season when they have retrograde ejaculation and the coagulum obstructs the urethra or bladder. This is corrected by urinary catheterization or an emergency cystotomy.
The nonhuman primate prostate does not form a ring encircling the urethra but lies solely on the posterior and lateral surfaces. It consists of two histologically distinct divisions, the cranial and caudal lobes (Hartman and Straus, 1933). The cranial prostate supplies the semen coagulation component, while the caudal prostate is homologous to the human prostate. Only the marmoset (Callithrix jacchus) and the orangutans (Pongo pygmaeus) have a single lobed prostate (Harrison and Lewis, 1986).
A common characteristic of all prosimians is a bicornuate uterus. The rhesus macaque has a unicornuate uterus that is slightly flattened anteriorposteriorly. In many primate species, the cervical canal is not straight, but has varying degrees of tortuosity (Hafez and Jaszczak, 1972).
Hysterosalpingography The fallopian tube patency can be assessed with a hysterosalpingography despite the tortuosity of the primate cervix. Once anesthetized, a blunt 18 ga. needle or catheter is placed in the cervical canal and manipulated until it passes through to the uterine cavity, and a positive contrast medium (approximately 1 ml) is injected. Good quality hysterosalpingograms can be obtained and radiopaque material can be visualized in both fallopian tubes in 75% of monkeys (Bennett et al., 1995).
Vaginography Vaginography is a radiographic study using a retrograde infusion of positive contrast media, performed to evaluate vagina, cervix and urethra including strictures, fistulas, masses, or ectopic ureters.
Pelvimetry Pelvimetry of squirrel monkeys is a good predictor of perinatal mortality (Bennett et al., 1995). Lateral and anterioposterior pelvic radiographs of Bolivian squirrel monkeys were obtained 6 months postpartum. The pelvic inlet, midpelvis and pelvic outlet dimensions were measured and compared, based on the outcome of parturition. It was concluded that the size of the pelvis was a determinant of the outcome of pregnancy. A 10% reduction in pelvic outlet size resulted in a 20% reduction in the area of the birth canal. The size difference was only 0.17 cm, which is a minor difference to be detected by a physical measurement.
Pregnancy detection Pregnancy is always abdominal in nonhuman primates (Abitbol, 1993). Radiographs can be used to confirm pregnancy, especially in the later stages of pregnancy when the skeleton calcifies. Bone maturation and ossification can be used as growth standards and age indicators in experimental animals whose exact age is unknown. However, significant acceleration of bone maturation in nonhuman primates is observed, compared to humans. For example, the onset of wrist ossification of the rhesus macaque is approximately 120 days of gestation compared to a chimpanzee fetus in the last four weeks of gestation or a full-term newborn human (Michejda, 1980).
Endometriosis This is one of the most common reproductive disorders in Old World primates. It is defined clinically as the presence of both endometrial glands and stroma outside of the uterine cavity. The ectopic endometrial tissue responds to cyclic hormonal activity and proliferates, necroses and sloughs just as it would inside the uterus. This tissue either forms a cystic structure (endometrioma or “chocolate” blood-filled cysts) or sloughs into the peritoneal cavity where it can cause peritonitis or abdominal adhesions.
Uterine leiomyomas These smooth muscle tumors are common in all species of nonhuman primates (Lowenstine, 2003).
The thoracolumbar spine of the rhesus macaque consists of 20 segments, the anticlinal region being near the 10th thoracic segment. The thoracic spine is slightly kyphotic and the caudal lumbar spine is slightly lordotic. There are 13 thoracic vertebrae, all bearing ribs. There are 7 sternebrae.
In myelography the spinal cord is outlined by a nonionic contrast media injected into the subarachnoid space.
Epidurography is a radiographic contrast investigation of the epidural space using positive contrast medium to assess the cauda equina and proximal portions of the nerve roots. The main indication for epidurography is in the assessment of the lumbosacral region of the vertebral column or to confirm placement of epidural catheters (De Weert et al., 1995).
In discography, positive contrast medium is injected into the nucleous pulposus of the intervertebral disc. Normally, only a very small amount can be introduced. If there is damage of the annulus fibrosus, more contrast can be injected and the leakage will be evident on subsequent radiographs. This technique is usually reserved for diagnosis of protrusion of the L7 intervertebral disc.
Skeletal radiographic procedures are performed similarly to the methods described for dogs (Morgan et al., 1975). The radiographic changes of bone are a reflection of the underlying disease process. Radiographic abnormalities include alterations of size, shape, contour and radiopacity.
Longitudinal radiographic evaluation of skeletal maturation in rhesus monkeys demonstrated that the majority of appendicular ossification centers were identified, radiographically, by 175 days of age and that physeal closure was complete at 7.2 years in females and 7.3 years in male rhesus monkeys (Silverman et al., 1983). The order of physeal closure was similar, but not identical, in both sexes.
Arthrography is a radiographic contrast study of a joint used to delineate joint margins and to assess the articular cartilage, intraarticular ligaments, tendons, meniscus, and joint capsule.
Noma or cancrum oris, derived from the Greek noun “to devour,” is an acute gangrenous process which most frequently affects the oral cavity, particularly the gingiva, cheeks and lips, often producing bone denudation, sequestration and extensive facial disfigurement (Adams, 1980; Lackner et al., 1993). The occurrence of noma is highly suggestive of infection with an immunosuppressive type D retrovirus. Radiographic findings might include osteonecrosis, osteomyelitis, and bone sequestration.
“Potts’ disease” has been described in nonhuman primates as tuberculous lesions involving the vertebrae and adjacent spinal cord (Jones et al., 1993a; Jones et al., 1993b).
Calcinosis circumscripta is a deposition of amorphous calcium salts in the subcutaneous tissue and skin, usually on the extremities, and over bony prominences. Occasionally the nodules ulcerate and drain a chalky white semisolid substance. A histologic examination is required to differentiate types of mineralization (e.g. ossification or calcification). Radiographically, there is diffuse soft tissue calcification (Line et al., 1984).
Metabolic bone disease. Radiographic lesions do not occur until late in the course of metabolic bone disease (MBD), after 40% of the osseous mineral has been absorbed. Nonetheless, radiography is frequently the key to diagnosis. Typical findings include marked osseous demineralization, decreased cortical density, thinning of the cortices, increased trabecular pattern and folding fractures in long, weight supporting bones. The lamina dura dentis disappears naturally with skeletal maturity and in the early in the course of MBD in young animals (Fowler, 1978).
Nutritional secondary hyperparathyroidism is the excessive production of parathyroid hormone as a response to hypocalcemia, resulting in calcium resorption from bone. Under special dietary deficiencies, calcium resorption becomes detrimental to the integrity of the bone. The ultimate result is rickets in the young animal and osteomalacea in the adult. It presents as a progressive nutritional disease characterized by hyper-phophatemia, hypocalcemia, increased alkaline phosphatase, soft tissue mineralization, impaired locomotion, and poor skeletal mineralization (Tomson et al., 1978; Snyder et al., 1978). Radiographic findings include generalized areas of decreased bone mineralization in the axial and appendicular skeleton, and a wide variety of pathological fractures. It might include thin bone cortices of the long bones, bony deformities caused by folding and stress fractures of long bones, and increased soft tissue swelling at areas of tendinous attachment, e.g. patella, tuber calcis, and olecranon (Martin, 1978).
Rickets is a failure of mineralization of osteoid or cartilaginous bone matrix in young growing animals. Radiographically, there is a widening of the radiolucent epiphyseal plate, bowing of long bones, and widening of the metaphysis (“cupping”).
Osteomalacia is characterized by softening of bone and a decrease in bone density caused by insufficient mineralization of osteoid in the adult bone. It is a common result of metabolic bone disease. Radiographically, there is loss of bone density, thinning of cortices, coarsened trabecular pattern, mottled radiolucent areas, folding fractures, and bowed long bones.
Vitamin D deficiency. New World primates require dietary vitamin D3 to maintain normal skeletal mineral homeostasis. Failure to supply vitamin D3 to growing animals results in rickets, and osteomalacia in adults. Osteodystrophia fibrosa is considered to be a descriptive form of these conditions (Potkay, 1992).
Fibrous osteodystrophy is a condition that may be seen as a result of mineral imbalance or osteoporosis. There is an osteoclastic resorption of osteoid being replaced by a highly cellular connective tissue. Bones of the face and mandible are affected most frequently. It is a common manifestation of nutritional secondary hyperparathyroidism in New World primates such as spider and woolly monkeys. The mandible may become soft and pliable (“rubber jaw”). Radiographically, there is a marked decrease in bone density at the craniofacial bones.
Osteoporosis is a condition in which resorption of osteoid overbalances the deposition of new bone. Osteoporosis may be observed by protein malnutrition, hyperadrenocorticism (Cushing's disease), and iatrogenically by the exogenous administration of corticosteroids. Radiographic signs are detected only in advanced disease; bones are light, brittle and fragile. In young growing animals the sequence of cartilaginous transformation to bone may be delayed. Cancellous bone is primarily involved, non-weight bearing trabeculae being the first to be resorbed. Radiographic signs include thinning of the cortices with a corresponding increase in the medullary space.
Vitamin C deficiency or Scurvy. Most severe bone and joint changes associated with scurvy result from deficiency during periods of rapid bone growth. In the growth plate of long bones there is disruption of the normal maturation process. Radiographic signs include a transverse methaphyseal “white line” attributed to the thickening of the provisional zone of calcification on the growth plate and the “scurvy line”, a transverse zone of rarefaction shaftward to the “white line” (Eisele et al., 1992, Ratterree et al., 1990).
Additional radiographic findings were epiphyseal separations and displacements, peripheral metaphyseal clefts, cortical thinning, enlarged costochondral junctions, subperiosteal hemorrhages and physeal fractures (Eisele et al., 1992; Martin, 1978; Ratterree et al., 1990). Subsequent radiographs demonstrate angular deformities associated with physeal fractures. Subperiosteal cranial hemorrhages, or cephalohematomas, is a well known manifestation of vitamin C deficiency in squirrel monkeys. Subsequently, hyperostosis occurs due to deposition of new bone by the periosteum (Demaray et al., 1978; Blackwell et al., 1974).
Fluoroscopy provides real time radiographic viewing of moving anatomic structures. It can evaluate respiratory function or assess motility and function of the pharynx, esophagus, stomach and bowel. Fluoroscopy is quite useful in interventional studies involving directed aspirates, biopsies, and catheter placements. Serial jejunal biopsies (bacterial culture, virus isolation, IgA levels, administration of therapeutic or experimental agents directly into the proximal small intestines, by-passing acid secretions) can be obtained with a steerable catheter and fluoroscopy (Ford et al., 1989). The advantage of this technique is the non-invasive nature of the procedure vs. operative alternatives.
Nuclear imaging is a modality that provides diagnostic information on the functional status of an organ or body part. Radiopharmaceutical drugs that emit radioactive gamma rays are administered into the patient and, after the radionuclide has been deposited in the organ or tissue of interest, a gamma scintillation camera is used to detect ionizing gamma rays emitted from the animal's body. The radionuclide distribution is usually recorded as an image on x-ray film. Examples of scintigraphy studies thyroid, brain and bone scintigraphy. Scintigraphy imaging can also be used to observe and evaluate the presence of portosystemic shunts, gastric emptying, renal function, pulmonary perfusion, and for pulmonary ventilation studies (Owens, 1999).
Any correspondence should be directed to Dr. Kari L. Christe, California National Primate Research Center, University of California, Davis, One Shields Avenue, Davis, CA 95616-8542, USA. Phone: (530) 752-0447; Fax: (530) 752-2880; Email: cnprc_info@primate.ucdavis.edu