Comparative Medicine Copyright 2016 by the American Association for Laboratory Animal Science
Vol 66, No 5 October 2016 Pages 420–423
Case Report
Juxtaarticular Myxoma in a Pigtail Macaque (Macaca nemestrina) Brianna L Skinner,1,* Crystal H Johnson,2 and Shannon H Lacy3 A 10-y-old pigtail macaque presented with a subcutaneous, soft-tissue mass overlying the right stifle joint. Here we describe the clinical case and histopathologic and immunohistochemical analysis of this lesion. This case represents the first published report of juxtaarticular myxoma in a pigtail macaque.
Myxomas are rare benign soft tissue neoplasms believed to be of fibroblastic origin.2 They arise in a variety of tissues, including the skin and subcutis, bone aponeuroses, genitourinary tract, retroperitoneum, intestines, muscle, joints, pharynx, and tonsils.1 Grossly, myxomas are mucoid, myxoid, gelatinous, and cystic or multicystic.10 These lesions have been reported in humans, dogs, sheep, nonhuman primates, and a rabbit.3,5,9-12 Here we describe the clinical, gross, and light microscopic findings regarding a subcutaneous myxoma in an adult pigtail macaque (Macaca nemestrina). To our knowledge, this case represents the first report of a myxoma in a pigtail macaque.
Materials and Methods
The pigtail macaque was singly housed in accordance with the Guide for the Care and Use of Laboratory Animals in an AAALACaccredited facility at the Centers for Disease Control and Prevention (Atlanta, GA).6 Relative humidity and temperature in the animal room were maintained at 30% to 70% and 64 to 84 °F (18 to 29 °C), respectively, under a 12:12-h light:dark cycle. Water was provided without restriction through an automatic delivery system. The diet comprised a mixture of high-protein chow (Lab Diet High-Protein Monkey Diet 5045, PMI Nutrition International, St Louis, MO) high-fiber chow (Fiber-Plus Monkey Diet 5049, PMI Nutrition International), various fruits and vegetables, and treats (Bio-serv, Frenchtown, NJ). All animal procedures and protocols were approved by the IACUC at the Centers for Disease Control and Prevention in accordance with the Guide for the Care and Use of Laboratory Animals.6
Case History
At the time of the clinical presentation, the 9.6-kg, 10-y-old, female pigtail macaque was not assigned to or used on any research protocols. Semiannual physical examinations and hematology, Received: 28 Feb 2016. Revision requested: 21 Apr 2016. Accepted: 28 Apr 2016. 1 National Center for Emerging and Zoonotic Infectious Diseases, Division of Scientific Resources, Animal Resources Branch, Atlanta, Georgia; 2Icahn School of Medicine at Mount Sinai, Center for Comparative Medicine and Surgery, New York, New York; and 3 Veterinary Pathology Service, Joint Pathology Center, Silver Spring, Maryland. *Corresponding author. Email: [email protected]
clinical chemistry, and bacteriology (for example, screening for Shigella, Salmonella, Campylobacter, and Yersinia) analyses performed in 2012 and 2013 revealed no abnormal findings. An antibody titer for measles was positive, and antibody titers for Macacine herpesvirus 1, simian T-cell leukemia virus type 1, simian retrovirus type D, and SIV were negative; the macaque also was PCR-negative for simian retrovirus. In September 2012, the macaque presented with soft-tissue swelling at the craniomedial aspect of the right stifle joint, with no visible wounds, bruising, or hair loss present; she exhibited full weight-bearing on the affected limb when observed in the cage. Further examination under sedation (10 mg/kg ketamine IM) revealed full range of motion of the limbs. The initial differential diagnosis was lipoma or a benign cystic lesion. A biopsy was scheduled for 3 d later, by which time the swelling had resolved completely, prompting cancellation of the planned biopsy. In May 2013, the macaque again presented with soft-tissue swelling overlying the right stifle joint, and she again was sedated (10 mg/kg ketamine IM). Examination of the right pelvic limb revealed a well-encapsulated, moveable, semifirm, lobular subcutaneous mass that was approximately 5 cm in diameter (Figure 1 A and B). An attempt to obtain a fine-needle aspirate from the mass did not produce a sample, and because of its apparent reoccurrence, excisional biopsy was performed. The macaque was placed in dorsal recumbency, and the skin overlying the anterior aspect of the right stifle joint was prepared for an aseptic regional lumpectomy. For surgery, anesthesia was induced by isoflurane (Isothesia, Henry Schein, Melville, NY) at 5% initially and then maintained by using a gas flow rate of 1% to 3%. A longitudinal incision (approximately 1.5 in. [3.8 cm]) was made deep to the skin on the craniolateral aspect of the right stifle joint just adjacent to the mass. The mass appeared pale, yellow, and lipomatous grossly (Figure 2). The mass was bluntly dissected away from the surrounding normal tissue by using Mayo scissors. The entire mass and some muscular attachments were removed. Due to the proximity of the mass to the patella, the presence of the drawer reflex and cruciate ligament integrity were verified. All hemorrhage was controlled by applying pressure or hemostats, and the incision was closed in 3 layers, comprising 2 simple continuous patterns with 3-0 polyglactin
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Juxtaarticular myxoma in a pigtail macaque
Figure 1. (A) Lateral view of the subcutaneous soft-tissue mass on the right stifle joint. (B) Anterior view of the subcutaneous soft-tissue mass on the right stifle joint
910 (Ethicon, Somerville, NJ) and skin apposition with surgical glue (SutureVet Vetclose, Henry Schein) reinforced with simple interrupted sutures of 3-0 nylon (Ethicon). The excised mass was fixed in 10% neutral buffered formalin and submitted for histopathology. Perioperative analgesic treatment (0.3 mg/kg IM; Metacam, Boehringer Ingelheim Vetmedica, St Joseph, MO) was provided. No complications occurred during surgery or recovery. Postsurgical analgesic treatment (0.2 mg/kg IM; Buprenorphine SR, ZooPharm, Windsor, CO) was administered once during recovery from anesthesia, and oral meloxicam (0.3 mg/kg PO daily) was initiated the next day and provided for a total of 3 d. The day after surgery, the animal was observed moving around in her cage, bearing full weight on the affected limb. There was no drainage from the incision site, and the macaque did not exhibit any signs of pain. Six weeks after surgery, dorsovental and lateral radiographs of the right stifle joint revealed no abnormalities. A subsequent annual physical examination (in 2014) revealed no abnormalities.
Histologic Examination
Representative tissue samples were embedded in paraffin, processed routinely, sectioned at 4 to 6 μm, and stained with hematoxylin and eosin. The neoplasm multifocally extended to surgical
margins, and consisted of evenly spaced spindle to stellate cells with distinct cell borders, scant eosinophilic fibrillar cytoplasm, and centrally placed ovoid nuclei with finely stippled chromatin and generally distinct nucleoli (Figure 3). At its borders, the neoplasm compressed adjacent preexisting fibrous connective tissue (Figure 3). No mitotic figures were observed, and no nuclear or cellular atypia was present. Neoplastic cells were widely separated by an abundant myxomatous matrix, which stained positively with Alcian blue 2.5 (Figure 4). Immunohistochemistry did not indicate S100 protein expression by neoplastic cells (data not shown). In light of these findings, the microscopic diagnosis was an incompletely excised benign subcutaneous myxoma.
Discussion
A classification scheme developed after examination of more than 60 human myxoma lesions comprises 8 categories, including a mainstream myxoma of soft tissue termed juxtaarticular myxoma.1 Juxtaarticular myxoma is a benign tumor that primarily occurs in the subcutaneous adipose tissue in the vicinity of large joints, with 88% of those in humans arising adjacent to the knee.7,10 Additional reported anatomic sites include the elbow region, biceps tendon, shoulder region, and ankle.10 Clinical presentation can include a palpable mass or swelling
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Figure 4. Subcutaneous fibroadipose tissue; pig-tailed macaque. Myxoma. Abundant myxomatous extracellular matrix (blue) widely separates neoplastic spindle cells (pink, black arrows). Alcian blue 2.5 stain; magnification, 400×.
Figure 2. Surgical incision of the right stifle joint. A well-circumscribed, encapsulated mass with a gelatinous appearance is located in the subcutis and lies anterior to the stifle joint.
did not observe obvious clinical signs of pain in our macaque, the gross and microscopic characteristics of her tumor are consistent with juxtaarticular myxoma in humans. As evidenced in this case report, even wide surgical resection may not be sufficient to achieve tumor-free margins, and local recurrence remains a possibility. Approximately 34% of juxtaarticular myxoma cases in humans have recurred one or more times.10 Despite being incomplete, surgical resection in this macaque eliminated the need for additional treatments until the time of euthanasia—this macaque was placed on a SIV–HIV study 3 mo after the surgical procedure but was euthanized due to irreversible cardiac and hepatic abnormalities. As with human patients, the management of NHP with juxtaarticular myxomas may require additional treatment (for example, meniscectomy, arthrostomy) after surgical removal of the tumor if joint or menisci involvement is present.4,7,8,10 Although myxomas reportedly are rare in NHP, the true prevalence has not yet been established and may become more apparent as data and reports accumulate.
Acknowledgments
Figure 3. Subcutaneous fibroadipose tissue; pig-tailed macaque. Myxoma. A neoplasm composed of evenly spaced spindle to stellate cells that are arranged in haphazard streams is expanding the subcutis and compressing adjacent preexisting fibrous tissue (black arrows, bottom). Neoplastic cells are widely separated by abundant myxomatous matrix (blue arrows, clear space and amphophilic fibrillar material). Hematoxylin and eosin stain; magnification, 100×.
that may be painful. Histologically, juxtaarticular myxomas appear as fibroblast-like cells in a hypovascular myxoid matrix or as a diffuse pattern of cells without well-defined boundaries and entrapped in islets of fat cells.10 Mitotic figures are usually absent or rare.10 The myxoma in this macaque was confined to subcutis overlying the right stifle, with minimal attachment to the vastus medialis. Myxomas have been reported in primates previously,11,12 but none have been reported in pigtail macaques. Although we 7
We thank the veterinarians, managers, and technicians in the Animal Resources Branch at CDC for their efforts in supporting the care of this animal. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Centers for Disease Control and Prevention, Department of Health and Human Services, Department of the Army, Department of Defense, or the US Government.
References
1. Allen PW. 2000. Myxoma is not a single entity: a review of the concept of myxoma. Ann Diagn Pathol 4:99–123. 2. Berrocal A, Millan Y, Ordas J, de las Mulas JM. 2001. A joint myxoma in a dog. J Comp Pathol 124:223–226. 3. Craig LE, Krimer PM, Cooley AJ. 2010. Canine synovial myxoma: 39 cases. Vet Pathol 47:931–936. 4. Fukuda K, Hitora T, Chikami K, Kawaguchi Y, Imaizumi Y, Yamamoto T. 2012. Locking of the knee caused by an intraarticular myxoma. Cancer Therapy 8:113–117. 5. Ilhan F, Yener Z. 2009. Pulmonary myxoma in a sheep. Vet Pathol 46:457–459.
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6. Institute for Laboratory Animal Research. 2011. Guide for the care and use of laboratory animals, 8th ed. Washington (DC): National Academies Press. 7. Korver RJ, Theunissen PH, van de Kreeke WT, van der Linde MJ, Heyligers IC. 2010. Juxtaarticular myxoma of the knee in a 5-year-old boy: a case report and review of the literature. Eur Radiol 20:764–768. 8. Kosty JW, Moore JG. 2009. Juxtaarticular myxoma within the suprapatellar pouch masquerading as a ganglion cyst. Orthopedics 32:527.
9. Lohr CV, Hedge ZN, Pool RR. 2012. Infiltrative myxoma of the stifle joint and thigh in a domestic rabbit (Oryctolagus cuniculus). J Comp Pathol 147:218–222. 10. Meis JM, Enzinger FM. 1992. Juxta-articular myxoma: a clinical and pathologic study of 65 cases. Hum Pathol 23:639–646. 11. Shalev M, Murphy JC, Fox JG, Wallstrom AC, Gottlieb LS. 1980. Myxoma of bone in a nonhuman primate. Cancer 45:2573–2582. 12. Wallace SM, Szabo KA, Schlabritz-Loutsevitch NE, Dick EJ, Blanchard TW, Hubbard GB. 2008. Myxomatous neoplasms in the perineal region of baboons. J Med Primatol 37:261–270.
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Vol 66, No 5 October 2016 Pages 420–423
Case Report
Juxtaarticular Myxoma in a Pigtail Macaque (Macaca nemestrina) Brianna L Skinner,1,* Crystal H Johnson,2 and Shannon H Lacy3 A 10-y-old pigtail macaque presented with a subcutaneous, soft-tissue mass overlying the right stifle joint. Here we describe the clinical case and histopathologic and immunohistochemical analysis of this lesion. This case represents the first published report of juxtaarticular myxoma in a pigtail macaque.
Myxomas are rare benign soft tissue neoplasms believed to be of fibroblastic origin.2 They arise in a variety of tissues, including the skin and subcutis, bone aponeuroses, genitourinary tract, retroperitoneum, intestines, muscle, joints, pharynx, and tonsils.1 Grossly, myxomas are mucoid, myxoid, gelatinous, and cystic or multicystic.10 These lesions have been reported in humans, dogs, sheep, nonhuman primates, and a rabbit.3,5,9-12 Here we describe the clinical, gross, and light microscopic findings regarding a subcutaneous myxoma in an adult pigtail macaque (Macaca nemestrina). To our knowledge, this case represents the first report of a myxoma in a pigtail macaque.
Materials and Methods
The pigtail macaque was singly housed in accordance with the Guide for the Care and Use of Laboratory Animals in an AAALACaccredited facility at the Centers for Disease Control and Prevention (Atlanta, GA).6 Relative humidity and temperature in the animal room were maintained at 30% to 70% and 64 to 84 °F (18 to 29 °C), respectively, under a 12:12-h light:dark cycle. Water was provided without restriction through an automatic delivery system. The diet comprised a mixture of high-protein chow (Lab Diet High-Protein Monkey Diet 5045, PMI Nutrition International, St Louis, MO) high-fiber chow (Fiber-Plus Monkey Diet 5049, PMI Nutrition International), various fruits and vegetables, and treats (Bio-serv, Frenchtown, NJ). All animal procedures and protocols were approved by the IACUC at the Centers for Disease Control and Prevention in accordance with the Guide for the Care and Use of Laboratory Animals.6
Case History
At the time of the clinical presentation, the 9.6-kg, 10-y-old, female pigtail macaque was not assigned to or used on any research protocols. Semiannual physical examinations and hematology, Received: 28 Feb 2016. Revision requested: 21 Apr 2016. Accepted: 28 Apr 2016. 1 National Center for Emerging and Zoonotic Infectious Diseases, Division of Scientific Resources, Animal Resources Branch, Atlanta, Georgia; 2Icahn School of Medicine at Mount Sinai, Center for Comparative Medicine and Surgery, New York, New York; and 3 Veterinary Pathology Service, Joint Pathology Center, Silver Spring, Maryland. *Corresponding author. Email: [email protected]
clinical chemistry, and bacteriology (for example, screening for Shigella, Salmonella, Campylobacter, and Yersinia) analyses performed in 2012 and 2013 revealed no abnormal findings. An antibody titer for measles was positive, and antibody titers for Macacine herpesvirus 1, simian T-cell leukemia virus type 1, simian retrovirus type D, and SIV were negative; the macaque also was PCR-negative for simian retrovirus. In September 2012, the macaque presented with soft-tissue swelling at the craniomedial aspect of the right stifle joint, with no visible wounds, bruising, or hair loss present; she exhibited full weight-bearing on the affected limb when observed in the cage. Further examination under sedation (10 mg/kg ketamine IM) revealed full range of motion of the limbs. The initial differential diagnosis was lipoma or a benign cystic lesion. A biopsy was scheduled for 3 d later, by which time the swelling had resolved completely, prompting cancellation of the planned biopsy. In May 2013, the macaque again presented with soft-tissue swelling overlying the right stifle joint, and she again was sedated (10 mg/kg ketamine IM). Examination of the right pelvic limb revealed a well-encapsulated, moveable, semifirm, lobular subcutaneous mass that was approximately 5 cm in diameter (Figure 1 A and B). An attempt to obtain a fine-needle aspirate from the mass did not produce a sample, and because of its apparent reoccurrence, excisional biopsy was performed. The macaque was placed in dorsal recumbency, and the skin overlying the anterior aspect of the right stifle joint was prepared for an aseptic regional lumpectomy. For surgery, anesthesia was induced by isoflurane (Isothesia, Henry Schein, Melville, NY) at 5% initially and then maintained by using a gas flow rate of 1% to 3%. A longitudinal incision (approximately 1.5 in. [3.8 cm]) was made deep to the skin on the craniolateral aspect of the right stifle joint just adjacent to the mass. The mass appeared pale, yellow, and lipomatous grossly (Figure 2). The mass was bluntly dissected away from the surrounding normal tissue by using Mayo scissors. The entire mass and some muscular attachments were removed. Due to the proximity of the mass to the patella, the presence of the drawer reflex and cruciate ligament integrity were verified. All hemorrhage was controlled by applying pressure or hemostats, and the incision was closed in 3 layers, comprising 2 simple continuous patterns with 3-0 polyglactin
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Juxtaarticular myxoma in a pigtail macaque
Figure 1. (A) Lateral view of the subcutaneous soft-tissue mass on the right stifle joint. (B) Anterior view of the subcutaneous soft-tissue mass on the right stifle joint
910 (Ethicon, Somerville, NJ) and skin apposition with surgical glue (SutureVet Vetclose, Henry Schein) reinforced with simple interrupted sutures of 3-0 nylon (Ethicon). The excised mass was fixed in 10% neutral buffered formalin and submitted for histopathology. Perioperative analgesic treatment (0.3 mg/kg IM; Metacam, Boehringer Ingelheim Vetmedica, St Joseph, MO) was provided. No complications occurred during surgery or recovery. Postsurgical analgesic treatment (0.2 mg/kg IM; Buprenorphine SR, ZooPharm, Windsor, CO) was administered once during recovery from anesthesia, and oral meloxicam (0.3 mg/kg PO daily) was initiated the next day and provided for a total of 3 d. The day after surgery, the animal was observed moving around in her cage, bearing full weight on the affected limb. There was no drainage from the incision site, and the macaque did not exhibit any signs of pain. Six weeks after surgery, dorsovental and lateral radiographs of the right stifle joint revealed no abnormalities. A subsequent annual physical examination (in 2014) revealed no abnormalities.
Histologic Examination
Representative tissue samples were embedded in paraffin, processed routinely, sectioned at 4 to 6 μm, and stained with hematoxylin and eosin. The neoplasm multifocally extended to surgical
margins, and consisted of evenly spaced spindle to stellate cells with distinct cell borders, scant eosinophilic fibrillar cytoplasm, and centrally placed ovoid nuclei with finely stippled chromatin and generally distinct nucleoli (Figure 3). At its borders, the neoplasm compressed adjacent preexisting fibrous connective tissue (Figure 3). No mitotic figures were observed, and no nuclear or cellular atypia was present. Neoplastic cells were widely separated by an abundant myxomatous matrix, which stained positively with Alcian blue 2.5 (Figure 4). Immunohistochemistry did not indicate S100 protein expression by neoplastic cells (data not shown). In light of these findings, the microscopic diagnosis was an incompletely excised benign subcutaneous myxoma.
Discussion
A classification scheme developed after examination of more than 60 human myxoma lesions comprises 8 categories, including a mainstream myxoma of soft tissue termed juxtaarticular myxoma.1 Juxtaarticular myxoma is a benign tumor that primarily occurs in the subcutaneous adipose tissue in the vicinity of large joints, with 88% of those in humans arising adjacent to the knee.7,10 Additional reported anatomic sites include the elbow region, biceps tendon, shoulder region, and ankle.10 Clinical presentation can include a palpable mass or swelling
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Figure 4. Subcutaneous fibroadipose tissue; pig-tailed macaque. Myxoma. Abundant myxomatous extracellular matrix (blue) widely separates neoplastic spindle cells (pink, black arrows). Alcian blue 2.5 stain; magnification, 400×.
Figure 2. Surgical incision of the right stifle joint. A well-circumscribed, encapsulated mass with a gelatinous appearance is located in the subcutis and lies anterior to the stifle joint.
did not observe obvious clinical signs of pain in our macaque, the gross and microscopic characteristics of her tumor are consistent with juxtaarticular myxoma in humans. As evidenced in this case report, even wide surgical resection may not be sufficient to achieve tumor-free margins, and local recurrence remains a possibility. Approximately 34% of juxtaarticular myxoma cases in humans have recurred one or more times.10 Despite being incomplete, surgical resection in this macaque eliminated the need for additional treatments until the time of euthanasia—this macaque was placed on a SIV–HIV study 3 mo after the surgical procedure but was euthanized due to irreversible cardiac and hepatic abnormalities. As with human patients, the management of NHP with juxtaarticular myxomas may require additional treatment (for example, meniscectomy, arthrostomy) after surgical removal of the tumor if joint or menisci involvement is present.4,7,8,10 Although myxomas reportedly are rare in NHP, the true prevalence has not yet been established and may become more apparent as data and reports accumulate.
Acknowledgments
Figure 3. Subcutaneous fibroadipose tissue; pig-tailed macaque. Myxoma. A neoplasm composed of evenly spaced spindle to stellate cells that are arranged in haphazard streams is expanding the subcutis and compressing adjacent preexisting fibrous tissue (black arrows, bottom). Neoplastic cells are widely separated by abundant myxomatous matrix (blue arrows, clear space and amphophilic fibrillar material). Hematoxylin and eosin stain; magnification, 100×.
that may be painful. Histologically, juxtaarticular myxomas appear as fibroblast-like cells in a hypovascular myxoid matrix or as a diffuse pattern of cells without well-defined boundaries and entrapped in islets of fat cells.10 Mitotic figures are usually absent or rare.10 The myxoma in this macaque was confined to subcutis overlying the right stifle, with minimal attachment to the vastus medialis. Myxomas have been reported in primates previously,11,12 but none have been reported in pigtail macaques. Although we 7
We thank the veterinarians, managers, and technicians in the Animal Resources Branch at CDC for their efforts in supporting the care of this animal. The views expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Centers for Disease Control and Prevention, Department of Health and Human Services, Department of the Army, Department of Defense, or the US Government.
References
1. Allen PW. 2000. Myxoma is not a single entity: a review of the concept of myxoma. Ann Diagn Pathol 4:99–123. 2. Berrocal A, Millan Y, Ordas J, de las Mulas JM. 2001. A joint myxoma in a dog. J Comp Pathol 124:223–226. 3. Craig LE, Krimer PM, Cooley AJ. 2010. Canine synovial myxoma: 39 cases. Vet Pathol 47:931–936. 4. Fukuda K, Hitora T, Chikami K, Kawaguchi Y, Imaizumi Y, Yamamoto T. 2012. Locking of the knee caused by an intraarticular myxoma. Cancer Therapy 8:113–117. 5. Ilhan F, Yener Z. 2009. Pulmonary myxoma in a sheep. Vet Pathol 46:457–459.
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6. Institute for Laboratory Animal Research. 2011. Guide for the care and use of laboratory animals, 8th ed. Washington (DC): National Academies Press. 7. Korver RJ, Theunissen PH, van de Kreeke WT, van der Linde MJ, Heyligers IC. 2010. Juxtaarticular myxoma of the knee in a 5-year-old boy: a case report and review of the literature. Eur Radiol 20:764–768. 8. Kosty JW, Moore JG. 2009. Juxtaarticular myxoma within the suprapatellar pouch masquerading as a ganglion cyst. Orthopedics 32:527.
9. Lohr CV, Hedge ZN, Pool RR. 2012. Infiltrative myxoma of the stifle joint and thigh in a domestic rabbit (Oryctolagus cuniculus). J Comp Pathol 147:218–222. 10. Meis JM, Enzinger FM. 1992. Juxta-articular myxoma: a clinical and pathologic study of 65 cases. Hum Pathol 23:639–646. 11. Shalev M, Murphy JC, Fox JG, Wallstrom AC, Gottlieb LS. 1980. Myxoma of bone in a nonhuman primate. Cancer 45:2573–2582. 12. Wallace SM, Szabo KA, Schlabritz-Loutsevitch NE, Dick EJ, Blanchard TW, Hubbard GB. 2008. Myxomatous neoplasms in the perineal region of baboons. J Med Primatol 37:261–270.
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