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What Is Your Diagnosis?

History

A 1.5-year-old male Faverolles chicken was presented to the Louisiana State University Veterinary Teaching Hospital because of a soft-tissue wound associated with the dorsolateral aspect of digit 4 of the right foot. The wound was first observed 2 weeks before presentation and appeared to be associated with one of the digit feather follicles. The owners began treating the toe lesion at home with a combination of systemic and topical antibiotic therapies (a store-bought, penicillin-based injectable product and topical, dilute iodine lavage). Per the owners, the wound initially improved with their treatment efforts; however, they were unable to maintain medical therapy. The bird was obtained from a pet store as a chick and had been vaccinated for fowl pox. The bird lived with 20 to 25 other hens and roosters in a large outdoor enclosure, except during the night when they were placed in a coop. The husbandry was considered excellent by veterinary evaluation. The owners also noted that a few birds might have succumbed to Marek's disease several years previously; however, a definitive diagnosis was never obtained on these suspect cases.

On physical examination, the bird was bright, alert, and responsive with a weight-bearing lameness associated with the right leg. The bird weighed 3.6 kg with a body condition score of 3/5. The wound was associated with digit 4 of the right foot, extending from the digit 4 nail to the distal tarsometatarsus. This region was markedly edematous with the lesion extending to the dorsolateral aspect of digit 3. A 3.5-cm-diameter thick scab that appeared to extend into the subcutaneous tissues characterized the wound (Figs la and b). The surrounding tissue was markedly erythematous. The plantar aspect of the foot was unremarkable. The remainder of the physical examination was unremarkable.

Initial treatment consisted of a long-acting doxycycline hyclate injection (50 mg/kg IM q7d; Vibramycin, Pfizer PFE Switzerland GmbH, Zurich, Switzerland) and meloxicam (1 mg/kg PO q24h). The foot was cleaned with dilute iodine, but the wound was not debrided. A nonadherent bandage was applied to the foot to prevent further contamination.

Two days after admission, the bird appeared to be in less pain and the previously noted lameness had improved. A blood sample was collected from the right jugular vein and was submitted for a complete blood count (CBC) and biochemical analysis. Results of the CBC were unremarkable. A marked increase in creatine kinase (CK) activity was noted (43 120 U/L; reference interval, 100-200 U/L) along with a moderate increase in activity of aspartate aminotransferase (AST) (765 U/L; reference interval, 20-350 U/L). (1,2) The remaining biochemical parameters were within the reference intervals. For further diagnostic testing, the bird was induced with 5% isoflurane delivered via facemask in a 1.5-L flow of oxygen. Once induced, the patient was intubated with an uncuffed, 4.5-mm endotracheal tube and maintained on 2.0%-2.5% isoflurane and a 1.5-L flow of oxygen. Radiographs of the whole body and collimated views of the right foot were performed under general anesthesia. A circumferential soft-tissue swelling of the right digit 4 was observed, but no evidence of bone remodeling was visible. An enlarged soft-tissue structure consistent with spleen or gonads was observed. Mineralization associated with another soft-tissue opacity in the region of the kidneys was also observed (Fig 2). The bird recovered from anesthesia uneventfully.

Diagnosis

Based on the patient's history and presenting clinical signs, a severe pyogranulomatous soft-tissue reaction associated with the dorsolateral aspect of digit 4 was suspected. A feather cyst with resulting infection was considered a top differential diagnosis based on the initial examination and diagnostic test results. Direct trauma to the digit with secondary infection was also considered. A bacterial pathogen was believed to be a contributing factor of the toe lesion, given that the wound improved with topical therapies and injectable antibiotics. Neoplasia was considered less likely; however, after observing mineralization of soft-tissue structures on the radiographs, a fine-needle aspirate of the digit was performed. Results of cytologic examination showed 58%-75% intermediate to large lymphocytes, 21%-34% small lymphocytes, and 3%-4% heterophils. Cytologic interpretation was consistent with cutaneous lymphoma; however, because of poor preservation of cells, biopsy was recommended. Diagnostic options included amputation of the digit with subsequent histopathologic examination, coelioscopy with biopsy of any abnormal organ tissue, or a combination of the 2 procedures. The owners elected coelioscopy.

Coelioscopy was performed by using a 2.9-mm rigid endoscope. The bird was anesthetized as previously described. A 3.0-mm incision was made into the left lateral flank, extending into the coelom. The endoscope was introduced and viscera and air sacs were visualized. A large amount of intracoelomic fat was observed. The liver was mildly rounded, but no obvious abnormalities were observed on the capsular surface. The visualized portions of the spleen, testicles, and kidneys appeared grossly normal. The lungs and air sacs appeared hypervascular. Biopsies and impression smears of the lungs, air sacs, liver, and kidneys were performed. The incision was closed with a single simple-interrupted absorbable suture and the patient recovered uneventfully from the procedure.

No cytologic abnormalities were identified from the coelioscopic biopsy samples submitted. Histopathologic examination demonstrated no overtly atypical cells or evidence of lymphoma. Although lymphoma rarely presents as an isolated lesion, it was still considered possible. Regardless of the cause, amputation of the digit would likely result in better quality of life. Therefore, the owner elected amputation and biopsy of the digit.

The bird was premedicated with hydromorphone (0.3 mg/kg IM) and was induced for general anesthesia as previously described. The surgical site was aseptically prepared. Using a # 10 scalpel blade, an elliptical incision was made around the ulcerated portion of the lesion. The previously noted scab was found to extend into the dermis (Fig 3a). A firm, well-demarcated, white tissue deep to the scab extended through the subcutaneous and muscular tissues, coming in close contact with the phalanx. This tissue did not appear to involve the bone (Fig 3b). The lesion was excised and the skin and soft tissues proximal to the lesion were undermined and reflected proximally beyond the level of the tarsometatarsal-phalangeal joint. Amputation of digit 4 was performed. The previously undermined tissues were sutured in a simple interrupted pattern (40 polydioxanone; PDS II, Ethicon, Somerville, NJ, USA). The bird recovered from anesthesia uneventfully. A nonadherent bandage was placed over the surgical site. By the next morning, the bird was ambulating well and was completely weight-bearing on the right foot. The bird was prescribed meloxicam (1 mg/kg PO q24h) and discharged. The owners were instructed to keep the patient indoors and perform daily bandage changes to prevent contamination of the surgical site. A recheck exam was scheduled for the next week.

Results of histopathologic evaluation of the amputated digit were consistent with cutaneous lymphoma. The bird was reexamined 5 days after discharge; however, the bird acutely decompensated the night before presentation. The owners described an ambulatory paresis of the right leg that progressed to nonambulatory paresis the next morning. Before the right leg paresis, the bird was doing well at home and was appropriately cage rested. The owners did not believe that the acute paresis was due to trauma.

On physical examination, the bird was nonambulatory in the right leg. Motor function was not observed in the right leg, but pain sensation was present. An obvious fracture or luxation associated with the limb and joints was not palpated. The surgical site appeared to be healing well. The left limb was unremarkable. No other abnormalities were observed. Because of poor prognosis, the owners elected euthanasia and the carcass was submitted for necropsy.

At necropsy, a small cutaneous mass was found on the ventral aspect of the neck in the midcervical region. There were numerous, pale tan to pink, multifocal nodules on the serosa of the duodenum and pancreas. Two firm, white masses were also present in the duodenal and jejunal walls. The testes were bilaterally enlarged. On cut surface, the right testicle was yellow to white and avascular with the left testicle being pink with prominent vasculature. The right kidney was almost completely expanded and replaced by a tan, 8.0 X 3.0 X 2.0-cm mass (Fig 4). The mass had extended into the right lateral body wall and adjacent skeletal muscle. The right sciatic plexus was embedded and replaced by the mass. The bone marrow was diffusely dark red.

Histopathologic examination of the cutaneous cervical mass and the tissue surrounding the amputation site were both consistent with a round cell neoplasm. Both the kidneys and testicles contained a similar round cell neoplasm, which was more pronounced on the right than left. Tumor cells also infiltrated the small and large intestine, pancreas, ventriculus, mesentery, and bone marrow. Lymphoma was the primary differential. The brain and sections of the left sciatic plexus and brachial plexus were unremarkable. Because of extensive body wall infiltration, the right sciatic plexus could not be accurately assessed. A formalin-fixed sample of the right kidney tumor was sent to the University of Georgia Poultry Diagnostic and Research Center for Marek's disease testing. Analysis via polymerase chain reaction was positive for Marek's disease.

Discussion

Lymphoma is a broad term for any neoplastic disease affecting peripheral lymphoid tissues and cells. It is a common form of neoplasia in all domestic animal species; however, cell origin and tissue affected are variable. Cutaneous lymphoma is one subtype of lymphoma and can present as a single tumor or as a manifestation of systemic disease.

Viral etiologies have been linked to lymphoma across many species. (3) Although viral infections are associated with lymphoma, the disease can also occur without an infectious etiology. As an example, cattle may develop lymphoid tumors without bovine leukosis virus. Similarly, a cat diagnosed with lymphoid leukemia may not have been exposed to feline leukemia virus. This concept is true in avian medicine as well.

In birds, the current understanding of viral etiologies and lymphoid neoplasia is limited. Both lymphoid leukemia and lymphoma have been documented in psittacine species; however, an infectious etiology has not yet been determined. (4-6) In poultry, lymphoid tumors have been associated with herpesviruses (Marek's disease) and retroviruses (lymphoid leukosis and reticuloendotheliosis). (7-10) The extensive amount of research supporting these viral etiologies has been conducted largely because of the inherent nature of poultry playing a role in the food animal industry.

Marek's disease is a worldwide, contagious disease of chickens. Although vaccination has greatly reduced the number of cases in commercial flocks, new strains of the virus emerge, resulting in decreased vaccine efficacy and increased mortality. (7,9) Caused by an oncogenic [alpha]-herpesvirus, Marek's disease is a highly contagious, lympho-proliferative, and neuropathic disorder of domestic chickens, turkeys, and quail. (5,7) The virions are transmitted through inhalation of skin and feather debris from a chicken that is currently shedding the virus. (9) Pathogenesis is complex, involving a latent phase, an immunosuppression phase, and finally, neoplastic transformation and tumor development. (7) Furthermore, 4 forms of the disease are clinically recognized, which can complicate diagnosis. (7) The first form involves wing or leg paresis or paralysis. This neuropathy results from invasion of the nerves of the sciatic plexus, nerves of the brachial plexus, or ischiatic nerves by neoplastic lymphocytes. The second form involves an acute presentation of high mortality whereby lymphoid tumors develop in the viscera, eyes, nerves, and skin. The third form of the disease, which is considered rare, is typified by an intermittent paresis or paralysis that resolves in 24-48 hours. The fourth form of the disease is considered the most virulent. In these cases, the birds succumb to the disease before any lymphoid tumors develop.

Historically, Marek's disease has been described as a disease that afflicts birds less than 1 year of age; however, the data are likely skewed as commercial birds are slaughtered before adulthood. (7,9) Backyard flocks represent only a small fraction of reported cases. In our experience, lesions consistent with Marek's disease have been found in older birds at necropsy.

In this case, the owner did not provide information regarding any new birds that may have been introduced to the flock. All other birds were reportedly healthy. The owner reported that some birds had died several years previously and that the clinical signs were consistent with Marek's disease. The herpesvirus associated with Marek's disease can survive in feather dust for up to 7 months at room temperature, making this case unlikely to be associated with the previous outbreak. (9) How this bird obtained the virus is unclear; however, early infection with latency is suspected. Therefore, the bird may have been exposed to Marek's disease virus before purchase. Based on necropsy results, the bird succumbed to the acute form of the disease as viscera, skin, and nerves were affected. Interestingly, the owner also reported that 3 months before presentation, all birds in the flock suffered from a respiratory infection. None of the birds were treated, and all recovered within a 1-month period. The only bird that continued to show signs of excessive sneezing and occasional nasal discharge was the rooster presented in this report. The authors postulate that Marek's disease caused immunosuppression, even though the bird did not demonstrate any clinical signs of Marek's disease at the time, which is consistent with the reported pathogenesis of the virus. (7)

This case also exemplifies the challenge of diagnosis of Marek's disease in chickens when classic clinical signs are not present. In this instance, coelioscopy did not reveal any gross, visceral abnormalities and pathologic changes were not observed on hepatic, renal, and lung biopsy. This bird had predominantly right-sided neoplastic changes; therefore, it is likely that the gross lesions were missed on coelioscopy because of entry from the left body wall. Additionally, while confirmation of cutaneous lymphoma was obtained after digit amputation, the bird was not showing any signs of limb paresis, muscle atrophy, or systemic disease. Although lymphoid tumors in poultry are typically caused by viral pathogens, we also had to consider a noninfectious cause and possibly, a single lesion. If this were the case, prognosis and treatment would be altered. Interestingly, the owners also reported that they believed the digit wound was associated with a feather follicle. During the viremic stage of Marek's disease, the virions inhabit the feather follicles, resulting in a clinical infection that results in the virus being shed into the environment. (7) Faverolles chickens have feathers along the feet; therefore, the initial lymphoproliferative stage possibly began as a single feather follicle along digit 4.

This case illustrates the variable presentations of Marek's disease and how this disease may not cause death in birds until they reach an older age. Wounds associated with feather follicles should be scrutinized more carefully, and aspirates or skin biopsies performed. While cutaneous lymphoma is a known manifestation of Marek's disease, one may mistakenly not consider this disease as a differential diagnosis because of patient signalment and lack of classic clinical signs. (8,11)

This case was submitted by Alyssa M. Scagnelli, DVM, Nobuko Wakamatsu-Utsuki, DVM, PhD, Dipl ACVP, Dipl ACPV, and Thomas N. Tully, Jr, DVM, MS, Dipl ABVP (Avian), Dipl ECZM (Avian) from the Department of Veterinary Clinical Sciences (Scagnelli, Tully) and the Department of Pathobiological Sciences (Wakamatsu-Utsuki), School of Veterinary Medicine, Louisiana State University, Skip Bertman Drive, Baton Rouge, LA 70803, USA.

References

(1.) Lewandowski A, Campbell T, Harrison G. Clinical chemistries. In: Harrison GJ, Harrison LR. Clinical Avian Medicine and Surgery. Philadelphia. PA: WB Saunders; 1986:192-200.

(2.) Abdi-Hachesoo B, Talebi A, Asri-Rezaei S. Comparative study on blood profiles of indigenous and Ross308 broiler breeders. Glob Vet. 2011;7(3):238-241.

(3.) Villalobos A. Lymphocytic, histiocytic, and related cutaneous tumors. Merck Vet Manual Web site. Updated 2016. Accessed May 14, 2017.

(4.) Rivera S, McClearen J, Reavill DR. Treatment of nonepitheliotropic cutaneous B-cell lymphoma in an umbrella cockatoo (Cacatua alba). J Avian Med Surg. 2009;23(4):294-302.

(5.) Murthy V, Laniesse D, Beaufrere H, et al. What is your diagnosis? Peripheral neuritis secondary to Marek's disease in a chicken. J Avian Med Surg. 2016;30(2):204-208.

(6.) Burgos-Rodriguez AG, Garner M, Ritzman TK, Orcutt CJ. Cutaneous lymphosarcoma in a double yellow-headed Amazon parrot (Amazona ochrocephala oratrix). J Avian Med Surg. 2007;21(4):283-289.

(7.) Payne LN, Venugopal K. Neoplastic diseases: Marek's disease, avian leukosis and reticuloendotheliosis. Rev Sei Tech. 2000;19(2):544-564.

(8.) Liu L, Qu Y, Wang T, et al. Skin involvement in lymphomas caused by Marek's disease virus infection in silkie chickens. J Vet Diagn Investig. 2014; 26(2):302-307.

(9.) Couteaudier M, Denesvre C. Marek's disease virus and skin interactions. Vet Res. 2014;45(36):1-12.

(10.) Witter RL. Avian tumor viruses: persistent and evolving pathogens. Acta Vet Hung. 1997;45(3):251-266.

(11.) Cho KO, Mubarak M, Kimura T, et al. Sequential skin lesions in chickens experimentally infected with Marek's disease virus. Avian Pathol. 1996;25(2): 325-343.

Caption: Figure 1. A 1.5-year-old male Faverolles chicken with a wound encompassing the digit 4 of the right foot. Erythema and edema extended from the digit 4 nail-bed to the tarsometatarsal-phalangeal joint, (a) Additionally, the erythema extended medially involving a small portion of the proximal aspect of digit 3. (b) The laterally oriented image shows the extent of the ulcerated lesion that appeared to extend beyond the epidermis.

Caption: Figure 2. Same bird as described in Figure 1. In comparison to the unaffected left limb, circumferential soft-tissue swelling was associated with the digit 4 of the right pes. The edema is mostly lateralized, as observed in the dorsoventral image, and extended from the distal phalanx to the distal tarsometatarsus. Signs of osseous remodeling are not noted.

Caption: Figure 3. Same bird as described in Figure I. (a) The ulcerated portion of the lesion was found to extend into the dermis, (b) A firm, well-demarcated, white tissue deep to the scab, extended through the soft tissues, coming in close contact with the phalanx.

Caption: Figure 4. Postmortem image of the bird described in Figure 1 showing the extent of the right-sided pathologic lesions. Most coelomic structures have been removed. The testes are bilaterally enlarged, but are asymmetric in that the right testicle is larger and paler in color (white arrow). The right kidney is obscured from the image, as it is replaced by an expansile white mass that extended into the dorsal body wall (bordered by black arrowheads).
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Publication:Journal of Avian Medicine and Surgery
Date:Sep 1, 2018
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