Wiener Tierärztliche Monatsschrift – Veterinary Medicine Austria 105 (2018)

Clinic for Small Mammals, and Birds1, Small Clinic2, and Department of Pathology3, University of Veterinary Medicine Hannover, Foundation, Germany Lipogranulomatous oophoritis in a Leach´s giant ( leachianus)

S. KOPHAMEL1 , M. LEBENS1, P. GÜNTHER1, P. WOHLSEIN3, C. PUFF3, M. FEHR1,2 and K. MATHES1

received September 18, 2017 accepted January 24, 2018

Keywords: pre-ovulatory follicular Schlüsselwörter: Präovulatorische stasis (POFS), reproductive tract, Follikelstase (POFS), Reproduktions- cystic ovarian disease, ovariectomy, trakt, Ovarialzyste, Ovariektomie, . Reptil.

Summary Zusammenfassung

A three-year-old female in- Lipogranulomatöse Oophoritis tact Leach´s giant gecko bei einem Neukaledonischen () kept Riesengecko (Rhacodactylus for breeding purposes was present- leachianus) ed for mass removal of the right ovary. Six weeks after discharge Ein drei Jahre alter, für die erholte sich der Patient gut. from the hospital, ultrasound and Zucht gehaltener weiblicher Kontrolluntersuchungen inklusive radiography rechecks revealed a Neukaledonischer Riesengecko Ultraschalluntersuchungen bestä- similar morphological alteration on (Rhacodactylus leachianus) wur- tigten dies. Bis zum jetzigen the left ovary and ovariectomy of de zur chirurgischen Entfernung Zeitpunkt, zwei Jahre nach dem the left ovary was also performed. des rechten Ovars aufgrund ei- Eingriff, ist der Gecko weiterhin In both cases, histopathological ner Umfangsvermehrung in die- munter, in guter Körperkondition examination revealed a lipogran- sem Bereich vorgestellt. Sechs und hält sein Gewicht. Nach dem ulomatous oophoritis with cystic Wochen nach dem Eingriff wur- Wissen der Autoren ist eine lipog- changes that may have developed de mittels Röntgen- und Ultra- ranulomatöse, zystische, nicht-in- due to pre-ovulatory follicular sta- schalluntersuchung dieselbe Ver- fektiöse und nicht-neoplastische sis (POFS) related to inappropriate änderung im linken Ovar fest- Oophoritis in dieser Form bisher in husbandry. No infectious agents or gestellt. Daher wurde eine keiner Reptilienspezies beschrie- neoplastic cells were found. The Ovariektomie auch des linken ben worden, obwohl POFS häufig patient recovered well from both Ovars durchgeführt. Hauptbefund in oviparen Echsen auftreten. surgeries. Check-ups including ul- der histopathologischen Unter- trasonographic examination con- suchung war in beiden Fällen firmed that the animal was recov- eine lipogranulomatöse Oophoritis ering successfully. Currently, two mit Zystenbildung, die sich wahr- years post surgery, the gecko re- scheinlich im Zusammenhang mit mains bright and in good body con- einer haltungsbedingten präovula- dition and is maintaining its weight. torischen Follikelstase (POFS) ent- To the best of our knowledge, wickelt hat. Es wurden weder infek- lipogranulomatous, cystic non- tiöse Erreger noch neoplastische inflammatory and non-neoplastic Veränderungen festgestellt. Nach oophoritis has not been described beiden erfolgreichen Operationen

* e-mail: [email protected]

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in any of reptile, although POFS is often reported in oviparous lizards.

Introduction

The popularity of lizards as pets is steadily increasing and reproduc- tive tract diseases in pet reptiles are being diagnosed more frequently (RIVERA, 2008; CRUZ CARDONA et al., 2011; HOCHLEITHNER and HOLLAND, 2014). Infectious diseas- es and neoplastic alterations of the reproductive tract are often asso- ciated with inflammatory disorders (SCHILDGER and HÄFELI, 2003; KNOTEK et al., 2016). However, there are few reports of ovarian in- Fig. 1: The patient: a female Leach´s giant gecko (Rhacodactylus leachianus). / Der Patient: Ein weiblicher Neukaledonischer Riesengecko (Rhacodactylus leachianus). flammations in (LE SOUEF et al., 2015). In non-reptilian species such as humans, granulomatous oophoritis is consid- is the largest oviparous gecko species worldwide and ered to be a relatively uncommon and chronic inflam- belongs to the family . It is naturally re- matory process leading to ovarian tissue destruction. stricted to the islands of . This case Histologically, a lipogranulomatous cystic inflammatory serves to illustrate the clinical signs, diagnostic proce- process is observed (GUPTA and GUPTA, 2015). dures and histopathological findings in an adult female The Leach´s giant gecko (Rhacodactylus leachi- Rhacodactylus leachianus with ovarian changes con- anus), also known as the New Caledonian giant gecko, sistent with a lipogranulomatous oophoritis.

Case description

Medical History

A three-year-old intact female Leach´s giant gecko with a body weight of 280 grams was presented for light tremors as well as lethargy and inappetence for the preceding two weeks (Fig. 1). The tremors had decreased prior to presentation after nine days’ daily administration of cal- cium powder with the diet and could not be observed on initial presenta- tion at the clinic. The animal was individually housed in a 50 x 50 x 90 cm glass terrarium, on clay and pine bark substrate. Food items were offered daily and consisted of Repashy Superfood´s Meal Replacement Powder® and com- Fig. 2: Dorsoventral radiographic image of the female Leach´s giant gecko (Rhacodactylus leachianus) upon presentation. A radio-opaque mass is present in the coelomic cavity (ar- mercially available fruit puree for hu- row). / Dorsoventrale Röntgenaufnahme des weiblichen Neukaledonischen Riesengeckos mans (a variety of purees). In addi- (Rhacodactylus leachianus). Nachweis einer hyperdensen Umfangsvermehrung in der tion, vitamin supplements containing Zölomhöhle (Pfeil). vitamins A, D3 and B2 were provid-

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ed, as was sepia powder. The enclosure was lit by a formed using small vascular clips. The surrounding tis- fluorescent tube; ultra-violet spectrum lighting was not sue, as well as the left ovary and salpinx, had no mac- provided. The humidity was 60 to 70 % and the tem- roscopic abnormalities. Other gross findings included perature in the enclosure ranged from 18 to 27 ºC. The a firm, yellowish liver with a gritty surface texture and gecko had no prior medical conditions, had never been 3 ml brownish coelomic effusion, which was sampled mated and had never laid .

Physical examination, further dia- gnosis and surgical intervention

On physical examination, the an- imal was bright, alert and in good body condition but had a firm and dis- tended coelom. Palpation revealed a well filled gastrointestinal tract, as well as a firm, rounded, nonmova- ble mass in the right caudal coelom. No other abnormalities were detect- ed. Radiographs (settings: Bird S/M 60 cm; 25 kV; 4.2 mAs) revealed a 3 x 2 cm caudo-coelomic mass con- sistent with an alteration of the re- productive tract (Fig. 2). Ultrasonographic findings includ- ed two altered vitellogenic follicles of the right ovary (2.3 x 2 cm and 2 x 1.5 cm; Fig. 3). Whereas one fol- licle was filled with anechogenic flu- id, the follicular cavity of the other Fig. 3: Ultrasonographic image of the female Leach´s giant gecko (Rhacodactylus leachianus), was almost completely occupied by 18 Mhz linear probe, demonstrating the two altered, vitellogenic follicles. / Ultraschallbild an echogenic, homogeneous mass. des weiblichen Neukaledonischen Riesengeckos (Rhacodactylus leachianus), 18 Mhz The examination also revealed an Linearsonde. Darstellung der zwei veränderten vitellogenen Follikel. additional homogeneous coelomic mass with an uneven surface in the right caudal coelomic cavity, in im- mediate proximity to the right ovary and consistent with the radiographic finding. Ovarian disease in conjunc- tion with a pre-ovulatory follicular stasis (POFS) was suspected. The animal was hospitalized for an ovariectomy the next day. The gecko was intended for breeding purposes and the owner therefore requested a unilateral ovariectomy. The patient was premedicated with carprofen (4 mg/kg s.c., Rimadyl®) and pre-anaesthetized with keta- mine (5 mg/kg i.m., Ketasel-5®) and diazepam (1 mg/kg i.m., Lipuro®) in the front legs. Induction and mainte- nance were achieved by 2–5 % iso- flurane (Isofluran CP®). The coelio- tomy revealed a well vascularized Fig. 4: Coeliotomy in a Leach´s giant gecko (Rhacodactylus leachianus) diagnosed ovarian mass that did not seem to with ovarian mass. Right ovary, nodular and well-vascularised mass. / Zöliotomie bei ei- cause compression of other organs nem Neukaledonischen Riesengecko (Rhacodactylus leachianus), bei dem eine ovarielle and was surgically removed (Fig. 4). Umfangsvermehrung diagnostiziert wurde. Rechtes Ovar, grobknotige und hochgradig ge- Unilateral ovariectomy was per- fäßreiche Umfangsvermehrung.

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episodes of physical uneasiness were observed during the month after surgery. Six weeks after discharge from the hospital, similar changes were found on the left ovary by means of ul- trasound and radiography. The gecko´s body weight was 273 g. POFS with cystic ovarian changes was suspected on the left ovary. An additional coeliotomy and unilateral ovariectomy of the remaining ovary was therefore proposed. Prior to surgery, and with the ani- mal already sedated, computed tomography (CT) was performed. The images (16 slice CT; layer thickness 0.72 mm, pitch 0.64 mm, rotation time 0.5 s at 120 kV and 150 mA/s/slice) revealed two 1.5 x 1 cm, one 2.5 x 1.5 cm and one 2.5 x 2.5 cm follicles that were centrally located in the caudal coelom (Fig. 5). The anaesthetic procedure and surgery were conducted in the same manner as the first surgery to remove the left ovary. The patient´s weight after surgery was 239 g. Postoperative care followed the same procedure as for the first operation and recovery was complete and uneventful.

Microbiological and histopathological examinations

The coelomic effusion was processed by the Institute for Microbiology, University of Veterinary Medicine Fig. 5: Computed tomography scan image of the female Leach´s giant Hanover, Germany, following the regular laboratory gecko (Rhacodactylus leachianus). Coronal image, soft tissue window. procedure for detecting both aerobic and anaerobic Four altered layered vittelogenic follicles with different densities and bacteria and yeast species. Several in-house culture sizes are present in the caudal abdomen: two hypoechogenic (thin media were inoculated by fractional smear: chocolate arrows), one showing hyperechogenic structures (thick arrow) and one moderately enlarged (arrowhead). / Computertomographische agar and Kimmig’s agar, Columbia and Gassner agar, Darstellung des weiblichen Neukaledonischen Riesengeckos Staph/Strep selective agar and Hamburg test agar for (Rhacodactylus leachianus). Coronaler Schnitt, Weichteilfenster. Vier fungal culture. Aerobic culture was performed for 48– mehrfach geschichtete vitellogene Follikel unterschiedlicher Dichte 72 h at 30 ºC after processing by enrichment bouil- und Größe im kaudalen Bereich der Zölomhöhle: Zwei hypoechogene lon (Institute for Microbiology, University of Veterinary (dünne Pfeile), einer mit hyperechogenen Strukturen (dicker Pfeil) und Medicine Hanover, Germany). Chocolate agar plates einer mittelgradig vergrößert (Pfeilspitze). were incubated in a microaerophilic atmosphere (5 %

CO2). Neither microbiological nor mycological patho- and submitted for bacterial and fungal culture. The gens could be identified in any culture. The removed coelomic cavity was lavaged with warm, sterile phys- ovaries were fixed in 10 % neutral buffered formalin, iological saline and closed with 5-0 PDS in a simple, paraffin embedded, sectioned at 5 μm and stained continuous everting pattern. with haematoxylin and eosin (HE). Additionally, Ziehl- After surgery, the gecko´s weight was reduced to 261 g. Neelsen’s, Gram’s and Giemsa stains, PAS-reaction Postoperative treatment during the one-week hospitali- and Grocott´s methanamine silver impregnation were zation period included daily pain management with car- performed. profen (4 mg/kg s.c., Rimadyl®) and s.c. fluid therapy with Histopathology of the right ovary revealed multiple sterofundin maintenance fluid (10 ml/kg, Sterofundin cysts demarcated by connective tissue with severe ac- ISO®), butaphosphan and vitamin B12 (100 mg/kg and cumulation of intracellular hyaline proteins (confirmed 0.05 mg/kg; Catosal 10 %®) and 24 % calcium boro- by PAS-reaction) and empty vacuoles consistent with gluconate solution (200 mg/kg, Kalziumborogluconat fat droplets (Fig. 6). No normal ovarian tissue was Infusionslösung®), as well as a single administration of found. Findings in the left ovary included regular imma- vitamin B (10 mg/kg s.c., Be-Complex®) and vitamin C ture follicles with an intact theca interna and a mature (200 mg/kg s.c., Vitamin C®). In addition, chloromycetin follicle with protein accumulation. A cystic mass (40 mg/kg p.o., Chloramphenicol®) was given for seven with lipogranulomatous inflammation was also found, days. The gecko was released from the clinic with in- consisting of macrophage infiltrations with intracellular structions to continue peroral chloromycetin (40 mg/kg hyaline proteins. Cristalloid and solitary empty gap-like p.o., Chloramphenicol®) for two more weeks. No other structures cholesterol were also identified (Fig. 7). No

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infectious agents or neoplastic cells were identified microscopically in ei- ther ovary. Rechecks of the patient (one and four weeks, four months and one and two years later) have not re- vealed any anomalies.

Source of supplies: 5-0 PDS: Ethicon, Norderstedt, Germany; Brilliance CT 16 slice: DS, Philips GMBH, Germany; Butaphosphan and Vitamin B12: Bayer, Leverkusen, Germany; Calcium boro- gluconate solution: WDT, Garbsen, Germany, Carprofen: Pfizer, Berlin, Germany, Chloro- mycetin: Zoetis-Pfizer, Berlin, Germany.; Diazepam: Braun, Aschaffenburg, Germany, Gassner agar: Oxoid Deutschland GmbH, Wesel, Germany; Isoflurane: Henry Schein VET, Hamburg, Germany; Ketamine: Selectavet, Weyarn-Holzolling, Germany; Maintenance fluid sterofundin: Braun, Aschaffenburg, Germany; Radiography Fig. 6: Histopathology of the right ovary of a Leach´s giant gecko (Rhacodactylus leachi- device: Gierth HF 400 A, Gierth X-Ray Int., anus). Segment of an ovarian cyst demarcated by connective tissue (arrowheads) with severe Riesa, Germany; Repashy Superfood´s accumulation of intracellular proteins and empty vacuoles consistent with fat droplets (X). Crested Gecko Meal Replacement Powder: HE, 100x. / Histopathologische Untersuchung des rechten Ovars eines Neukaledonischen Repashy Ventures, Inc., Oceanside, Riesengeckos (Rhacodactylus leachianus). Segment einer ovariellen Zyste mit bindegewe- California; Ultrasound device: Vivid 7 biger Demarkation (Pfeilspitzen) und hochgradige Akkumulation von Proteinen und leeren Dimension; GE Healthcare, Munich; 18 Mhz Vakuolen übereinstimmend mit Fetttröpfchen (X). HE, 100x. linear probe; Vascular clips: Vitaltec Surgical, Plymouth, Massachusetts, USA; Vitamin B: CP-Pharma, Burgdorf, Germany; Vitamin C: Rebopharm, Bocholt, Germany.

Discussion

This clinical case displayed a pathological change that has not previously been reported in this form in reptiles and adds knowledge of re- productive disorders in Leach´s gi- ant geckos. Reproductive disorders in rep- tiles may be related to inadequate husbandry and/or dietary condi- tions, as the reproductive cycle in reptiles is mediated by factors such as the quantity and composition of diet (with disorders often linked to an unvaried, high-caloric diet); am- bient temperature; lighting condi- tions and humidity; the provision Fig. 7: Histopathology of the left ovary of a Leach´s giant gecko (Rhacodactylus leachianus). of a nesting site; and cage mates Segment of an ovarian cyst demarcated by connective tissue (arrows). Lipogranulomatous (SYKES, 2010). As imbalances in inflammation consisting of infiltration of macrophages with intracellular hayline proteins (ar- rowheads) as well as empty vacuoles consistent with fat droplets. and severe extracellu- the reproductive cycle occur, POFS lar accumualtion of lipoproteins (X). HE, 400x. / Histopathologische Darstellung des linken or post-ovulatory stasis (POES) Ovars eines Neukaledonischen Riesengeckos (Rhacodactylus leachianus). Segment einer may develop (CAMPBELL, 2009b). ovariellen Zyste mit bindegewebiger Demarkation (Pfeile). Lipogranulomatöse Entzündung Post-ovulatory egg stasis is con- mit Infiltration von Makrophagen, die neben hyaline Proteine (Pfeilspitzen) auch Fetttröpfchen sidered to be frequent in gekkoidae (optisch leere Vakuolen, X) gespeichert haben. Extrazellulär hochgradige Akkumulation von (HOCHLEITHNER and HOLLAND, Lipoproteinen (X). HE, 400x .

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2014). Clinical signs of reproductive disorders may in- as a side effect of the inflammation of the reproductive clude anorexia, apathy, coelomic distension and/or tract (GARDNER and BARROWS, 2010; CAMPBELL, dyspnoea due to the effect of the space-occupying pro- 2015). Due to the owner´s wish not to perform cess (STACY et al., 2004; BARTEN, 2006). analysis, and as no liver biopsy was taken, it was not As in the present case, diagnostic imaging proce- possible to confirm the diagnosis of hepatic lipido- dures can assist in the diagnosis of pre-ovulatory fol- sis and any inflammatory process and monocytosis, licular stasis, e.g. in determining whether the follicles which is often associated with granulomatous altera- already create a calcified outer shell, which allows tions (CAMPBELL, 2009a; DI GIROLAMO and MANS, the diagnosis of pre-ovulatory stasis to be eliminated 2016), via haematological assessment. (HERNÁNDEZ-DIVERS, 2006; GUMPENBERGER, Based on evidence from birds, cystic ovarian chang- 2017). The techniques are also useful for detecting tu- es may be either congenital or acquired (SCHMIDT, moural growth within the coelomic cavity (JACOBSON, REAVILL and PHALEN, 2015). Acquired changes in 2007). reptiles may develop due to neoplastic growth (STACY POFS is more commonly observed in captive rep- et al., 2004; CRUZ CARDONA et al., 2011) or, as tiles (BACKUES and RAMSAY, 1994). The alteration shown in birds, secondary to a hormonal disruption is defined by retained follicles due to the lack of ovula- (BOWLES, 2002; BOWLES, 2006; HADLEY, 2010). tion, although vitellogenesis has taken place (SYKES, Hormone analysis was not taken into consideration 2010). The condition may result in the resorption of fol- due to the lack of reference data for the species. licles or coelomitis if the follicles rupture or ectopic ovu- Previously reported granulomatous ovarian changes lation occurs (RIVERA, 2008; CRUZ CARDONA et al., in reptiles were mainly caused by specific pathogens. 2011). Ovariectomy is indicated in cases of POFS in A malignant granulosa cell tumour has been observed lizards that show anorexia and lethargic or abnormal in a green iguana (Iguana iguana) (CRUZ CARDONA behaviour (GIBBONS and TELL, 2009). The procedure et al., 2011) and an ovarian papillary cystadenocarci- is useful for preventing coelomitis and is recommend- nomas (STACY et al., 2004) in the same species. In ed by several authors (OROSZ et al., 1992; FUNK, both cases, cystic alterations were also found. The lit- 2002; SCHILDGER and HÄFELI, 2003). For these rea- erature also includes descriptions of fungi or mycobac- sons, and especially owing to the marked changes in teria as the causal agents of granulomatous inflamma- the reproductive tract, surgical therapy was proposed tions (SOLDATI et al., 2004; MITCHELL, 2012). In the in this case. current case, neither the microbiological nor the his- Despite the use of the diagnostic methods described topathological analysis (HE, Ziehl-Neelsen´s, Gram´s, above, it can be difficult to determine whether a female Giemsa and Grocott´s stains, PAS-reaction) identified is undergoing a physiological or a pathological repro- any infectious agents, suggesting that mycobacterio- ductive cycle, as captive lizards may mature at differ- sis, and particularly a mycotic infection, were unlikely ent ages (DE NARDO, 2006). Female Leach´s giant to be the cause of the granulomatous oophoritis. geckos reach sexual maturity by 2.5 to 4 years and/or The literature also contains scattered reports of by 82 g to 140 g (smaller insular and larger mainland reptile oophoritis. In one case, a Duvaucel´s gecko populations, respectively) and in most of their natural (Hoplodactylus duvaucelii) was documented with in- range they usually lay a single clutch, while in captivity fectious oophoritis due to Salmonella enterica spp. they normally lay three clutches per breeding season (LE SOUEF et al., 2015). A chronic oophoritis as- (DE VOSJOLI, FAST and REPASHY, 2003). sociated with a necrotic ovary in a veiled chamele- in captivity may mature at an earlier age, largely be- on (Chamaeleo calyptratus) has also been described cause the husbandry methods are designed to maxi- (KNOTEK, 2014), as has a post-ovulatory stasis as- mize growth for early breeding. sociated with an oophoritis in a Hermann´s tortoise The fact that this animal´s weight was high despite (Testudo hermanni) (HERNÁNDEZ-DIVERS, 2004). a decreased appetite and the finding of a firm, - Non-neoplastic proliferative ovarian alterations, e.g. ish liver suggests that an underlying fatty liver disease ovarian hyperplasia or oophoritis, are usually associ- may have been present, which may have led to the ac- ated with a follicular rupture or an inflammatory pro- cumulation of hyaline proteins and to the reproductive cess, although evidence from birds suggests that ovar- disorder (MARTÍNEZ SILVESTRE, 2013). The fruit pu- ian atresia or atrophy may also be involved (HADLEY, ree provided may not have satisfied the dietary require- 2010). The cause of the granulomatous oophoritis in ments of the species and could have played a part in this case remains speculative, as there was no associ- the development of adiposity. Vitamin E deficiency can ated infection. Our hypothesis is that it may have been also lead to a disorder of lipid metabolism in reptiles caused due to the follicular degeneration. This altera- (DIERENFELD, 1989). However, because of the gap tion may be attributable primarily to the POFS. In addi- in data on the vitamin E need of the species, it is not tion, the apparent heavy weight of the gecko, hyporex- possible to assess the influence of a putative Vitamin ia and the appearance of the liver indicates fatty liver E deficiency in the present case. A coelomic effusion, disease, which in turn may have been caused by an in- as observed in this patient, can be present in reptiles adequate high-caloric and unbalanced diet.

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This is the first report of POFS and lipogranuloma- Conclusion tous oophoritis in a Leach´s giant gecko, and, to the We show that the patient´s history and diet should be best of the authors´ knowledge, the first report of a carefully examined. Diagnostic imaging procedures are non-infectious and non-neoplastic lipogranulomatous useful in formulating a preliminary diagnosis; howev- and cystic oophoritis in a reptile. The case expands the er, a definitive diagnosis is only possible after histolog- current knowledge of reproductive disorders in reptiles ical examination of ovarian tissue. Non-infectious and and highlights the importance both of a comprehensive non-neoplastic ovarian changes should be included in study of the husbandry and of regular examination of the list of differential diagnoses for reproductive disor- females to enable an early diagnosis and increase the ders in reptiles. chances of a successful reproductive outcome.

Fazit für die Praxis: Dieser Fallbericht zeigt, dass ovarielle Veränderungen im Zusammenhang mit Haltungsbedingungen kli- nisch behutsam untersucht werden sollten. Eine vorläufige Diagnose ist durch Bildgebungsverfahren mög- lich, die definitive Diagnose ist jedoch erst durch eine histologische Untersuchung zu bestimmen. Unsere Befunde stellen dar, dass nicht-infektiöse und nicht-neoplastische ovarielle Veränderungen in die Liste der Differentialdiagnosen für Reproduktionsstörungen bei Reptilien ebenfalls aufgenommen werden sollten.

References

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