Granulomatous pneumonia due to pythiosis in captive South American coatis (Nasua nasua)

Pneumonia granulomatosa decorrente de pitiose em quatis sul-americanos (Nasua nasua) de cativeiro

Kalinne S. Bezerra Tarcísio A. Santos Janaina M.A. Rosa Carolina A. Pescador Valeria Dutra Luciano Nakazato David Driemeier Edson M. Colodel About the authors

ABSTRACT:

Pythiosis is an emerging infectious disease affecting captive and free-ranging wild animals. We report granulomatous pneumonia due to Pythium insidiosum in two South American coatis (Nasua nasua), who were found dead without any clinical records. Severe granulomatous pneumonia associated with pleural effusion was revealed in the necropsy. Microscopically, variably sized granulomas and pyogranulomas presented negative hyphae profiles at the periphery of their necrotic cores. Grocott methenamine silver stain highlighted these structures, and immunostain (anti- P. insidiosum) was strongly positive. Molecular analysis by polymerase chain reaction amplified P. insidiosum specific DNA. These findings characterized P. insidiosum as a cause of granulomatous pneumonia in coatis and proved that pythiosis needs to be considered in the differential diagnosis of respiratory diseases affecting this species in endemic areas.

INDEX TERMS:
Granulomatous pneumonia; pythiosis; captive animals; South America; coatis; Nasua nasua; pneumonia; Procyonidae; Pythium insidiosum; Southern coati; Stramenopila

RESUMO:

A pitiose é uma doença infecciosa emergente que afeta animais silvestres de cativeiro e em vida livre. Reportamos dois casos de pneumonia granulomatosa decorrentes da infecção por Pythium Insidiosum em quatis sul-americanos (Nasua nasua), que foram encontrados mortos sem apresentar nenhum quadro clínico prévio. Pneumonia granulomatosa severa associada a efusão pleural foi observada durante a necropsia. Na microscopia, foram observados múltiplos granulomas e piogranulomas de tamanhos variados que continham imagens negativas de hifas na periferia de seus centros necróticos. A coloração de metenamina de prata (Grocott) evidenciou estas estruturas, e a imunomarcação (anti-P. insidiosum) foi fortemente positiva. A análise molecular pela reação de polimerase em cadeia amplificou o DNA específico do P. insidiousum. Estes achados caracterizaram o P. insidiosum como a causa da pneumonia granulomatosa nos quatis e provou que a pitiose deve ser considerada um diagnostico diferencial para outras doenças respiratórias que afetam esta espécie.

TERMOS DE INDEXAÇÃO:
Pneumonia granulomatosa; pitiose; quatis; América do Sul; Nasua nasua; cativeiro; Procynidae; Pythium insidiosum; quati; Stramenopila

Introduction

Pythium insidiosum (kingdom: Stramenopila, phylum: Pseudofungi, class: Oomycetes, order: Pythiales, family: Pythiaceae) is the causative agent of pythiosis and an emerging pathogen in captive and free-ranging wild animals (Wellehan et al. 2004Wellehan J.F., Farina L.L., Keoughan C.G., Lafortune M., Gooters A.M., Mendonza L., Brown M., Terrell S.P., Jacobson E.R. & Heard D.J. 2004. Pythiosis in a dromedary camel (Camelus dromedarius). J. Zoo. Wildl. Med. 35(4):564-568. <http://dx.doi.org/10.1638/03-098> <PMid:15732604>
https://doi.org/10.1638/03-098...
, Buergelt et al. 2006Buergelt C., Powe J. & White T. 2006. Abdominal pythiosis in a Bengal tiger (Panthera tigris tigris). J. Zoo. Wildl. Med. 37(2):186-189. <http://dx.doi.org/10.1638/05-003.1> <PMid:17312799>
https://doi.org/10.1638/05-003.1...
, Pesavento et al. 2008Pesavento P.A., Barr B., Riggs S.M., Eigenheer A.L., Pamma R. & Walker R.L. 2008. Cutaneous pythiosis in a nestling white-faced ibis. Vet. Pathol. 45(4):538-541. <http://dx.doi.org/10.1354/vp.45-4-538> <PMid:18587102>
https://doi.org/10.1354/vp.45-4-538...
, Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
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, Videla et al. 2012Videla R., van Amstel S., O’neill S.H., Frank L.A., Newman S.J., Vilela R. & Mendonza L. 2012. Vulvar pythiosis in two captive camels (Camelus dromedarius). Sabouraudia 50(2):212-224. <http://dx.doi.org/10.3109/13693786.2011.588970> <PMid:21696258>
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). It is commonly known for causing chronic and granulomatous disease in humans and domestic animals, particularly horses. Recently, it has become significant in zoos and feral herds, such as the wild ponies in Chincoteague Island (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
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, Hedgpeth 2018Hedgpeth D. 2018. Wild horse dies of ‘swamp cancer’ at Chincoteague Island, others sickened. Avaialable at < Avaialable at https://www.washingtonpost.com > Accessed mar 16, 2020
https://www.washingtonpost.com...
).

Usually associated with aquatic environments, it can manifest as mild to severe tumor-like masses or ulcerated lesions that can affect any part of the body depending on the species (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
). They can be cutaneous, subcutaneous or gastrointestinal (Tabosa et al. 2004Tabosa I.M., Riet-Correa F., Nobre V.M.T., Azevedo E.O., Reis-Junior J.L. & Medeiros R.M.T. 2004. Outbreaks of pythiosis in two flocks of sheep in northeastern Brazil. Vet. Pathol. 41(4):412-415. <http://dx.doi.org/10.1354/vp.41-4-412> <PMid:15232143>
https://doi.org/10.1354/vp.41-4-412...
, Buergelt et al. 2006Buergelt C., Powe J. & White T. 2006. Abdominal pythiosis in a Bengal tiger (Panthera tigris tigris). J. Zoo. Wildl. Med. 37(2):186-189. <http://dx.doi.org/10.1638/05-003.1> <PMid:17312799>
https://doi.org/10.1638/05-003.1...
, Pesavento et al. 2008Pesavento P.A., Barr B., Riggs S.M., Eigenheer A.L., Pamma R. & Walker R.L. 2008. Cutaneous pythiosis in a nestling white-faced ibis. Vet. Pathol. 45(4):538-541. <http://dx.doi.org/10.1354/vp.45-4-538> <PMid:18587102>
https://doi.org/10.1354/vp.45-4-538...
, Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
). As the disease progresses, the infection can spread to the lungs or other sites (Grooters 2003Grooters A.M. 2003. Pythiosis, lagenidiosis, and zygomycosis in small animals. Vet. Clin. N. Am., Small Anim. Pract. 33(4):695-720. <http://dx.doi.org/10.1016/s0195-5616(03)00034-2> <PMid:12910739>
https://doi.org/10.1016/s0195-5616(03)00...
, Reis et al. 2003Reis J.L. Jr, de Carvalho E.C., Nogueira R.H., Lemos L.S. & Mendoza L. 2003. Disseminated pythiosis in three horses. Vet Microb. 96(3):289-295. <http://dx.doi.org/10.1016/j.vetmic.2003.07.005> <PMid:14559176>
https://doi.org/10.1016/j.vetmic.2003.07...
, Tabosa et al. 2004Tabosa I.M., Riet-Correa F., Nobre V.M.T., Azevedo E.O., Reis-Junior J.L. & Medeiros R.M.T. 2004. Outbreaks of pythiosis in two flocks of sheep in northeastern Brazil. Vet. Pathol. 41(4):412-415. <http://dx.doi.org/10.1354/vp.41-4-412> <PMid:15232143>
https://doi.org/10.1354/vp.41-4-412...
, Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
, Gaddis & Brinkman 2017Gaddis K.L. & Brinkman E.L. 2017. What Is Your Diagnosis? J. Am. Vet. Med. Assoc. 250(11):1231-1233. <http://dx.doi.org/10.2460/javma.250.11.1231>
https://doi.org/10.2460/javma.250.11.123...
). Pneumonia rarely occurs as a primary infection, and seems to have been limited to a single case report of a Central American jaguar among non-domestic species (Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
). As it is a life-threatening condition, an accurate and early diagnosis is critical to improve prognosis (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
). However, unusual presentations like pulmonary pythiosis could be difficult to detect and easily overlooked.

South American coatis, Southern coatis, brown-nosed coatis, or ring-tailed coatis (Nasua nasua) are members of the Procyonidae family and broadly distributed in South America (Desbiez & Borges 2010Desbiez A.L.J. & Borges P.A.L. 2010. Density, habitat selection and observations of South American coati Nasua nasua in the central region of the Brazilian Pantanal wetland. Small Carnivore Conserv. 42:14-18.). Here, we document the first report of pulmonary pythiosis infection in two captive coatis in midwest Brazil.

Materials and Methods

Two coatis, a 1-year-old female (Coati 1) and a 4-month-old male cub (Coati 2), were found dead during the rainy season in an outdoor zoo enclosure at the “Universidade Federal do Mato Grosso” Zoo, Cuiabá, Brazil. The facility had 15 coatis in total, with a history of recurrent territorial and sexual fighting and consequent suppurative cutaneous wounds due to bites. During the wet season, respiratory signs like nasal discharge and respiratory distress occurred sporadically. The Coati 1, presenting a non-healing purulent bite wound on its dorsal part, was hospitalized at the time for suspected pneumonia.

The bodies of Coatis 1 and 2 were submitted for necropsy and samples of all organs were collected and fixed in 10% buffered formalin for routine histopathological processing and hematoxylin and eosin (HE) staining. Special Grocott methenamine silver stains (GMS) stain was performed in the lung to detect negative hyphae profiles, besides immunohistochemistry (IHC) using rabbit polyclonal anti-Pythium insidiosum antibody (non-commercial) (Pesavento et al. 2008Pesavento P.A., Barr B., Riggs S.M., Eigenheer A.L., Pamma R. & Walker R.L. 2008. Cutaneous pythiosis in a nestling white-faced ibis. Vet. Pathol. 45(4):538-541. <http://dx.doi.org/10.1354/vp.45-4-538> <PMid:18587102>
https://doi.org/10.1354/vp.45-4-538...
), and polymerase chain reaction with primers PI-1: 5’-TTCGTCGAAGCGGACTGCT-3’ and PI-2: 5’-GCCGTACAACCCGAGAGTCATA-3’ encoding the sequence ITS1 and rDNA of P. insidiosum (Pesavento et al. 2008Pesavento P.A., Barr B., Riggs S.M., Eigenheer A.L., Pamma R. & Walker R.L. 2008. Cutaneous pythiosis in a nestling white-faced ibis. Vet. Pathol. 45(4):538-541. <http://dx.doi.org/10.1354/vp.45-4-538> <PMid:18587102>
https://doi.org/10.1354/vp.45-4-538...
).

Results

Grossly, Coati 1 and 2 presented unilateral, severe, and chronic granulomatous pneumonia (Fig.1A). The affected lung was greatly enlarged and consolidated, showing numerous coalescent nodular granulomas with yellowish caseous cores (Fig.1B). Coati 1 was emaciated and showed marked subcutaneous thoracic edema, as well as mild mucopurulent nasal flow. In Coati 2, the lung lesions seemed more severe, sometimes presenting a cavernous and lytic pattern. In both cases, a large amount of serofibrinous pleural exudate and multiple points of chronic pleural adherences surrounded the affected lung. Mediastinal lymph nodes were enlarged and embedded among the granulomatous masses.

Fig.1.
Pythium insidiosum infection, coati, lung. (A) The affected left lung was greatly enlarged. (B) Multiple granulomas scattered through the pulmonary parenchyma. (C) A hypha is situated in the necrotic center. GMS, obj.40x. (D) IHC for Pythium insidiosum shows strong immunostaining on the hyphae-like wall. IHC, obj.40x.

Microscopically, the lesions were similar with variable intensity in both the coatis. Lung sections showed multiple coalescing granulomas and pyogranulomas characterized by extensive caseous necrosis associated with a dense collection of epithelioid macrophages, eosinophils, degenerate neutrophils, and a mild number of Langhans cells. There was an outer layer of lymphocytes, plasmocytes, and less reactive macrophages and marked proliferation of fibrous connective tissue. Hemorrhage, fibrin thrombi, and necrotizing vasculitis were frequent, but there was no evidence of angioinvasion. Intensely eosinophilic and radiant amorphous material (Splendore-Hoeppli reaction) was frequently observed in these granulomas. Negative hyphae-like profiles were often seen.

Grocott methenamine silver staining of the lung sections revealed several broad, sparsely septate, and irregularly branched hyphae-like organisms that were 3-7µm in diameter and located predominantly at the Splendore-Hoeppli reaction cores with only a few ones scattered throughout the adjacent areas (Fig.1C). Mediastinal lymph nodes presented lymphoid hyperplasia with marked granulomatous inflammation. The hyphae-like organisms were consistently found in the pulmonary granulomas. There was no angioinvasion or hyphae in the lymphnodes. Hyphae-like organisms were regularly marked using the rabbit polyclonal anti- Pythium insidiosum antibody (non-commercial) (Fig.1D)

Environmental enclosure water, nasal secretions, and a cutaneous punch biopsy of the coati 1 were collected for pathological and epidemiologic investigation. The skin biopsy showed pyogranulomatous dermatitis and granulation tissue. However, hyphae-like organisms were not observed. All samples tested positive by polymerase chain reaction with primers PI-1: 5’-TTCGTCGAAGCGGACTGCT-3’ and PI-2: 5’-GCCGTACAACCCGAGAGTCATA-3’ encoding the sequence ITS1 and rDNA of P.insidiosum as indicated by the amplification fragment 105pb. All attempts of culture and isolation of P. insidiosum from fresh tissues were unsuccessful.

Discussion

Pythiosis is a well-described condition that manifests as a chronic and progressive granulomatous disease. Its etiologic agent, Pythium insidiosum, is a oomycete pathogen frequently associated with tropical or subtropical aquatic environments (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
). Brazil is endemic for this disease and its warm temperatures with long rainy seasons through the year are highly favorable for the growth and proliferation of this pathogen (Tabosa et al. 2004Tabosa I.M., Riet-Correa F., Nobre V.M.T., Azevedo E.O., Reis-Junior J.L. & Medeiros R.M.T. 2004. Outbreaks of pythiosis in two flocks of sheep in northeastern Brazil. Vet. Pathol. 41(4):412-415. <http://dx.doi.org/10.1354/vp.41-4-412> <PMid:15232143>
https://doi.org/10.1354/vp.41-4-412...
, Machado et al. 2016Machado N.G., Biudes M.S., Querino C.A.S., Danelichen V.H.M. & Velasque M.C.S. 2016. Seasonal and interannual pattern of meteorological variables in Cuiabá, Mato Grosso state, Brazil. Revta Bras. Geof. 33(3):1-12. <http://dx.doi.org/10.22564/rbgf.v33i3.949>
https://doi.org/10.22564/rbgf.v33i3.949...
). These cases were unique because the primary site of infection appeared to be the lungs and the presentation occurred in more than one animal from the same group, in contrast to the individual reports described till date (Goad 1984Goad M.E.P. 1984. Pulmonary pythiosis in a horse. Vet. Pathol. 21(2):261-262. <http://dx.doi.org/10.1177/030098588402100224> <PMid:6730214>
https://doi.org/10.1177/0300985884021002...
, Heath et al. 2002Heath J.A., Kiehn T.E., Brown A.E., LaQuaglia M.P., Steinherz L. J., Bearman G., Wong M. & Steinherz P.G. 2002. Pythium insidiosum pleuropericarditis complicating pneumonia in a child with leukemia. Clin. Infect Dis. 35(6):e60-e64. <http://dx.doi.org/10.1086/342303> <PMid:12203186>
https://doi.org/10.1086/342303...
, Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
, Kepler et al. 2017Kepler D., Cole R., Lee-Fowler T., Koehler J., Shrader S. & Newton J. 2017. Pulmonary pythiosis in a canine patient. Vet. Radiol. Ultrasound 60(2):e20-e23. <http://dx.doi.org/10.1111/vru.12516> <PMid:28547920>
https://doi.org/10.1111/vru.12516...
). To the best of our knowledge, this is the first reported case of pythiosis in coatis. This report broadens the spectrum of the disease in non-domestic species. Pythiosis should be included as a differential diagnosis of coatis and zoo animals presenting unspecified respiratory signs or non-healing wounds, especially in endemic regions.

There are very few reports of pulmonary pythiosis. In most cases, it occurs as a consequence of metastatic spread within the progression of the disease in its systemic form, or through aspiration secondary to nasal infection as already described in sheep, horses, and dogs (Reis et al. 2003Reis J.L. Jr, de Carvalho E.C., Nogueira R.H., Lemos L.S. & Mendoza L. 2003. Disseminated pythiosis in three horses. Vet Microb. 96(3):289-295. <http://dx.doi.org/10.1016/j.vetmic.2003.07.005> <PMid:14559176>
https://doi.org/10.1016/j.vetmic.2003.07...
, Tabosa et al. 2004Tabosa I.M., Riet-Correa F., Nobre V.M.T., Azevedo E.O., Reis-Junior J.L. & Medeiros R.M.T. 2004. Outbreaks of pythiosis in two flocks of sheep in northeastern Brazil. Vet. Pathol. 41(4):412-415. <http://dx.doi.org/10.1354/vp.41-4-412> <PMid:15232143>
https://doi.org/10.1354/vp.41-4-412...
, Ubiali et al. 2013Ubiali D.G., Cruz R.A., De Paula D.A, Silva M.C., Mendonça F.S., Dutra V., Nakazato L., Colodel E.M. & Pescador C.A. 2013. Pathology of nasal infection caused by Conidiobolus lamprauges and Pythium insidiosum in sheep. J. Comp. Pathol. 149(2/3):137-145. <http://dx.doi.org/10.1016/j.jcpa.2012.12.002> <PMid:23375916>
https://doi.org/10.1016/j.jcpa.2012.12.0...
).

Pulmonary pythiosis as a primary infection is rare and includes only singular case reports in a horse, human, dog, and captive jaguar until now (Goad 1984Goad M.E.P. 1984. Pulmonary pythiosis in a horse. Vet. Pathol. 21(2):261-262. <http://dx.doi.org/10.1177/030098588402100224> <PMid:6730214>
https://doi.org/10.1177/0300985884021002...
, Heath et al. 2002Heath J.A., Kiehn T.E., Brown A.E., LaQuaglia M.P., Steinherz L. J., Bearman G., Wong M. & Steinherz P.G. 2002. Pythium insidiosum pleuropericarditis complicating pneumonia in a child with leukemia. Clin. Infect Dis. 35(6):e60-e64. <http://dx.doi.org/10.1086/342303> <PMid:12203186>
https://doi.org/10.1086/342303...
, Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
, Kepler et al. 2017Kepler D., Cole R., Lee-Fowler T., Koehler J., Shrader S. & Newton J. 2017. Pulmonary pythiosis in a canine patient. Vet. Radiol. Ultrasound 60(2):e20-e23. <http://dx.doi.org/10.1111/vru.12516> <PMid:28547920>
https://doi.org/10.1111/vru.12516...
). Similar to these coatis, there was no evidence or previous history of wounds or infection at any other site, except in the equine case. This horse previously presented cutaneous pythiosis, but the pulmonary infection was not related to it.

The disease typically involves lesions on parts of the body that have come in contact with warm, stagnant water containing motile zoospores, and infection occurs due to a high tropism that the pathogen has for damaged tissue (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
). In the coati from the group suspected of pneumonia and presenting the skin wound, amplification of the homologous sequence of P. insidiosum occurred. However, no hyphae-like organisms were observed in histological sections of skin biopsy of the affected site, and clinical correlation was not possible.

In these cases, the pulmonary infection most likely occurred through inhalation or ingestion with subsequent aspirations of contaminated water containing the pathogen. The pathogen was detected in a nasal swab from a coati of the same group, which suggests that the possible route was through inhaled aerosolized zoospores as seen in a similar case of a Central American jaguar (Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
)

Clinical signs of localized pulmonary pythiosis are usually non-specific, including chronic coughing, dyspnea, and exercise intolerance, as well as nasal discharge, anorexia, weight loss, decreased appetite, anemia, and hypoproteinemia (Goad 1984Goad M.E.P. 1984. Pulmonary pythiosis in a horse. Vet. Pathol. 21(2):261-262. <http://dx.doi.org/10.1177/030098588402100224> <PMid:6730214>
https://doi.org/10.1177/0300985884021002...
, Heath et al. 2002Heath J.A., Kiehn T.E., Brown A.E., LaQuaglia M.P., Steinherz L. J., Bearman G., Wong M. & Steinherz P.G. 2002. Pythium insidiosum pleuropericarditis complicating pneumonia in a child with leukemia. Clin. Infect Dis. 35(6):e60-e64. <http://dx.doi.org/10.1086/342303> <PMid:12203186>
https://doi.org/10.1086/342303...
, Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
, Kepler et al. 2017Kepler D., Cole R., Lee-Fowler T., Koehler J., Shrader S. & Newton J. 2017. Pulmonary pythiosis in a canine patient. Vet. Radiol. Ultrasound 60(2):e20-e23. <http://dx.doi.org/10.1111/vru.12516> <PMid:28547920>
https://doi.org/10.1111/vru.12516...
). No clinical signs were observed in these two coatis, but their group had a history of respiratory distress and the pathological findings were consistent with these signs. The subcutaneous edema in the female most likely occurred due to hypoproteinemia, as implied by the poor body condition.

The gross and histologic appearance of the lesions of these cases were very similar to those previously described (Martins et al. 2012Martins T.B., Kommer G.D., Trost M.E., Inkelmann M.A., Fighera R.A. & Schild A.L. 2012. A comparative study of the histopathology and immunohistochemistry of pythiosis in horses, dogs and cattle. J. Comp. Pathol. 146(2/3):122-131. <http://dx.doi.org/10.1016/j.jcpa.2011.06.006> <PMid:21824626>
https://doi.org/10.1016/j.jcpa.2011.06.0...
, Ubiali et al. 2013Ubiali D.G., Cruz R.A., De Paula D.A, Silva M.C., Mendonça F.S., Dutra V., Nakazato L., Colodel E.M. & Pescador C.A. 2013. Pathology of nasal infection caused by Conidiobolus lamprauges and Pythium insidiosum in sheep. J. Comp. Pathol. 149(2/3):137-145. <http://dx.doi.org/10.1016/j.jcpa.2012.12.002> <PMid:23375916>
https://doi.org/10.1016/j.jcpa.2012.12.0...
). When infection occurs through metastatic spread along lymphatics, the granulomas are randomly distributed in both lungs in a miliary pattern (Reis et al. 2003Reis J.L. Jr, de Carvalho E.C., Nogueira R.H., Lemos L.S. & Mendoza L. 2003. Disseminated pythiosis in three horses. Vet Microb. 96(3):289-295. <http://dx.doi.org/10.1016/j.vetmic.2003.07.005> <PMid:14559176>
https://doi.org/10.1016/j.vetmic.2003.07...
, Tabosa et al. 2004Tabosa I.M., Riet-Correa F., Nobre V.M.T., Azevedo E.O., Reis-Junior J.L. & Medeiros R.M.T. 2004. Outbreaks of pythiosis in two flocks of sheep in northeastern Brazil. Vet. Pathol. 41(4):412-415. <http://dx.doi.org/10.1354/vp.41-4-412> <PMid:15232143>
https://doi.org/10.1354/vp.41-4-412...
, Ubiali et al. 2013Ubiali D.G., Cruz R.A., De Paula D.A, Silva M.C., Mendonça F.S., Dutra V., Nakazato L., Colodel E.M. & Pescador C.A. 2013. Pathology of nasal infection caused by Conidiobolus lamprauges and Pythium insidiosum in sheep. J. Comp. Pathol. 149(2/3):137-145. <http://dx.doi.org/10.1016/j.jcpa.2012.12.002> <PMid:23375916>
https://doi.org/10.1016/j.jcpa.2012.12.0...
). When pythiosis is restricted to the lungs, the lesions tend to be more localized and form a large and compact mass containing multiple granulomas, as observed in the coatis of our report. The unilateral pulmonary consolidation seen here was also observed in the jaguar case (Camus et al. 2004Camus A.C., Grooters A.M. & Aquilar R.F. 2004. Granulomatous pneumonia caused by Pythium insidiosum in a central American jaguar, Panthera onca. J. Vet. Diagn. Invest. 16(6):567-571. <http://dx.doi.org/10.1177/104063870401600612> <PMid:15586573>
https://doi.org/10.1177/1040638704016006...
). However, “kunkers”, characteristic of the equine pythiosis, were not observed (Gaastra et al. 2010Gaastra W., Lipman L.J., De Cock A.W., Pege R.B., Scheurwater J., Vilela R. & Mendonza L. 2010. Pythium insidiosum: an overview. Vet. Microbiol. 146(1/2):1-16. <http://dx.doi.org/10.1016/j.vetmic.2010.07.019> <PMid:20800978>
https://doi.org/10.1016/j.vetmic.2010.07...
).

Microscopically, the eosinophilic pattern of necrosis was predominant and similar to that described in horses and sheep (Grooters 2003Grooters A.M. 2003. Pythiosis, lagenidiosis, and zygomycosis in small animals. Vet. Clin. N. Am., Small Anim. Pract. 33(4):695-720. <http://dx.doi.org/10.1016/s0195-5616(03)00034-2> <PMid:12910739>
https://doi.org/10.1016/s0195-5616(03)00...
, Martins et al. 2012Martins T.B., Kommer G.D., Trost M.E., Inkelmann M.A., Fighera R.A. & Schild A.L. 2012. A comparative study of the histopathology and immunohistochemistry of pythiosis in horses, dogs and cattle. J. Comp. Pathol. 146(2/3):122-131. <http://dx.doi.org/10.1016/j.jcpa.2011.06.006> <PMid:21824626>
https://doi.org/10.1016/j.jcpa.2011.06.0...
, Ubiali et al. 2013Ubiali D.G., Cruz R.A., De Paula D.A, Silva M.C., Mendonça F.S., Dutra V., Nakazato L., Colodel E.M. & Pescador C.A. 2013. Pathology of nasal infection caused by Conidiobolus lamprauges and Pythium insidiosum in sheep. J. Comp. Pathol. 149(2/3):137-145. <http://dx.doi.org/10.1016/j.jcpa.2012.12.002> <PMid:23375916>
https://doi.org/10.1016/j.jcpa.2012.12.0...
). Non-eosinophilic granulomatous infiltrate is more common in cattle and was also present in these cases, but only sporadically (Martins et al. 2012Martins T.B., Kommer G.D., Trost M.E., Inkelmann M.A., Fighera R.A. & Schild A.L. 2012. A comparative study of the histopathology and immunohistochemistry of pythiosis in horses, dogs and cattle. J. Comp. Pathol. 146(2/3):122-131. <http://dx.doi.org/10.1016/j.jcpa.2011.06.006> <PMid:21824626>
https://doi.org/10.1016/j.jcpa.2011.06.0...
). Despite the presence of severe necrotizing vasculitis within fibrin thrombus in many areas of the pulmonary parenchyma, there was no evidence of hyphae vascular invasion or hematogenous spread to other organs.

While the diagnosis is quite non-specific based only on the histopathological examination, these morphological findings narrow the range of possible etiologic agents to P. insidiosum, zygomycetes, and Lagenidium species. Lagenidium spp. primarily affects dogs, and it has been reported in cats and humans. The differential diagnosis between these infections is essential, because they are morphologically similar but differ in the epidemiology, choice of therapy, and prognosis (Grooters 2003Grooters A.M. 2003. Pythiosis, lagenidiosis, and zygomycosis in small animals. Vet. Clin. N. Am., Small Anim. Pract. 33(4):695-720. <http://dx.doi.org/10.1016/s0195-5616(03)00034-2> <PMid:12910739>
https://doi.org/10.1016/s0195-5616(03)00...
, Ubiali et al. 2013Ubiali D.G., Cruz R.A., De Paula D.A, Silva M.C., Mendonça F.S., Dutra V., Nakazato L., Colodel E.M. & Pescador C.A. 2013. Pathology of nasal infection caused by Conidiobolus lamprauges and Pythium insidiosum in sheep. J. Comp. Pathol. 149(2/3):137-145. <http://dx.doi.org/10.1016/j.jcpa.2012.12.002> <PMid:23375916>
https://doi.org/10.1016/j.jcpa.2012.12.0...
).

Conclusions

The anatomopathological changes, histologic and molecular findings show that Pythium insidiosum is the cause of granulomatous pneumonia in these coatis.

Due the non-specific clinical signs, pythiosis needs to be considered in the differential diagnosis of respiratory diseases affecting this species in endemic areas.

Acknowledgements

We extend our gratitude to all the technical and support staff of the “Universidade Federal de Mato Grosso” Zoo for providing the field data.

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Publication Dates

  • Publication in this collection
    23 Oct 2020
  • Date of issue
    Aug 2020

History

  • Received
    16 Mar 2020
  • Accepted
    20 Apr 2020
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