Epidemiological, Clinical and Diagnostic Aspects of Sheep Conidiobolomycosis in Brazil
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Ciência Rural, Santa Maria,Epidemiological, v.46, n.5, p.839-846, clinical mai, and 2016 diagnostic aspects of sheep conidiobolomycosis http://dx.doi.org/10.1590/0103-8478cr20150935 in Brazil. 839 ISSN 1678-4596 MICROBIOLOGY Epidemiological, clinical and diagnostic aspects of sheep conidiobolomycosis in Brazil Aspectos epidemiológicos, clínicos e de diagnóstico da conidiobolomicose ovina no Brasil Carla WeiblenI Daniela Isabel Brayer PereiraII Valéria DutraIII Isabela de GodoyIII Luciano NakazatoIII Luís Antonio SangioniI Janio Morais SanturioIV Sônia de Avila BottonI* — REVIEW — ABSTRACT As lesões da conidiobolomicose normalmente são de caráter granulomatoso e necrótico, apresentando-se sob duas formas Conidiobolomycosis is an emerging disease caused clínicas: rinofacial e nasofaríngea. O presente artigo tem como by fungi of the cosmopolitan genus Conidiobolus. Particular objetivo revisar as principais características da doença em ovinos, strains of Conidiobolus coronatus, Conidiobolus incongruus and particularizando a epidemiologia, assim como os aspectos clínicos Conidiobolus lamprauges, mainly from tropical or sub-tropical e o diagnóstico das infecções causadas por Conidiobolus spp. no origin, cause the mycosis in humans and animals, domestic or Brasil. Neste País, a enfermidade é endêmica nas regiões nordeste wild. Lesions are usually granulomatous and necrotic in character, e centro-oeste, afetando ovinos predominantemente de raças presenting two clinical forms: rhinofacial and nasopharyngeal. deslanadas, ocasionando a morte na grande maioria dos casos This review includes the main features of the disease in sheep, with estudados. As espécies do fungo responsáveis pelas infecções an emphasis on the epidemiology, clinical aspects, and diagnosis em ovinos são C. coronatus e C. lamprauges e a forma clínica of infections caused by Conidiobolus spp. in Brazil. In this country, predominante é a nasofaríngea. Tais infecções fúngicas são the disease is endemic in the Northeast and Midwest, affecting muito importantes, uma vez que comprometem o status sanitário predominantly woolless sheep breeds and occasioning death do rebanho ovino e acarretam sérios prejuízos econômicos à in the majority of the studied cases. The species responsible for ovinocultura. Dessa forma, pesquisas são necessárias para infections of sheep are C. coronatus and C. lamprauges and the investigar ferramentas rápidas de diagnóstico e métodos eficazes predominant clinical presentation is nasopharyngeal. These fungal de controle e tratamento da conidiobolomicose. infections are very important, since they compromise the health status of the sheep flock and cause serious economic losses to the Palavras-chave: micose, ovino, zigomicose, Conidiobolus spp. sheep industry. Thus, research is needed to investigate faster tools for diagnosis and effective methods for the control and treatment of conidiobolomycosis. INTRODUCTION Key words: Fungal infection, ovine, zygomycosis, Conidiobolus spp. Conidiobolomycosis is considered an RESUMO emerging disease caused by several species of fungi of the cosmopolitan genus Conidiobolus in phylum Conidiobolomicose é uma enfermidade emergente Entomophthoromycota. The latter in one of six causada por fungos cosmopolitas do gênero Conidiobolus. major phylogenetic lineages recognised among the Isolados de Conidiobolus coronatus, Conidiobolus incongruus e Conidiobolus lamprauges, principalmente de origem tropical former phylum Zygomycota (GRIGANSKI et al., e subtropical, afetam humanos, animais domésticos e silvestres. 2013). Pathogenic Conidiobolus species infects IPrograma de Pós-graduação em Medicina Veterinária (PPGMV), Departamento de Medicina Veterinária Preventiva (DMVP), Centro de Ciências Rurais (CCR), Universidade Federal de Santa Maria (UFSM), Santa Maria, RS, Brasil. IIDepartamento de Microbiologia e Parasitologia, Instituto de Biologia, Campus Universitário Capão do Leão, Universidade Federal de Pelotas (UFPEL), Pelotas, RS, Brasil. IIILaboratório de Microbiologia Veterinária e Biologia Molecular, Universidade Federal de Mato Grosso (UFMT), Cuiabá, MT, Brasil. IVLaboratório de Pesquisas Micológicas, Departamento de Microbiologia e Parasitologia, Universidade Federal de Santa Maria (UFSM), Av. Roraima, 1000, 97105-900, Santa Maria, RS, Brasil. E-mail: [email protected]. *Corresponding author. Received 06.27.15 Approved 10.30.15 Returned by the author 03.04.16 CR-2015-0935.R2 Ciência Rural, v.46, n.5, mai, 2016. 840 Weiblen et al. human beings (TADANO et al., 2005;MICHAEL shows two clinical manifestations: rhinofacial and et al., 2009; KIMURA et al., 2011; BACHELET nasopharyngeal infection (SILVA et al., 2007a,b; et al., 2014) as well as various species of domestic RIET-CORREA et al., 2008). In recent years, there and wild animals (Table 1). The majority of is an increasing number of case reports of disease Conidiobolus are non-pathogenic saprobes affecting woolless sheep flocks in Brazil, especially or opportunistic pathogens of arthropods and in the Northeast and Midwest regions (Table 2). This occur worldwide, but Conidiobolus coronatus, fact evidences that the epidemiological conditions Conidiobolus incongruus and Conidiobolus in the country are favorable for proliferation and lamprauges are the most frequent etiological maintenance of the fungus in the environment. agents of the conidiobolomycosis. Their pathogenic Brazilian sheep industry is becoming strains occur mainly in tropical and subtropical increasingly widespread and it is characterized by regions, in areas of high humidity, particularly in two aspects of production, including meat and skin Africa (EL-SHABRAWI et al., 2014); however, (mainly the Northeast region) and meat and wool cases have been reported worldwide (Table 1), (especially in the South region) (IBGE, 2002). The including Brazil (Table 2). conidiobolomycosis in sheep flocks compromises the Conidiobolomycosis is characterized health status of the herd and causes economic losses by granulomatous and necrotic lesions and it to sheep breeding, since mortality and lethality rates Table 1- Reported cases of conidiobolomycosis in animal species from outside Brazil. Number of Country/Year of disease Species Organism Site of infection Outcome Reference affected hosts occurrence or reported 1 United States/1994 Conidiobolus spp. Skin D 1 1 United States/1996 Conidiobolus spp. Oral R 2 Dog 1 United States/2006 Conidiobolus spp. Pulmonary R 3 1 United States/2014 C. incongruus Pulmonary D 4 1 Australia/1997 C. incongruus Disseminated D 5 Deer 1 United States/2009 C. incongruus Disseminated D 6 1 United States/1989 C. lamprauges Nasopharyngeal D 7 1 United States/1996 C. coronatus* Nasopharyngeal D 8 Horse 1 United States/2001 C. coronatus Granulomatous tracheitis R 9 1 United States/2001 C. coronatus Nasopharyngeal R 10 2 United States/2003 C. coronatus Nasopharyngeal R 11 Nodular dermatosis in 1 United States/1992 C. coronatus RI 12 external nares/Respiratory Llama Granulomatous dermatitis 1 United States/1994 C. coronatus D 13 and nasal commitment Non human 1 United States/1982 Conidiobolus spp.* Disseminated D 14 primates 700 Australia/1992 C. incongruus Rhinofacial D 15 Rhinofacial (n=1) and 5/200 Australia/1992 C. incongruus D 16 Sheep Rhinocerebral (n=4) 1/60 Trinidad/2001 Conidiobolus spp. Rhinocerebral D 17 1HILLIER et al. (1994), 2BAUER et al. (1997), 3HAWKINS et al. (2006), 4MACKEY et al. (2015), 5STEPHENS & GIBSON (1997), 6MADSON et al. (2009), 7HUMBER et al. (1989), 8ZAMOS et al. (1996), 9STEIGER & WILLIAMS (2000), 10ROBINSON et al. (2007), 11TAINTOR et al. (2004), 12MOLL et al. (1992), 13FRENCH & ASHWORTH (1994), 14MIGAKI & TOFT (1982), 15CARRIGAN et al. (1992), 16KETTERER et al. (1992), 17MORRIS et al. (2001). D=Died. R=Recovered. RI=Remaining infection. *Case was not confirmed with culture. Ciência Rural, v.46, n.5, mai, 2016. Epidemiological, clinical and diagnostic aspects of sheep conidiobolomycosis in Brazil. 841 reach 100% (SILVA et al., 2007a,b; RIET-CORREA Entomophthorales order (GRIGANSKI et al., 2013). et al., 2008, MENDONÇA et al., 2012; AGUIAR et Morphologically, Conidiobolus spp. have hyaline, al., 2014). These issues justify the concern about the coenocytic hyphae or shorter hyphal bodies, although occurrence of the disease in Brazilian sheep herds. septa may be more infrequentthanl the older parts of Thus, this review describes the main epidemiological the mycelium (CHAYAKULKEEREE et al., 2006). and clinical features, as well as the diagnostic methods Rounded dilations are often seen at the ends of hyphae relevant to conidiobolomycosis in sheep in Brazil. and these enlargements have been also described in case of conidiobolomycosis (KETTERER et Etiological agents al., 1992; SILVA et al., 2007b, BOABAID et al., Conidiobolus genus belongs to the 2008). These fungi are characterized by producing kingdom Fungi, Phylum Entomophthoramycota and asexual spores, which are relatively large globose Table 2- Epidemiological and clinical aspects of ovine conidiobolomycosis outbreaks reported in Brazil, 1979-2014. Climatic condition of State/year of Affected Total of Conidiobolus Clinical form Lethality % Breed the region Reference disease occurrence sheep (n) sheep (n) species (month of the year)* MG/1979 NI 3 NI NI SI/MN NI Conidiobolus spp. 1 PB/2001 Rhinofacial 5 80 100 SI Feb-May Conidiobolus spp. 2 157 (2002) 6380 (2002) 100 SI/MN Apr-Jun C. coronatus 3 152 (2003) 6115 (2003) 212 (2004) 6086 (2004) PI/2002/2003/2004 Nasopharyngeal 173.66 6194 (mean (average of of exposed number