Assessing the relationship between Malassezia and leishmaniasis in dogs with or without skin lesions

https://doi.org/10.1016/j.actatropica.2008.04.008Get rights and content

Abstract

The relationship among the frequency, population size and phospholipase activity of Malasseziapachydermatis was investigated for dogs with Leishmania infantum infection (Li+) and those without evidence of this infection (Li). A group of 188 dogs (141 without and 47 with skin lesions) was examined clinically, and samples were taken for the detection of Malassezia and L. infantum using various diagnostic methods. Malassezia was cultured from skin samples from 101 (53.7%) dogs and classified biochemically and molecularly as M. pachydermatis. A significantly higher mean population size of M. pachydermatis was cultured from the skin of L+ dogs compared with L dogs. For M. pachydermatis, most phospolipase-producing cultures and the highest phospholipase activity were recorded for L dogs with lesions and L+ dogs without lesions. The results showed that M. pachydermatis was a common commensal on dogs with or without L. infantum infection and established that L. infantum infection in dogs without skin lesions was associated with increased growth of M. pachydermatis and production of phospholipase in vitro.

Introduction

Species of Malassezia are lipophilic yeasts of the “normal cutaneous” microflora of most warm-blooded animals and sometimes act as opportunistic pathogens (Chen and Hill, 2005). Twelve species (Malassezia dermatis, Malassezia furfur, Malassezia globosa, Malassezia japonica, Malassezia nana, Malassezia obtusa, Malassezia restricta, Malassezia slooffiae, Malassezia sympodialis, Malassezia yamatoensis, Malassezia caprae and Malassezia equina) have been recognized to be lipid dependent, whereas Malassezia pachydermatis does not require lipid supplementation for growth in vitro (Guèho et al., 1996, Guillot et al., 1996, Sugita et al., 2002, Sugita et al., 2004, Hirai et al., 2004, Cabañes et al., 2007). Most of the lipid dependent species have been isolated from “normal” or “diseased” human skin, whereas M. pachydermatis from the skin and/or mucosa of birds and mammals (including dogs and cats) with dermatitis and otitis externa (Guèho et al., 1998, Gupta et al., 2004). The frequency and population size of M. pachydermatis can vary markedly between dogs with and those without skin lesions, depending on anatomical site, usually being larger on affected compared with healthy skin sites (Guillot and Bond, 1999, Bensignor et al., 2002, Cafarchia et al., 2005a, Cafarchia et al., 2005b). Yeast overgrowth at particular anatomical sites seems to influence the occurrence and extent of skin lesions (Cafarchia et al., 2005a, Chen and Hill, 2005), and several conditions (i.e., immune and endocrine disorders) or diseases (e.g., parasitic infections) may impair the “barrier function” of the skin (Chen and Hill, 2005), thus favouring Malassezia overgrowth on animals. It appears that the pathogenesis of Malassezia-dermatitis is related to various enzymes produced (e.g., lipases, lipoxygenase and/or zymogen) that might cause immunopathological changes in the skin of infected dogs (Chen and Hill, 2005). In particular, it has been proposed that phospholipases of M. pachydermatis could be linked to the occurrence of cutaneous lesions in dogs (Cafarchia and Otranto, 2004). Skin lesions in dogs can also be caused by several other pathogens, including species of bacteria, viruses, fungi and/or parasites (Grant, 1991).

In particular, the protozoan parasite Leishmania infantum causes an important, usually chronic disease (Ciaramella et al., 1997, Brachelente et al., 2005) which is transmitted via the bite of an infected plebotomine sandfly (Gramiccia and Gradoni, 2005, Paradies et al., 2006, Otranto et al., 2007), and is zoonotic (Gramiccia and Gradoni, 2005). In dogs, the clinical forms of leishmaniasis (cutaneous, mucocutaneous and visceral) can relate to severe or fatal cases, although asymptomatic forms appear to occur in approximately half of infected dogs (Ciaramella et al., 1997). The pathogenic effects are due to the immunopathological responses against the replicating parasite (amastigotes) within macrophages in or around the site of the sandfly bite. Depending in host immune responses, the parasite can disseminate systemically, replicate within mononuclear phagocytes of the reticuloendothelial system (RES) and simultaneously or subsequently cause visceral disease (Ciaramella et al., 1997). Clinically, the cutaneous form is typified by dry, exfoliative dermatitis, erythema with ulceration and/or diffuse or periorbital alopecia (Ciaramella et al., 1997, Solano-Gallego et al., 2004). Cutaneous leishmaniasis is relatively prevalent in dogs in a number of countries of the Mediterranean basin, South America and the Far East (Gradoni et al., 1996). In Italy, the prevalence of canine leishmaniasis can vary from 1.7 to 48.4%, with a mean seroprevalence of 24.7% in southern regions (Otranto et al., 2007).

Recently, based mainly on clinical, microbiological and biochemical evidence (Bensignor et al., 2002, Cafarchia and Otranto, 2004, Cafarchia et al., 2005a, Cafarchia et al., 2005b, Chen and Hill, 2005), a number of authors (Guillot and Bond, 1999, Chen and Hill, 2005) have proposed that Malassezia species (e.g., M. pachydermatis) can interact biochemically or molecularly with other pathogens to exacerbate clinical signs in the skin. However, to date, there has been limited investigation of this aspect. Given the clinical significance of cutaneous leishmaniasis in dogs as well as the zoonotic importance of this disease, we focused herein on evaluating, using a combined clinical–microbiological–epidemiological approach, whether there is a relationship between Malassezia species and L. infantum. Specifically, the aim of the study was to assess whether there is an association between the frequency, population size and phospholipase activity of Malassezia species and the presence of L. infantum in dogs with or without skin lesions.

Section snippets

Study area and dogs

The present study was conducted from October 2006 to March 2007 in the Apulia region of southern Italy (latitude 42° and 39° North, longitude 15° and 18° East) in which canine leishmaniasis is endemic (Otranto et al., 2007). Dogs (n = 188) were examined clinically for skin lesions and grouped as follows: 141 healthy dogs without skin lesions with no history of skin or ear diseases in the preceding 7 months; 47 dogs with skin lesions (of which 38 dogs had dry, exfoliative dermatitis and/or

Results

Of 188 dogs tested, 65 (34.6%) were positive for L. infantum infection in at least one of the three diagnostic tests. Of the dogs without skin lesions, 42 (29.7%) tested positive for L. infantum; of the dogs with skin lesions, 23 (48.9%) were test positive for this parasite. Of the same 188 dogs, 101 (53.7%) were test positive for Malassezia for at least one anatomical site. In total, 651 isolates were collected from the 188 dogs and identified biochemically as M. pachydermatis. Table 1 lists

Discussion

The results of the present study provide evidence that M. pachydermatis is a common commensal on the skin of dogs, irrespective of the inferred infection status with L. infantum, as there was no statistically significant difference in the prevalence of M. pachydermatis between Li+ and Li dogs.

The population size of Malassezia for dogs with skin lesions was smaller than for those without lesions, irrespective of the L. infantum test result (Table 1). This finding suggests that skin disease,

Acknowledgements

The authors thank Drs Dorothee Stanneck and Norbert Mencke for their support. This study was partially funded by Bayer HealthCare, Germany. We are grateful to Giuseppe Menga and Isidoro Grillo for assistance during field work.

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