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Pythium Insidiosum SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH IN VITRO ANTIMICROBIAL ACTIVITY OF VOLATILE ORGANIC COMPOUNDS FROM MUSCODOR CRISPANS AGAINST THE PATHOGENIC OOMYCETE PYTHIUM INSIDIOSUM Theerapong Krajaejun1, Tassanee Lowhnoo2, Wanta Yingyong2, Thidarat Rujirawat2, Suthat Fucharoen3 and Gary A Strobel4 1Department of Pathology, 2Research Center, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok; 3Thalassemia Research Center, Institute of Molecular Biosciences, Mahidol University, Nakhon Pathom, Thailand; 4Department of Plant Sciences, Montana State University, Bozeman, MT, USA Abstract. Pythium insidiosum is an oomycete capable of causing a life-threatening disease in humans, called pythiosis. Conventional antifungal drugs are ineffec- tive against P. insidiosum infection. A synthetic mixture of the volatile organic compounds (VOCs) from the endophytic fungus Muscodor crispans strain B23 demonstrates antimicrobial effects against a broad range of human and plant pathogens, including fungi, bacteria, and oomycetes. We studied the in vitro ef- fects of B23 VOCs against 25 human, 1 animal, and 4 environmental isolates of P. insidiosum, compared with a no-drug control. The B23 synthetic mixture, at amounts as low as 2.5 µl, significantly reduced growth of allP. insidiosum isolates by at least 80%. The inhibitory effect of the B23 VOCs was dose-dependent. The growth of all isolates was completely inhibited by a dose of 10.0 µl of B23 VOCs, and all isolates were killed by a dose of 20.0 µl. Synthetic B23 VOCs of M. crispans had inhibitory and lethal effects against all P. insidiosum isolates tested. Further studies are needed to evaluate this mixture for treatment of pythiosis. Keywords: pythiosis, Pythium insidiosum, oomycete, in vitro susceptibility, Mus- codor crispans, endophytic fungus INTRODUCTION oomycete Pythium insidiosum (Mendoza et al, 1996). P. insidiosum belongs to the Pythiosis is a life-threatening infec- Stramenopiles of the supergroup Chro- tious disease caused by the pathogenic malveolates, and is the only Pythium species known to infect both humans and Correspondence: Dr Theerapong Krajaejun, animals living in tropical and subtropical Department of Pathology, Faculty of Medicine, areas of the world (Mendoza et al, 1996; Ramathibodi Hospital, Mahidol University, et al, Rama VI Road, Bangkok 10400, Thailand. Kamoun, 2003; Keeling 2005). The E-mail: [email protected] microorganism has two forms: branching Gary A Strobel, PhD, Department of Plant hyphae and a mobile zoospore (Mendoza Sciences, Montana State University, Bozeman, et al, 1993). The zoospore is an infective MT, USA. unit that invades host tissue. Although, E-mail: [email protected] P. insidiosum has similar morphological 1474 Vol 43 No. 6 November 2012 EFFECT OF VOCS AGAINST P. INSIDIOSUM features to filamentous fungi, it is more of the disease (Pracharktam et al, 1991; phylogenically related to diatoms and Badenoch et al, 2001; Grooters and Gee, algae than to true fungi (Kwon-Chung, 2002; Krajaejun et al, 2002; Jindayok et al, 1994). 2009; Keeratijarut et al, 2009; Krajaejun Pythiosis was first described in ani- et al, 2009; Supabandhu et al, 2009). mals a century ago (Smith, 1884; de Haan Conventional antifungal drugs are and Hoogkamer, 1901). Its ability to cause generally ineffective in eradicating the disease in human was described in 1986 infection. An immunotherapy using the (Thianprasit, 1986). In the past decade, P. insidiosum protein extract demonstrated pythiosis has been increasingly diagnosed unfavorable treatment response, with dis- in humans and animals (Tabosa et al, 2004; ease clearance rates of ~50% for humans, Bosco et al, 2005; Mendoza and Newton, ~30% for dogs, and ~60% for horses with 2005; Rakich et al, 2005; Rivierre et al, 2005; pythiosis (Mendoza and Newton, 2005; Krajaejun et al, 2006; Rodrigues et al, 2006; Krajaejun et al, 2006). Therefore, radical Berryessa et al, 2008; Pesavento et al, 2008; excision of infected tissue or organ has White et al, 2008; Badenoch et al, 2009; become the main treatment option. Most Lekhanont et al, 2009; Neto et al, 2010; vascular pythiosis patients undergo limb Pereira et al, 2010; Tanhehco et al, 2011; amputation, while the majority of ocular Videla et al, 2012). The disease has high patients undergo infected eye removal. morbidity and mortality rates. The clini- Post-operative relapse can occur and can cal manifestations of pythiosis are similar cause further damage or death. Improving to infections caused by some filamentous treatment outcomes for patients suffer- fungi (Mendoza et al, 2004). Under-recog- ing from pythiosis is therefore the most nition of pythiosis may due to clinicians, important healthcare goal. veterinarians and microbiologists being The ineffectiveness of conventional unfamiliar with the disease and its caus- antifungal drugs against P. insidiosum may ative agent. Pythiosis is mostly diagnosed due to the lack of the antifungal drug- in horses and dogs (Mendoza et al, 1996). target: ergosterol biosynthetic pathway Affected animals usually present with (Schlosser and Gottlieb, 1966; Krajaejun cutaneous/subcutaneous infections or et al, 2006). Pythium species are classified gastrointestinal tract infections. Animals as a unique group of microorganisms with pythiosis die if left untreated. In hu- that differ phylogenetically and physio- mans, pythiosis has two common forms: logically from almost all other fungal 1. vascular pythiosis affecting medium- pathogens, which are the usual targets for to-large size arteries resulting in arterial conventional antifungal agents (Kwon- occlusion and 2. ocular pythiosis causing Chung, 1994). There is only one report of corneal ulcers or keratitis (Krajaejun et al, conventional antifungal drugs successful- 2006). Definitive diagnosis of pythiosis is ly treating human patient with pythiosis made by culture, which is an insensitive (Shenep et al, 1998). Many conventional and time-consuming procedure. Serodiag- antifungal drugs from different phar- nostic assays (immunodiffusion, ELISA, macotherapeutic groups (itraconazole, Western blot, immunochromatography, posaconazole, voriconazole, terbinafine, hemagglutination and immunohisto- caspofungin, amphotericin-B, and fluv- logical stain) and PCR-based assays have astatin) have been tested in vitro, alone or been devised to facilitate early detection in combination, against clinical isolates of Vol 43 No. 6 November 2012 1475 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH P. insidiosum (Sekhon et al, 1992; Pereira species) (Mitchell et al, 2010). The use of et al, 2007; Argenta et al, 2008; Cavalheiro synthetic B23 VOCs mimicking the com- et al, 2009a, b; Loreto et al, 2011; Argenta ponents of the native M. crispans mixture et al, 2012). Other agents (ibuprofen, di- revealed compatible and equivalent anti- phenyl diselenide, rifampicin, metronida- microbial effects (Mitchell et al, 2010). The zole, macrolides, and tetracycline antibiot- ingredients of the synthetic B23 VOCs are ics) have been tested against the pathogen on the US Food and Drug Administra- as well (Brown et al, 2008; Cavalheiro tion’s GRAS list of harmless substances et al, 2009b; Loreto et al, 2011, 2012). These (http://www.fda.gov/), making it possible drugs have had no appreciable results, for in vivo therapeutic application in hu- limited fungicidal activity, unachievable mans and animals. In the present study, drug levels in tissue, or no in vivo evalu- we used a radial growth agar plate bioas- ations. Mefenoxam has been shown to say to test the antimicrobial effects of the possess anti-oomycete activity (Brown synthetic B23 VOCs against 25 human, 1 et al, 2008; Hummel et al, 2011). However, animal, and 4 environmental isolates of mefenoxam is a fungicide developed for P. insidiosum. agricultural use and its toxicity in mam- mals, and especially humans, is unclear. MATERIALS AND METHODS There is no administrable formula of this drug for patients, making it inappropri- Microorganisms ate for use in the treatment of pythiosis. Thirty isolates of P. insidiosum were An antimicrobial agent clinically effective obtained from humans (n = 25; isolate ID, against P. insidiosum is still needed. M01-25), the environment (agricultural fields in Thailand; n = 4; isolate ID, M26- Some organic compounds extracted 29), and one animal (mosquito lava; n = from endophytic fungi have been re- 1; isolate ID, M30) (Table 1). The isolates ported to have antimicrobial effects were maintained by subculturing monthly against a variety of pathogens (Strobel on Sabouraud dextrose agar (SDA) con- and Daisy, 2003; Ezra et al, 2004; Mitchell taining 1% (wt/vol) bacto peptone (Becton et al, 2010). Among these is a mixture of Dickinson, Sparks, MD), 2% (wt/vol) dex- volatile organic compounds (VOCs) from trose (HiMedia, Mumbai, India) and 1.5% the Muscodor crispans strain B23, a novel (wt/vol) agar (Becton Dickinson, Sparks, endophytic fungus of Ananas ananassoides MD) and incubated at room temperature (wild pineapple) growing in the Boliv- (~28ºC). ian Amazon Basin (Mitchell et al, 2008, 2010). GC/MS analysis reveals the major M. crispans synthetic B23 VOCs components of this compound include: The synthetic B23 VOCs were pre- propanoic acid, 2-methyl-, methyl ester; pared using the method of Strobel propanoic acid, 2-methyl-; 1-butanol, et al (2001) and Mitchell et al (2010). The 3-methyl-;1-butanol, 3-methyl-, acetate; components of the native B23 VOCs propanoic acid, 2-methyl-, 2-methylbutyl were analyzed using GC/MS techniques ester; ethanol;
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