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Original Article Pathogenic Fungal Species Associated with Digestive System of americana (Blattaria: ) Trapped from Residential Dwellings in Ahvaz City, Southwestern Iran

*Hamid Kassiri 1, Majid Zarrin 2, Rahele Veys-Behbahani 3

1Medical Entomology and Vector Control Department, Health Faculty, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 2Medical Mycology Department, Medicine Faculty, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran 3Student Research Committee, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

(Received 13 May 2016; accepted 24 Jan 2018)

Abstract Background: are the most prevalent domestic pests of a worldwide distribution. They were recognized as possible vectors of pathogenic bacteria, viruses, fungi and parasites in residential dwellings and hospital environ- ments. The present study isolated and identified yeasts and filamentous fungi from digestive tract of American cock- roaches, collected from three different residential regions of Iran. Methods: Seventy cockroaches were sampled using direct collection (hand catch), vacuum cleaner and sticky traps in Ahvaz, Iran in 2009–2010. Their medically important fungal microorganisms were isolated from digestive tract using standard mycological methods. Filamentous fungi were identified by macroscopic and microscopic examina- tion. Yeasts were identified by API ID32C-32100 kit. Results: A high percentage of cockroaches (88.6%) were detected to carry fungi of medical importance. Overall, 23 fungi species/genera were isolated from the American cockroaches' alimentary tract. The fungi isolated from cock- roaches, from the residential regions were species of Aspergillus, Rhizopus, Penicillium, Mucorales, Alternaria, Cladosporium, Mycelia, Chrysosporium, Candida, Rhodotorula, Zygosaccharomyces, and Debaryomyces. Candida spp. (41.4%), Aspergillus spp. (37.1%) and Rhodotorula spp (27.1%) were the most common fungi recovered on cockroaches. Candida albicans and Candida glabrata were the commonest species of the genus Candida. In addi- tion, Aspergillus niger and A. flavus were the most frequent species of the genus Aspergillus. Conclusion: American cockroaches may carry pathogenic fungi in the urban areas of Ahvaz.

Keywords: Periplaneta americana, American , Residential environments, Fungal flora, Isolation

Introduction

Cockroaches are distinguished by the sub- are associated with human dwellings (1, 2). sequent characteristics: wings and tarsus, re- House cockroaches such as American cock- productive organs, head frontal, shape and the roach, Periplaneta Americana (: Blat- number of spines on the femora and color. They tidae), German cockroach, Blattella germanica comprise five families of (Blat- (Blattodea: Ectobiidae), brown-banded cock- tellidae), , Cryptocercidae, Blattidae roach, Supella logipalpa (Blattodea: Ectobi- and Corydiidae (Polyphagidae) (1). Cockroach- idae) and Oriental cockroach, orientalis es can be detected in a broad range of sur- (Blattodea: Blattidae) are found frequently in roundings all over the globe, particularly in Iran (2). A number of faunistic studies of cock- tropical and subtropical areas. More than 4500 roaches in the human dwellings of Iran showed species are reported from different parts of the that B. germanica as the most frequent species world. They are one of the most generally followed by P. americana (3, 4). American and prominent household pests and about 30 species German cockroaches, respectively, were intro- 16 *Corresponding author: Dr Hamid Kassiri, E-mail: http://jad.tums.ac.ir [email protected] Published Online: March 18, 2018 www.SID.ir

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duced as the prevalent species in human res- ican cockroaches' digestive system and iden- idential habitats (5). The German cockroach, tified. which is approximately 15mm (0.59inch) long and the American cockroach, approximately Materials and Methods 30mm (1.2inches) long (2, 6).

Cockroaches are able to transfer fungi, bac- This research was carried out in Ahvaz teria, viruses, parasites and other medically sig- (31°192 133 N 48°402 093 E) as a part of the nificant pathogenic agents on their body sur- central coordination Khuzestan (31.3273°N faces and in their feces in infectious regions, 48.6940°E), capital of Khuzestan, a south- such as domestic habitats, hospitals, and in- western province of Iran. In this descriptive dustrial areas. From these collected from study, 70 American cockroaches were sam- such environments have been isolated im- pled in Ahvaz, Iran in 2009–2010, from hu- portant pathogenic microorganisms (7–10). man dwelling localities using direct collec- Plentiful pathogenic agents including 2 species tion (hand catch), vacuum cleaner and sticky of protozoans, 15 species of molds and fungi, traps. 32 species of bacteria (such as, Shigella and They were captured from kitchens, toilets Salmonella), 1 virus and 7 helminths which are or bathrooms of residential area. Each cock- damaging to humans being detected in the roach was placed in a single sterile test tube feces, in gut or on cuticle cockroaches (11–13). and transported to the laboratory for identifi- Some fungi have the capacity to distribute cation and processing for fungi examination. via cockroaches (6, 14). It makes them ideal The cockroaches were immobilized by freez- carriers for transferring a number of medically ing at 0 °C for 10min. Each anesthetized cock- important fungi (15, 16). Candida spp., As- roach was examined under the dissecting mi- pergillus spp., Penicillium spp. and other croscope, and the species were identified us- species of fungi have been isolated from cock- ing standard taxonomic keys. After identi- roaches recovered in several healthcare sec- fication, 2ml of sterile normal saline (0.9%) tors of the hospitals (2, 6, 15–17). Aspergil- was added to the test tube and the cock- lus spp. and Candida spp. are the most prev- roaches were vigorously shaken for 2min. alent fungi causing solemn healthcare-asso- After external washing, the cockroaches were ciated infections (18, 19). Aspergillosis is com- washed with 70% ethyl alcohol for 2min. mon in bone marrow transplant recipients and Then the cockroaches transferred to sterilized patients with lung disorders. In immunocom- tubes and allowed to dry. The cockroaches promised patients, obstructive bronchial asper- were then washed twice in sterile normal gillosis, allergic Aspergillus tracheobronchi- saline for 3min to remove traces of alcohol, tis, and pulmonary aspergilloma are reported and the gut was dissected out aseptically. The (20–23). Candida is known as an opportunistic gut was then macerated under aseptic condi- pathogenic agent, due to it can innocuously tions in 2ml of sterile normal saline. The re- colonize the human body (mouth, skin, gen- sulting macerate was cultured on Sabouraud's itourinary tract and gut). Candidiasis can cause dextrose agar with 0.05% chloramphenicol symptoms when a weakened immune system and incubated at 30 °C for 3wk. The differ- or other factors allow it to grow unabated ent yeast and filamentous colonies were dis- (24). To determine the possible role of Amer- tinguished by microscopic and macroscopic ican cockroaches in dissemination of medi- trials. Yeasts were diagnosed by germ tube test, cally important fungi, this study was carried the presence of chlamydoconidia on Corn meal out in residential areas of Iran. Fungi of med- plus Tween 80 agar and by API ID32C-32100 ical importance were isolated from the Amer- system.

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Results

A total of 70 American cockroaches, Peri- were the most molds appeared in the gut of planeta americana were sampled from 3 resi- American cockroaches. dential locations (30, 20 and 20 from Kyanpars, Other medically important mold, Myce- Amaniae and Golestan areas, respectively). lia sterilia, Mucorales spp., Alternaria spp., About 51.4% cockroaches (36/70) carried one Chrysosporium spp. and Cladosporium spp. or more species of medically important molds were rarely isolated from a few American cock- in digestive system and 55.7% (39/70) had one roaches. Among 29 (41.4%) American cock- or more species of medically important yeasts roaches, nine species of Candida were iden- in digestive system. About 88.6% (62/70) tified by mycological tests. Candida albicans cockroaches collected were contaminated with (31%), C. glabrata (10.3%) and C. famata one or more fungi species (mold or yeast). (6.9%) were the greatest species isolated from Overall, 23 species/genera of fungi were iso- cockroaches. Meanwhile, C. parapsilosis, C lated from these areas. The fungi isolated guilliermondi, C. tropicalis, C. krusie, C. lip- from cockroaches in these locations are shown olytica and Candida spp. were detected in in Table 1. In this investigation, Candida spp. the digestive canal in a few ones. Among 26 (74.3%) was the most yeast isolated in the gut (37.1%) American cockroaches, four species of American cockroaches and Rhodotrula spp. of Aspergillus were identified. Aspergillus (48.7%), Zygosaccharomyces spp. (15.4%) and niger (42.3%) was the highest species isolated Debaryomyces polymorphus (2.6%) were the from American cockroaches. Aspergillus flavus, next. In addition, Aspergillus spp. (72.2%), Pen- A. terreus, and Aspergillus spp. were detect- icillium spp. (22.2%) and Rhizopus spp. (13.9%) ed in the digestive canal in a few American cockroaches.

Table 1. Fungi isolated from the digestive system of Periplaneta americana captured in three residential areas, Ahvaz city, southeastern Iran

Fungi isolated Kyanpars area Amaniae area Golestan area Total No. (%) No. (%) No. (%) No. (%) Aspergillus flavus 4(13.3) 0(0) 1(5) 5(7.1) Aspergillus niger 10(33.3) 0(0) 1(5) 11(15.7) Aspergillus terreus 2(6.7) 0(0) 0(0) 2(2.9) Aspergillus sp. 4(13.3) 4(20) 0(0) 8(11.4) Rhizopus sp. 2(6.7) 2(10) 1(5) 5(7.1) Penicillium sp. 4(13.3) 4(20) 0(0) 8(11.4) Mucorales sp. 0(0) 1(5) 0(0) 1(1.4) Alternaria sp. 0(0) 1(5) 0(0) 1(1.4) Cladosporium sp. 0(0) 1(1.7) 0(0) 1(0.5) Mycelia sterilia 1(3.3) 2(10) 1(5) 4(5.7) Chrysosporium sp. 0(0) 1(5) 0(0) 1(1.4) Candida albicans 6(20) 0(0) 3(15) 9(12.9) Candida glabrata 1(3.3) 0(0) 2(10) 3(4.3) Candida parapsilosis 1(3.3) 0(0) 0(0) 1(1.4) Candida famata 1(3.3) 1(5) 0(0) 2(2.9) Candida tropicalis 0(0) 1(5) 0(0) 1(1.4) Candida guilliermondii 1(3.3) 0(0) 0(0) 1(0.5) Candida krusie 0(0) 1(5) 0(0) 1(1.4) Candida lipolytica 0(0) 1(5) 0(0) 1(1.4)

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Table 1. Continued … Candida sp. 5(16.7) 1(5) 4(20) 10(14.3) Rhodotorula sp. 5(16.7) 6(30) 8(40) 19(27.1) Zygosaccharomyces sp. 3(10) 1(5) 2(10) 6(8.6) Debaryomyces polymorphus 1(3.3) 0(0) 0(0) 1(1.4) Yeasts 3(10) 5(25) 10(50) 18(25.7)

Discussion

The objective of this research was to iso- tious agents carried by cockroaches can infect late and identify the fungi found of gut of human, and food resources in some con- American cockroaches as a source of con- ditions (1, 3, 4, 6–10, 25). tamination. All cockroaches collected were This study confirmed that these insects in identified as P. americana. Different patho- residential areas were contaminated with fungi genic and nonpathogenic fungal agents were of medical importance. A total of 12 yeast and recovered from this cockroach in human en- 11 filamentous species of fungi were isolated vironments. Periplaneta americana can car- from American cockroaches. In this study, a ry pathogenic fungi in its internal organs. high percentage of the cockroach specimens Therefore, P. americana is much more than (88.6%) from the houses were found to carry a harassment and that it has important health known fungal pathogens including Penicil- hazards as a mechanical vector. Therefore, the lium spp., Candida spp. and Aspergillus spp. abundance of American cockroaches’ popu- Thus, the isolation of medically important lation has to be reduced by various control fungi suggests a serious risk concern for pa- methods, such as the proper management of tients. Although the direct involvement of garbage and organic waste disposal, sanita- American cockroaches in transmission of in- tion and using safe insecticides. Clearly, pres- fectious agents is difficult to demonstrate. ence of cockroaches in sensitive environments, Other several studies have also isolated, from hospitals and houses are more dangerous than cockroaches from residential areas and hos- other parts due to the special circumstances pitals, medically important fungi (14-17, 25- and the special people hospitalized and can 27). In the present study, the main fungi iso- affect to environmental, people and commu- lated were species of Candida spp. (41.4%), nity health. Density of cockroaches in most Aspergillus spp. (37.1%), Rhodotrula spp. parts of the hospital and residential dwell- (27.1%) and Penicillium spp. (11.4%). The ings as well as their feeding from secretions, findings from this study about medically im- human feces, and their ability to transmit a portant fungi isolated from cockroaches are wide range of pathogenic agents, make it as agreed with the results of some workers. In a ideal vector to transmit most medically im- study in Thailand, Penicillium spp. and As- portant microorganisms. Nowadays, cockroach- pergillus spp. appeared frequently on integ- es have access to an infection source, human ument of 16 (35.6%) and 11 (24.4%) cock- food and the place for food production, their roaches, respectively (17). In another study role in the transmission of the disease is un- in Brazil, Candida sp. (38.6%), Aspergillus deniable. The propensity of American cock- sp. (30.7%) and Penicillium sp. (8.9%) were roaches to move freely and dwell sewers, re- the most common fungi recovered on cock- strooms and drains can support to make the roaches (14). In addition, in Sari (Iran), Can- problem worse. Ability of cockroaches in the dida spp, Aspergillus spp., and Rhodotrula transmission of pathogens is emphasized in spp. were the most fungi appeared on cuticle many types of research in this regard. Infec- of cockroaches (25). In a survey in Kashan 19 http://jad.tums.ac.ir Published Online: March 18, 2018

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(Iran), the prevalence of fungal agents in cock- causes of morbidity in immunocompromised roaches was 41.1% and 22.8%, respectively. individuals especially in those remained in Candida spp. (39.5%), Aspergillus spp. (37, hospital for a long period (30). Aspergillus 2%) and Penicillium spp. (5.4%) had maxi- sp., an important medical species isolated in mum prevalence among fungi observed (27). our study, has been reported in hospital-ac- In India, Candida spp. and Aspergillus spp. quired infections. Aspergillus flavus, the spe- were the most frequent fungi of medically cies isolated in this study, had been isolated important genera from cockroaches from a in bone marrow transplant recipients (31). hospital and a residential area (29). Moreover, A. niger and A. flavus have been The finding of the present study also reported from patients with invasive disease showed, C. albicans (31%), C. glabrata (32-35). Furthermore, other mold species as (10.3%) and C. famata (6.9%) were the greatest Penicillium spp., Alternaria spp., Cladosporium species isolated from cockroaches. Candida spp., Mucorales spp. and Chrysosporium spp. glabrata (42.2%) was the highest species have lately appeared as significant pathogen- isolated from cockroaches. The second high- ic microorganisms inappropriately unable per- est was C. magnoliae which 17.8% of cock- sons (25). roaches contaminated (14). Yeast identifica- Among Candida species, C. albicans was tion of Candida species showed a higher per- the commonest species of this genus. Candida centage of C. glabrata (15.4%), C. parapsilo- is noticed as an opportunistic pathogenic mi- sis (15.4%) and C. pseudotropicalis (15.4%), croorganism. Candida albicans responsible than C. albicans (2.6%) isolated from cock- for the majority of hospital-acquired infec- roaches (17). Candida glabrata (52.8%) and tions. Candida albicans is the most prevalent C. albicans (38.8%) were the highest species fungi in healthy people, moreover the most isolated from cockroaches. In the present prevalent fungal pathogenic agent causing study, four species of Aspergillus were iden- deadly infections (especially in immunocom- tified. Aspergillus niger (42.3%) and A. flavus promised subjects). Candida tropicalis, C. (19.2%) were the highest species isolated from glabrata, C. guilliermondii, and C. parapsilosis American cockroaches. Aspergillus niger have lately emerged as significant infectious (50%) was the most species isolated from agents inappropriately unable people (36). cockroaches. Moreover, A. flavus and A. fu- Rhodotorula species have been reported as migatus were the most frequently recovered nosocomial meningitis and endophthalmitis, species from cockroaches (14). Aspergillus particularly in HIV infected persons (25). niger was significantly more frequent in the Cockroaches living near human environ- residential area and the hospital (28). In a ments were significant vectors of etiological study in the hospital environments in Ahvaz agents and all groups of possible pathogens City, 28 fungal species were isolated from such as protozoans, bacteria, helminths, and adult housefly. The main fungi isolated were viruses. Various bacteria universally associ- Aspergillus spp. (67.4%), Penicillium sp. ated with these insects are recognized to in- (11.6%), Mucorales sp. (11%), Candida spp. ure diarrhea, dysentery, and food intoxica- (10.5%), and Rhodotorula sp. (8.4%) (29). tion in humans. Cockroaches have been as- We have displayed that American cock- sociated with an outbreak of dysentery. Dif- roaches transport great number of species of ferent species of bacteria of public health medically significant fungi in their digestive significance have been isolated from Peri- system, incriminated as significant agents in planeta americana, such as Staphylococcus nosocomial infections. Hospital-acquired fun- aureus, Streptococcus spp., Enterobacteri- gal infections are considered consequential aceae, Pseudomonas aeruginosa, and so on.

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Cockroaches captured in hospitals and hous- ga sp. as a new species in Iran. J Ar- es have been found to harbor multi-drug re- thropod-Borne Dis. 9(2): 161–175. sistant bacteria (9). 2. Dehghani R, Atharizadeh M, Moosavi SG, Therefore, the high contamination of cock- Azadi S, Rashidi M, Paksa A (2014) roaches to the agents of infectious diseases Analysis of cockroach fauna and fre- can transmit fungal infections in public plac- quency in human residential habitats es such as hospitals and the home. Hospitals of North of Isfahan, Iran. Inter Arch and homes are the focus of infection and a Health Sci. 1(1): 25–29. good place to cockroaches can transfer infec- 3. Fakoorziba MR, Eghbal F, Hassanzadeh J, tious agents. Therefore, the occurrence of in- Moemenbellah-Fard MD (2010) Cock- fected cockroaches in the sensitive environ- roaches (Periplaneta americana and ment of hospital and home, that are places Blattella germanica) as potential vec- for treatment of patients and living of people, is tors of the pathogenic bacteria found very dangerous and threatening public health. in nosocomial infections. Annals Trop Therefore, control of these insects is essential Med Parasit. 104: 521–528. to achieve the essential goals of hospitals and 4. Vahabi A, Shemshadn K, Mohammadi P, to create a safe environment in homes. Sayyadi M, Shemshad M, Rafinejad J (2011) Microbiological study of do- Conclusion mestic cockroaches in human dwell- ing localities. Afr J Microbiol Res. 5:

5790–5792. We revealed the presence of pathogenic 5. Beccaloni GW, Eggleton P (1882) Order filamentous fungi and yeasts in the gut of Blattodea Brunner von Wattenwyl. In: Periplaneta americana collected from the Zhang ZQ. (Ed.) (2011) Animal bio- houses in the city of Ahvaz. Therefore, Amer- diversity: An outline of higher-level ican cockroaches are a potential vector of classification and survey of taxonom- pathogenic fungal microorganisms in residen- ic richness. Zootaxa. 3148: 199–200. tial environments. The control of P. america- 6. Pai HH, Chen WC, Peng CF (2004) Cock- na in residential dwellings is essential in or- roaches as potential vectors of noso- der to control the fungal infections in people. comial infections. Infect Control Hosp Epidemiol. 25: 979–984. Acknowledgements 7. Kassiri H, Kazemi S (2012) Cockroaches [Periplaneta americana (L.), Dicty- We thank medical entomology student Mr optera; Blattidae] as carriers of bacte- Javad Shamsi for his help in collecting the rial pathogens, Khorramshahr Coun- cockroaches. Chancellor for Research Affairs ty, Iran. Jundishapur J Microbiol. 5(1): of Ahvaz Jundishapur University of Medical 320–322. Sciences has partially financially supported 8. Feizhaddad MH, Kassiri H, Sepand MR, this project with number 89S.31. The authors Ghasemi F (2012) Bacteriological sur- declare that there is no conflict of interests. vey of American cockroaches in hos- pitals. Middle East J Sci Res. 12(7): References 985–989. 9. Kassiri H, Kasiri A, Quaderi A (2014) De-

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