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Original Article Epidemiological Study on Cutaneous Leishmaniasis in an Endemic Area, of Qom Province, Central Iran

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Original Article Epidemiological Study on Cutaneous Leishmaniasis in an Endemic Area, of Qom Province, Central Iran J Arthropod-Borne Dis, September 2017, 11(3): 403–413 A Saghafipour et al.: Epidemiological Study on … Original Article Epidemiological Study on Cutaneous Leishmaniasis in an Endemic Area, of Qom Province, Central Iran Abedin Saghafipour 1, *Hassan Vatandoost 2,3, *Ali Reza Zahraei-Ramazani 2, Mohammad Reza Yaghoobi-Ershadi 2, Moharram Karami Jooshin 4 ,Yavar Rassi 2, Mohammad Reza Shirzadi 5, Amir Ahmad Akhavan 2, Ahmad Ali Hanafi-Bojd 2 1Department of Medical Entomology and Vector Control, School of Public Health, International Campus (IC -TUMS), Tehran University of Medical Sciences, Tehran, Iran 2Department of Medical Entomology and Vector Control, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran 3Department of Environmental Chemical Pollutants and Pesticides, Institute for Environmental Research, Tehran University of Medical Silences, Tehran, Iran 4Qom Provincial Health Center, Qom University of Medical Sciences, Qom, Iran 5Communicable Diseases Management Center, Ministry of Health and Medical Education, Tehran, Iran (Received 25 Jan 2016; accepted 2 Oct 2017) Abstract Background: Cutaneous leishmaniasis (CL) is one of the most important health problems in many areas of Iran. There are two forms of the disease in Iran, anthroponotic and zoonotic CL. This study conducted to assess the epidemiological situation of CL in an endemic area of Qom Province, central Iran from Apr to Nov 2015. Methods: The sticky paper traps and aspirating tubes were used for collecting adult sand flies. Sherman traps and small insect nets were used to capture rodents and small mammals. Giemsa staining was used for preparing the expanded smear and followed by PCR for identifying the causative agent in human, vectors, and reservoirs. In this study, relative frequency of CL was also calculated. Results: Fourteen species of Phlebotomine sand flies were collected. Phlebotomus papatasi (61.74%) was the predom- inant species through the period of activity. Overall, 62 Meriones libycus, 8 Nesokia indica, 4 Mus musculus, 16 Al- lactaga elater and 2 Hemiechinus auritis were caught. PCR technique showed 6 out of 150 P. papatasi (2%), two out of 62 M. libycus (3.23%) and all of suspected human's skin tissue samples (100%) were infected with Leishmania major. The relative frequency of CL was 0.30%. Conclusion: This is the first detection of L. major within P. papatasi, M. libycus and human in Kahak District in Qom Province of Iran. Zoonotic cycle of CL exists in this area, L. major is the causative agent, P. papatasi is the main vector and M. libycus is the main reservoir of the disease. Keywords: Zoonotic cutaneous leishmaniasis, Leishmania major, Phlebotomus papatasi, ITS1- PCR, Iran Introduction Currently, cutaneous leishmaniasis (CL) is major is the causative agent of Zoonotic CL one of the most important vector borne dis- in Iran. Leishmania major, L. (L.) tropica and eases in Iran (1) and still the leading cause of L. (L.) aethiopica cause CL in the Old World considerable morbidity of a large number of (3). The parasite has been isolated and identi- people in the endemic foci characterized by fied from naturally infected P. papatasi, P. chronic skin lesions followed by scars and de- caucasicus, Rhombomys opimus, Meriones formation of the infected tissue (2). libycus and human in such endemic areas (4- Phelebotomus papatasi is the main and 8). The P. papatasi and M. libycus were as proven vector and Leishmania (Leishmania) proven vector and reservoir in Qomrood, Iran *Corresponding authors: Dr Hassan Vatandoost, 403 E-mail: [email protected], Dr Ali Reza http://jad.tums.ac.ir Zahraei-Ramazani, E-mail: [email protected] Published Online: September 08, 2017 J Arthropod-Borne Dis, September 2017, 11(3): 403–413 A Saghafipour et al.: Epidemiological Study on … district (9) and as probable vector and reser- Materials and Methods voir in Ghanavat district (10). In addition, a big part of the lowland areas of Qom Province Study area provides good ecological niches for P. The Qom Province is bounded by Tehran papatasi and therefore it has higher transmis- Province in the north, Esfahan Province in the sion potential (11). south, Semnan Province in the east, and Markazi In the recent years, molecular methods Province in the west with an area of approxi- have been employed for identification of cer- mately 11240 square kilometers (0.68% total tain species of Leishmania, either isolated from area of Iran) (Fig. 1). This study was per- cultures or from patients (3) as well as in the formed from Apr to Nov 2015 in 3 villages detection of the parasite in individual or (Khor Abad, Sarm, and Ghobadbezan) of pooled Phlebotomine specimens (12). Suc- Kahak rural district (34o09'–35o11' N latitude cessful establishment of the disease in an en- and 50o06'–51o58' E longitude) of Qom Prov- demic area is the outcome of a close associa- ince with the elevation of almost 1500m tion between the Leishmania parasite and its above sea level (20). The average annual min- natural sand fly vector (13). Thus, vector and imum and maximum temperatures were 16.5 parasite identification have great impact on °C and 49 °C in Jan and Jul, respectively. The predicting expansions of the disease in en- total annual rainfall was about 150mm and the demic area, also help authorities to design new average Max and Min monthly Relative humid- strategic programs to limit spreading vectors ity were 84% and 28% in Dec and Jun, re- and disease (14, 15). spectively (21). Molecular methods are increasingly em- ployed for diagnostic and epidemiological Sand fly collection purposes in order to confirm Leishmania in- Sand flies were collected from indoor (bed- fection and to characterize the parasites at the room, bathroom, toilets, hall, and stables) and species or genotype level in hosts and vectors outdoor (rodent burrows) fixed places from (16, 17). The detection of Leishmania para- the first half of Apr 2015 to the first half of sites by PCR methods is highly specific and Nov 2015. To capture the sand flies, 30 Sticky sensitive, with values reaching up to 100%. Paper Traps (castor oil coated white paper Accurate and sensitive diagnostic and identi- 20×32cm) was used twice a month from sun- fication procedures are required to distinguish set to sunrise. The caught sand flies were Leishmania species/strains whose geographic transferred to the laboratory in Qom Health distribution can overlap, which is crucial for Center. To species identification, the head and adequate treatment and appropriate public the last two abdominal segments of the sand health control measures (18). flies were mounted in Puris’ medium (24) and Based on a rapid increase in incidence of identified after 24–72h, using the morpholog- CL reported in an endemic area of Kahak Dis- ical characters (25). Then, they were counted trict of Qom Province in central Iran (19), and and segregated by sex. The rest of the abdo- due to lack of knowledge on the epidemiolog- men, the wings and the legs used for DNA ex- ical situation of CL, this study was conducted traction were stored in 1.5ml sterile micro to determine the epidemiological features of tubes containing 96% ethanol. The females CL including human infection and the reser- were examined for abdominal status and the voir hosts and their putative vector species in numbers of unfed, fresh-blood fed, and gravid this endemic area during 2015. and semi-gravid sand flies were recorded. The parous females were distinguished from nulliparous sand flies by observation of the 404 http://jad.tums.ac.ir Published Online: September 08, 2017 J Arthropod-Borne Dis, September 2017, 11(3): 403–413 A Saghafipour et al.: Epidemiological Study on … appearance of the accessory glands (26). In 300μl saccharin phenol. After adding this so- order to determine the natural promastigote lution, the tube was centrifuged at 9300 rpm infections of female sand flies, some unfed, for 5min. After transferring upper phase to blood fed, semi-gravid and gravid female sand new tube, 300μl phenol- chloroform should flies (captured from rodent burrows) dissected be added and was centrifuged at 10000rpm in a fresh drop of sterile saline (9/1000) for the for 5min. Again transferred the upper phase presence of promastigotes in alimentary canal to new tube and washed with pure chloro- during Jun and Sep 2015. form. Thirty μl MgCl2 and 1000μl ethanol were added to upper phase and stored at -20 Reservoirs collection and smear prepara- °C for 2h before was centrifuged at 10000rpm tion for 10min and washed down phase by 70% The rodents were captured by Sherman ethanol with TE and was centrifuged at 10000 Live Traps (Fig. 2). Collection of dipodids rpm for 10min and the TE buffer was added. (Rodentia: Dipodidae) was done by using small insect nets. Then the impression smears Polymerase chain reaction-restriction frag- of ears were fixed with absolute methanol and ment length polymorphism (PCR-RFLP) examined by Giemsa staining method. The for detection of Leishmania infection Leishman bodies were observed using light The DNA samples were examined for the microscope and then were subjected to Leishmania species ITS1 by PCR amplifica- molecular technique for identification. Tissue tion using the universal primer pair L5 8S (5´- samples were also taken from the edge of the TgA-TaC-CAC-TTA-TCg-CAC-T-<T>-3´) lesions in 45-suspected CL patients. Lesion and LITSR (5´-CTg-gAT-CAT-TTT-CCg- smears were fixed with absolute methanol and AT-<g>-3´) (Table 1). then stained with Giemsa for CL diagnosis. In this present study, we also calculated the rel- Molecular study ative frequency of CL. PCR production was followed by RFLP technique (27). The cycling conditions were DNA extraction 95 °C for 5min., followed by 35 amplification DNA extractions were carried out by crash- cycles, each consisting of three steps: dena- ing of the contents on the slides prepared from turation at 94 °C for 30sec, annealing 48 °C the digestive system of the 180 dissected fe- for 30sec, and extension at 72 °C for one min, male sand flies, the 78 rodent's ear lobes se- followed by a final extension at 72 °C for rous fluids and the 45 patient's lesion tissues, 7min in thermocycler.
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