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Prevalence of Leishmania Species Among Patients with Cutaneous Leishmaniasis in Qassim Province of Saudi Arabia Zafar Rasheed1* , Ahmed A

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Prevalence of Leishmania Species Among Patients with Cutaneous Leishmaniasis in Qassim Province of Saudi Arabia Zafar Rasheed1* , Ahmed A Rasheed et al. BMC Public Health (2019) 19:384 https://doi.org/10.1186/s12889-019-6710-8 RESEARCHARTICLE Open Access Prevalence of Leishmania species among patients with cutaneous leishmaniasis in Qassim province of Saudi Arabia Zafar Rasheed1* , Ahmed A. Ahmed2, Tarek Salem1, Mohammed S. Al-Dhubaibi3, Ahmad A. Al Robaee3 and Abdullateef A. Alzolibani3 Abstract Background: Leishmaniasis is a parasitic infection endemic in more than ninety countries of the world. The cutaneous leishmaniasis (CL) is a most common form of leishmaniasis and it remains to be a major public health issue in Saudi Arabia. This study was undertaken to investigate the Leishmania species responsible for CL infection in different provinces of Qassim, Saudi Arabia. Methods: Skin biopsies were obtained from CL patients and DNA was extracted using the Magna pure system. Leishmania species were identified by highly specific/sensitive quantitative and qualitative PCR. Results: Out of total 206 CL biopsies, 49.5% biopsies were found to be positive for Leishmania major (L. major), 28.6% biopsies were positive for Leishmania tropica (L. tropica), 3.9% were found to be positive for Leishmania infantum/donovani (L. infantum/donovani). Not only have these, all tested CL biopsies showed negative test for Leishmania mexicana (L. mexicana) and Leishmania viannia (L. viannia). Conclusions: This is the first comprehensive study that shows the majority of CL in Qassim was caused by L. major and L. tropica. To the best of our knowledge, this is the very first report that shows the occurrence of L. infantum/ donovani in Saudi Arabia. This requires higher alert to the Ministry of Health of Saudi Arabia to take proactive actions in preventing the onset of L. major, L. tropica, L. infantum and L. donovani infections. Keywords: Cutaneous leishmaniasis, L. major, L.tropica, L. infantum/donovani, Qassim, Saudi Arabia Background specific L. species is important for the prescription of Leishmaniasis is a parasitic infection endemic in more appropriate therapy [5]. Treatment of CL patients than ninety countries of the world and the cutaneous without identification of L. species cause harmful effects leishmaniasis (CL) is a most common form of this infec- to the patients as the attribution of the relative import- tion caused by phlebotomine sand fly [1]. The World ance of specific L. species in humans are reported [6]. In Health Organization reported in 2016 that about 15 general, diagnosis is still based on clinical symptoms, million individuals have leishmaniasis and more than microscopic parasitic detection and tissue culturing of 360 million individuals are breathing in those regions promastigotes. However in cases with promastigotes which are prone for this infection and this infection culture, additional efforts should also be needed such as causes ~ 70,000 deaths per year [1, 2]. It is now well biochemical and serological analysis for further documented that CL is caused by more than 22 different characterization of parasites [7]. These additional efforts species of the genus Leishmania (L) but their prevalence for the determination of L. species are time taken and varies from region to region [3, 4]. Identification of are not sensitive, not accurate and sometime give wrong information [8]. Recently, several PCR based detection of L. species were developed, which are rapid, sensitive * Correspondence: [email protected] 1Department of Medical Biochemistry, College of Medicine, Qassim and accurate and now become a powerful approach to University, P.O. Box 6655, Buraidah 51452, Saudi Arabia determine the L. species types at all levels of detection Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Rasheed et al. BMC Public Health (2019) 19:384 Page 2 of 8 such as genus, complex, and species [9, 10]. Recently, Real time PCR Abuzaid et al. have extensively reviewed the prevalence Quantitative real-time PCR amplification was carried of CL in Saudi Arabia. They noticed that CL remains an out for the detection of L. major, L. viannia, L. mexicana unsolved public health issue of the country [10]. Al- and L. infantum/donovani by the Light cycler PCR though, CL is endemic in all over the regions of Saudi system (Roche Diagnostics, Mannheim, Germany). By Arabia but the majority of patients are continuously the use of CLUSTAL program in Lasergene software reported in Riyadh, Hassa, Aseer, Hail, Madinah, Taif (Madison, WI), the amplicons were aligned and nucleo- and also in Qassim [10–13]. Despite of all taking care by tide differences among the various Leishmania com- the Ministry of Health, Saudi Arabia but CL remains to plexes were determined as described previously [19]. be a major health issue of the country, which may be Using primer express software (PE Biosystems, Foster due to urbanization and huge population immigration City, CA), appropriate probes and flanking primers were [10]. As the information on the diversity of L. species in designed to specifically identify each Leishmania com- different provinces of Saudi Arabia is poor, therefore the plex. The following primers/probe combination for each current study was aimed to identify the L. species in dif- complex was designed: L. major complex: F-5’TTCT ferent provinces of Qassim, Saudi Arabia using highly GCTCCGTCGGTGTAGA3’,R-5’GCTTTCGATTGGCT specific and sensitive PCR-based approach. ACGACAA3’; and Lmaj-probe 5′-CCTGTCAGGAAT TCCACAAA-3′; L. infantum/donovani complex: F-5’CC Methods AGATGCCGACCAAAGC3’,R-5’CGCGCACGTGATGG Patients recruitment, biopsies collection and DNA extraction ATAAC3’ and Lid-probe 5′-ATCGGCAGGTTCT-3′; L. The study was carried out in accordance with the Code mexicana complex: F-5’CCAGTCCCAGAACACAAAC of Ethics of the World Medical Association (Declaration ATG3’,R-5’CCTATCGACCAACACAGAAAAGG3’ and of Helsinki as revised in Tokyo 2004) for humans and Lm probe 5′-ATGCCGAACTCCCGAA-3′; L. viannia the study protocol was approved by the National Plan complex: F-5’CAACAAAATGCTTCGCAACAG3’,R-5’C for Science, Technology and Innovation of Saudi Arabia GCAACGCCTTCATGGA3’ and LV-probe 5′-CGAC (NSTIP/KACST # 11-MED1068–09). With the Institu- GGGATATTGTTTGACTT-3′. PCR amplification with tional Review Board (IRB) approval, study subjects were specific primer for L. species was performed in the same recruited through the dermatology outpatient clinics of ways as described previously [19–21] with some modifi- Qassim region of Saudi Arabia. Patients were diagnosed cations. Briefly, typical profile times used were initial after careful clinical examination based on clinical step, 95 °C for 3 min, followed by 40 cycles of denatur- presentation and microscopy and were classified as ation at 95 °C for 15 s. and annealing/extension at 60 °C cutaneous leishmaniasis as described previously [14]. for 30 s, followed by 4.0 °C up to 24 h. The reactions Demographic details of the studied subjects are shown were conducted in a 20 μl and set up in a 96-well optical in Table 1. A total of 206 biopsies were taken from cuta- reaction plate. The reactants mix are containing 1x fast neous lesions and DNA samples were extracted from all start master mix (Integrated DNA Technologies, USA), biopsies by MagNaA pure DNA extraction Pure LC 3.0 pg. to 100 ng of DNA template, 1 μM of each primer DNA Isolation Kit (cat. # 03186229001, Roche Applied (Integrated DNA Technologies, USA). The presence of Science, Mannheim, Germany) using MagNA Pure LC amplified products (a positive result) was determined by Automated Instrument according to the manufacturer’s melting curves and values were recorded for estimation instruction (Roche) as described previously [15, 16]. The the L. species. All samples were run again with conven- absorbance of DNA solution was monitored at 260 nm tional PCR assays to determine L. tropica species. and 280 nm to ascertain its concentration and purity by using Perkin Elmer UV-Spectrophotometer (L7110223-D, Qualitative PCR Lambda XLS, Germany) as described previously [17, 18]. The qualitative PCR for L. tropica was carried out by using the following primers sequence F-5’TCGTCTGAT Table 1 Demographic and clinic characterization of studied TCAAAGTTCTC3’,R-5’CACACGCGCACACCGCGAT cutaneous leishmaniasis patients in Qassim, Saudi Arabia C3’ designed from Leishmania tropica GTG1 sequence SNo. Parameters Results (GenBank: AY826393.1) as described previously [22]. 1. Total number patients 206 The Go Taq® Green Mix (cat. # M7123, Promega 2. Patients age (mean ± SD., years) 34.20 ± 13.3 Corporation, WI, USA) was used according the instruc- 3. Gender (Males/Females) 114 Males/92 Females tions provided by the manufacturer (Promega, WI, μ 4. No. of lesions 1–14 USA). Briefly, the reaction mixture (50 L) contained 1X Go Taq® Green Master Mix, 1 μM of each primers 5. Sites of lesions Limb, facial or skill (Integrated DNA Technologies, USA), and 100–300 ng 6. Disease duration (mean ± SD., months) 58.99 ± 43.86 of the extracted DNA. The amplification was performed Rasheed et al. BMC Public Health (2019) 19:384 Page 3 of 8 by MWG Biotech Inc. Primus 96 Thermal Cycler, 220 we used quantitative and qualitative PCR for identifica- VAC (Mfr# TC-9600-226 V; Item # EW-93941-05) using tion of different L. species using specific sets of primers an initial heating of 95 °C for 2 min. 40 cycles were for L. major, L. infantum/donovani complex, L. mexi- applied with three stages: denaturation (95 °C for 30 s), cana, L.
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