Modeling of Environmental Factors Affecting the Prevalence of Zoonotic and Anthroponotic Cutaneous, and Zoonotic Visceral Leishmaniasis in Foci of Iran: A Remote Sensing and GIS Based Study

Abdolali Golpayegani; Ali Reza Moslem; Amir Ahmad Akhavan; Azam Zeydabadi; Amir Hossein Mahvi; Ahmad Allah-Abadi

Modeling of Environmental Factors Affecting the Prevalence of Zoonotic and Anthroponotic Cutaneous, and Zoonotic Visceral Leishmaniasis in Foci of Iran: A Remote Sensing and GIS Based Study

Abstract

Background: Leishmaniasis is a re-emerging serious international public health problem, and both visceral and cutaneous types of leishmaniasis became important endemic diseases in Iran. In this study, the relationships between environmental factors (vegetation and elevation) and the prevalence of diseases have been investigated.
Methods: All international and national online databases were searched by terms such as leishmaniasis, incidence, prevalence and other related words attributed to Iran and published until first quarter of 2015. The developed database in Excel, later imported to the ArcMap for spatial analyst and mapping. Afterwards, the software was used for modeling the relationship between the prevalence/incidence and environmental variables (vegetation and elevation) by both linear and nonlinear regression.
Results: After mapping the prevalence data from 144 studies, considering non-parametric ANOVA, the tendency of zoonotic visceral leishmaniasis to presence in high elevation and high vegetation was more than Anthroponotic and zoonotic cutaneous leishmaniasis. While linear regression showed weaker results for modeling, however, additive nonparametric regression analysis suggested that 10km buffers for elevation, and 10 as well as 50km buffers for vegetation could contribute in better fitness in modeling of these variables.
Conclusion: The detailed maps for distribution of disease concluded. The nonlinear regression is a reliable predictor of the relationship between environmental factors and disease incidence, although more and wide researchers are needed to confirm it.

Cerbino Neto J, Werneck GL, Costa CHN (2009) Factors associated with the in¬cidence of urban visceral leishmaniasis: an ecological study in Teresina, Piauí State, Brazil. Cadernos de Saúde Pública. 25(7): 1543–1551.

WHO (2016) Leishmaniasis fact sheet no. 375. World Health Organization, Geneva, Switzerland. Available at: http://www.who.int/mediacentre/factsheets/fs375/en/.

Sharifi I, Aflatoonian MR, Fekri AR, Hakimi Parizi M, Aghaei Afshar A, Khosravi A, Sharifi F, Aflatoonian B, Khamesipour A, Dowlati Y, Mod-abber F, Nadim A (2015) A comprehensive review of cutaneous leishmaniasis in Kerman Province, southeastern iran-narrative review article. Iran J Public Health. 44(3): 299–307.

Kassiri H, Sharifinia N, Jalilian M, Shemshad K (2012) Epidemiological aspects of cutaneous leishmaniasis in Ilam Province, west of Iran (2000–2007). Asian Pac J Trop Med. 2: 382–386.

Mohebali M, Edrissian GH, Shirzadi MR, Akhoundi B, Hajjaran H, Zarei Z, Molaei S, Sharifi I, Mamishi S, Mahmoudvand H, Torabi V, Moshfe A, Malmasi A, Motazedian MH, Fakhar M (2011) An observational study on the current distribution of visceral leishmaniasis in different ge¬ographical zones of Iran and im-pli¬cation to health policy. Travel Med Infect Dis. 9(2): 67–74.

Mohebali M, Edrissian GH, Nadim A, Hajjaran H, Akhoundi B, Hoosh-mand B, Zarei Z, Arshi S, Mirsamadi N, Naeini Manouchehri K (2006) Ap¬plication of direct agglutination test (DAT) for the diagnosis and seroep¬ide-miological studies of visceral leish¬maniasis in Iran. Iran J Parasitol. 1 (1): 15–25.

Ghatee MA, Sharifi I, Haghdoost AA, Kanannejad Z, Taabody Z, Hatam G, Abdollahipanah A (2013) Spatial cor¬relations of population and ecological factors with distribution of visceral leishmaniasis cases in southwestern Iran. J Vector Borne Dis. 50(3): 179–187.

Mohebali M (2012) Epidemiological status of visceral leishmaniasis in Iran: ex-periences and review of literature. Int J Clin Exp Pathol. S3: 003.

Masimalai P (2014) Remote sensing andGeographic Information Systems (GIS) as the applied public health and en-vironmental epidemiology. Int J Med Sci Public Health 3(12): 1430–1438.

Ready PD (2010) Leishmaniasis emer-gence in Europe. Euro Surveill. 15 (10): 19505–19516.

Mollalo A, Alimohammadi A, Shah-risvand M, Shirzadi MR, Malek MR (2014) Spatial and statistical analyses of the relations between vegetation cover and incidence of cutaneous leishmaniasis in an endemic prov¬ince, northeast of Iran. Asian Pac J Trop Dis. 4(3): 176–180.

Rassi Y, Saghafipour A, Abai MR, Oshaghi MA, Mohebali M, Mosta-favi R (2013) Determination of Leish¬mania Parasite Species of Cutaneous Leish¬maniasis Using PCR Method in Cen¬tral County, Qom Province. Zahedan J Res Med Sci. 15(12): 13–16.

Palaniyandi M (2014) GIS for disease surveillance and health information man¬agement in India. Geospatial Today. 13(5): 44–46.

Bhunia GS, Kesari S, Chatterjee N, Mandal R, Kumar V, Das P (2012) Seasonal relationship between normal¬ized difference vegetation index and abundance of the Phlebotomus kala-azar vector in an endemic focus in Bihar, India. Geospatial Health. 7(1): 51–62.

Tsegaw T, Gadisa E, Seid A, Abera A, Teshome A, Mulugeta A, Herrero M, Argaw D, Jorge A, Aseffa A (2013) Identification of environmental param-eters and risk mapping of visceral leish-maniasis in Ethiopia by using geo-graphical information systems and a statistical approach. Geospatial Health. 7(2): 299–308.

Palaniyandi M, Anand PH, Maniyosai R (2014) Climate, landscape and the en¬vironments of visceral leishmaniasis transmission in India, using remote sensing and GIS. J Geophys Remote Sens. 3(3): 1–6.

R Core Team (2015) R: A Language and Environment for Statistical Compu-ting. R Foundation for Statistical Computing. Vienna, Austria.

Hereher ME (2015) Environmental monitoring and change assessment of Tosh¬ka lakes in southern Egypt using re¬mote sensing. ‎Environ Earth Sci. 73 (7): 3623–3632.

Land Processes DAAC NASA (2015) USGS Earth Resources Observation and Science (EROS) Center, MODIS Reprojection Tool (MRT). Sioux Falls, South Dakota. Available at: https://mrtweb.cr.usgs.gov/.

NASA and Japan ASTER Program (2015) ASTER Global Digital Elevation Model (ASTER GDEM) data center. Version 2. Available at: http://gdem.ersdac.jspacesystems.or.jp/search.jsp.

Fox J, Weisberg S (2010) Nonlinear regression and nonlinear least squares in R: An appendix to an R companion to applied regression. Retrieved from McMaster University: http://socserv.mcmaster.ca/jfox/Books/Companion/appendix/Appendix-Nonlinear-Regression.pdf.

Fox J, Weisberg S (2011) An {R} Companion to Applied Regression. Sec¬ond ed. Sage, Thousand Oaks, CA.

Fagih-Nayini F, Mohebali M, Javadian E (2002) Epidemiology of Visceral leishmaniasis in Kordan-savojbalagh. Pajoohandeh J. 7(2): 9–15.

Mazloumi Gavgani AS, Hodjati MH, Mohite H, Davies CR (2002) Effect of insecticide-impregnated dog col-lars on incidence of zoonotic visceral leishmaniasis in Iranian children: a matchedcluster randomised trial. The Lancet. 360(9330): 374–379.

Soleimanzadeh G, Edrissian GH, Movah¬hed-Danesh AM, Nadim A (1993) Epidemiological aspects of kala-azar in Meshkin-Shahr, Iran: human in¬fection. Bull World Health Organ. 71(6): 759–762.

Mohebali M, Edrissian GH, Shirzadi MR, Hosseingholizadeh G, Pashaei MH, Ganji A, Zarei Z, Kousha A, Ak-houndi B, Hajjaran H, Malekafzali H (2010) Integrated visceral leish¬man-iasis surveillance system in primary care for children in Meshkin-Shahr district, north-western Islamic Re-pub¬lic of Iran. Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majal¬lah al-sihhiyah li-sharq al-muta¬was¬sit. 16(10): 1050–1054.

Edrissian GH (1996) Visceral leish-man¬iasis in Iran and the role of sero-logi¬cal tests in diagnosis and epidemi¬olog¬ical studies. Parasitology for 21st Century ICOPA VIII, Izmir, Turkey: CAB International, pp. 63–78.

Mohebali M, Edrissian GH, Shirzadi MR, Hosseingholizadeh Y, Pashaei MH, Ganji A, Zarei Z, Kousha A, Ak-houndi B, Hajjaran H (2011) Estab-lishment and integration of a visceral leishmaniasis surveillance system in the primary health care system and its evaluation, Meshkin-Shahr District, Iran. J Sch Public Health Inst Public Health Res. 9(2): 1–8.

Mahami M, Moheb Ali M, Keshavarz H, Hajaran H, Akhoondi B, Zarei Z, Charedar S (2006) A seroepidemio-logical survey of visceral leishman-iasis (KALA-AZAR) in Germi Dis-trict, Ardabil Province. J Sch Public Health Inst Public Health Res. 4(1): 45–55.

Mohammadi-Kheyrabadi K, Mohebali M, Mamishi S, Arshi S (2004) Epidemi-o¬logical characteristics of Kala-Azar in hospitalized patients in Ardebil Prov-ince. J Sch Public Health Inst Public Health Res. 2(2): 11–24.

Nadim A, Tahvildar Birooni GH, Mohe¬bali M (1998) A report of cutaneous and post kala-azar dermal leish¬maniasis in Moghan, Ardabil Province Hakim Res J. 1(1): 57–60.

Arshi S, Mohebali M, Akhoundi B, Sadeghi-Bazargani H, Sepehram V, Zarei Z, Hajikhani S, Sezavar SH (2002) Identification of a new en-demic focus of kala-azar and seroepi¬demiological study of visceral Leish¬mania infection in Ardabil Province. J Sch Public Health Inst Public Health Res. 1: 9–18.

Mazloumi Gavgani AS, Malaki Rav-asan N, Mazloumi Gavgani F (2011) Comparison of Nomadic and non-Nomadic lifestyles in transmission of Visceral Leishaniasis. J Gorgan Univ Med Sci. 13(1): 94–100.

Mirsamadi N, Mohebali M, Atari MR, Edrisian GH (2003) Serological survey of Visceral leishmaniasis (Kala-Azar) in Azarshahr, Azarbaijan Province, northwest of Iran. Hakim Res J. 6(1): 17–22.

Yaghoobi-Ershadi MR, Shahbazi F, Dar¬vishi M, Akhavan AA, Jafari R, Khajeian M, Rassi Y, Soleimani H, Shirzadi MR, Hanafi-Bojd AA, Da-rabi H, Arandian MH, Sanei-Dehkor-di A, Heidari M (2013) Molecular ep¬idemiological study of cutaneous leish¬maniasis in the focus of bushehr City, southwestern Iran. J Arthropod Borne Dis. 7(2): 113–121.

Hamzavi V, Mohebali M, Edrissian G, Fourozani A (2000) Epidemiological study of cutaneous leishmaniasis in Dashti and Dashtestani district of Bu¬shehr Province. Iran J Public Health. 29: 177–191.

Mohebali M, Hamzavi Y, Edrissian GH,Forouzani A (2001) Seroepidemi¬ologi¬cal study of visceral leishmaniasis among humans and animal reservoirs in Bushehr Province, Islamic Repub¬lic of Iran. Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majal¬lah al-sihhiyah li-sharq al-muta¬wassit. 7(6): 912–917.

Ghatee M, Sharifi I, Mirhendi H, Kanan-nejad Z, Hatam G (2013) Investi-gation of Double-Band Electro¬pho¬ret¬ic Pattern of ITS-rDNA Region in Iranian Iso¬lates of Leishmania tropica. Iran J Par¬asitol. 8(2): 264–272.

Razmjou S, Hejazy H, Motazedian MH, Baghaei M, Emamy M, Kalantary M (2009) A new focus of zoonotic cuta¬neous leishmaniasis in Shiraz, Iran. Trans R Soc Trop Med Hyg. 103(7): 727–730.

Rassi Y, Javadian E, Jalali M, Motazedian MH, Vatndoost H (2004) Investiga-tion on Zoonotic Cutaneous Leishmaniasis, Southern Iran. Iran J Public Health. 33(1): 31–35.

Fakoorziba MR, Baseri A, Eghbal F, Rezaee S, Azizi K, Moemenbellah-Fard MD (2011) Post-earthquake out¬break of cutaneous leishmaniasis in a rural region of southern Iran. Ann Trop Med Parasitol. 105(3): 217–224.

Davami MH, Motazedian MH, Sarkari B (2010) The changing profile of cu-taneous leishmaniasis in a focus of the disease in Jahrom District, southern Iran. Ann Trop Med Parasitol. 104 (5): 377–382.

Sharafi M, Pezeshki B, Reisi A, Kalanta¬ri M, Naghizadeh MM, Dast Manesh S (2013) Detection of Cutaneous Leish¬maniasis by PCR in Fasa District in 2012. J Fasa Univ Med Sci. 3(3): 266–270.

Noorpisheh S, Naghizadeh MM, Nikrouz L (2013) A study on the life quality of patients suffering from leishman¬iasis. J Fasa Univ Med Sci. 3(2): 155–162.

Entezari M, Eskandari F (2014) Rela-tionship between Climatic Factors and the Prevalence of Cutaneous Leishman¬iasis in Larestan City J Mil Med. 16 (2): 99–104.

Fakhar M, Motazedian MH, Hatam GR, Asgari Q, Kalantari M, Mohebali M (2008) Asymptomatic human carriers of Leishmania infantum: possible res¬ervoirs for Mediterranean visceral leish¬maniasis in southern Iran. Ann Trop Med Parasitol. 102(7): 577–583.

Edrissian GH, Ahanchin AR, Ghara¬chahi AM, Ghorbani M, Nadim A, Ardeha-li S, Hafizi A (1993) Seroepidemi¬o-logical studies of visceral leishman-iasis and search for animal reservoirs in Fars province, southern Iran. Iran J Med Sci. 18(3–4): 99–105.

Sahabi Z, Seyedi Rashti MA, Nadim A, Javadian E, Kazemeini M, Abai MR (1992) A Preliminary Report on the Natural Leptomonad Infection of Phleboto¬mus Majorin an Endemic Fo¬cus of Visceral Leishmaniasis (Vl) in Fars Province, South of Iran. Iran J Public Health. 21(1–4): 87–93.

Fakhar M, Motazedian M, Asgari G, Mohebali M, Mehrbani D (2006) A new endemic focus of Visceral Leish-maniosis in southern Iran. Ar¬ma-ghane-Danesh. 11(2): 103–113.

Mollalo A, Alimohammadi A, Shirzadi MR, Malek MR (2015) Geographic information system-based analysis of the spatial and spatio-temporal distri¬bution of zoonotic cutaneous leish¬man¬iasis in Golestan Province, north-east of Iran. Zoonoses Public Health. 62(1): 18–28.

Rahbarian N, Mesgarian A, Mahmoudi Rad M, Hajaran H, Shahbazi F, Mesgar¬ian Z, Taghipour N (2009) Identification of Leishmania species isolated from human cutaneous leish¬maniasis using PCR method. J Res Health Sci. 9(2): 48–51.

Sofizadeh A, Cherabin M, Mehravaran A (2012) Cutaneous leishmaniasis in Gonbad Kavoos, North of Iran (2009–11): an epidemiological study. J Gor¬gan Univ Med Sci. 14(4): 100–106.

Baghaei A, Parvizi P, Amirkhani A, Ho-narvar MR, Badiei F (2012) Identifi-cation of Leishmania using micro-scopic and molecular methods in sus¬pected patients of Cutaneous Leish¬maniasis by targeting ITS-rDNA gene, Golestan Province, Iran (2009–10). J Gorgan Univ Med Sci. 14(3): 72–81.

Mesgarian F, Rahbarian N, Hajaran H, Shahbaz F, Mesgarian Z, Taghipour N (2010) Identification of Leishma-nia species isolated from human cu-taneous Leishmaniasis in Gonbad-e-Qabus city using a PCR method dur-ing 2006–2007. J Tehran Univ Med Sci. 68(4): 250–256.

Hanafi Bojd AA, Yaghoobi-Ershadi MR, Zamani GH, Barzekar A, Jafari R, Pour Abazari G (2006) Epidemiologic as¬pect of Cutaneaus Leishmaniasis in Hajiabad, Hormozgan, Iran (2003). Medical J Hormozgan Univ Med sci. 10(1): 63–70.

Nazari M (2012) Cutaneous leishmaniasis in Hamadan, Iran (2004–2010). Zahedan J Res Med Sci. 13(9): 39–42.

Azizi K, Soltani A, Alipour H (2012) Molecular detection of Leishmania isolated from cutaneous leishman-iasis patients in Jask County, Hormozgan Province, Southern Iran, 2008. Asian Pac J Trop Med. 5(7): 514–517.

Asgari Nezhad H, Borhani M, Norouzi M, Merzaie M (2012) Cutaneous Leish-man¬iasis in school children in a bor-der area at south-west of Iran. Sci Par-asitol. 13(4): 153–158.

Shazad B, Abbaszadeh B, Khamesipour A (2005) Comparison of topical paro-mo¬mycin sulfate (twice/day) with in¬trale¬sional meglumine antimoniate for the treatment of cutaneous leish-man¬iasis caused by L. major. Eur J Der¬matol. 15(2): 85–87.

Bahrami AM, Delpisheh A, Za¬man-dousti A (2011) Epidemiologic aspects of cutaneous Leishmaniasis and trapeu¬tic effect of traditional ointment con¬taining onion juice compared with Am¬photricin B. J Kermanshah Univ Med Sci. 15(4): 251–259.

Yazdanpanah HA, Rostamianpur M (2013) Analysis of Spatial Distri¬bu-tion of Leishmaniasis and its Rela-tion¬ship with Climatic Parameters (Case Study: Ilam Province). Bull Env Phar¬macol Life Sci. 2(12): 80–86.

Roghani A, Yasemi M, Jalilian M, Abdi J, Rezayee K (2012) Epidemiology of cutaneous leishmaniasis in Ilam. Pa¬joohesh dar Pezeshki. 36(5): 50–53.

Shiee MR, Mohebali M, Doroodgar A, Teimouri A, Afzali H, Shirzadi MR (2012) A molecular and parasito-logi¬cal survey on cutaneous leishman¬ia¬sis patients from historical city of Kashan in Isfahan Province, center of Iran. Asian Pac J Trop Dis. 2(6): 421–425.

Zahraei-Ramazani AR, Yaghoobi-Ershadi MR, Mokhtari AR, Akhavan AA, Abdoli H, Arandian MH (2007) An-throponotic Cutaneous Leishmaniasis in Nonendemic Quarters of a Cen¬teral City in Iran. Iran J Public Health. 36 (2): 7–11.

Doroodgar A, Sayyah M, Doroodgar M, Mahbobi S, Nemetian M, Rafizadeh S, Rassi Y (2012) Progressive increas¬ing of cutaneous leishmaniasis in Kashan district, central of Iran. Asian Pac J Trop Med. 2(4): 260–263.

Talari S, Rezvan Talaei R, Shajari G (2006) A clinical and epidemiology survey of cutaneous leishmaniasis in childhood. J Med Sci. 6(4): 693–697.

Yaghoobi-Ershadi M, Hanafi-Bojd A, Akhavan A, Zahrai-Ramazani A, Mohebali M (2001) Epidemiological study in a new focus of cutaneous leishmaniosis due to Leishmania ma-jor in Ardestan town, central Iran. Acta Trop. 79(2): 115–121.

Mohammadian A, Almasi M, Kheybari H, Karimi F, Tehrani S (1999) Iden-tification of species and charac¬ter¬is-tics of an outbreak of cutaneous leish¬maniasis in a new focus of Iran. Bi¬omedical J Iran. 3(1): 31–39.

Yaghoobi-Ershadi M, Javadian E (1995) leishmaniose cutanée zoonotique au nod d'Ispahan: le point sur l'infection humaine en 1991. Bull Soc Pathol Exot. 88(1): 42–45.

Yaghoobi-Ershadi M, Moosa-Kazemi S, Zahraei-Ramazani A, Jalai-Zand A, Akhavan A, Arandian M, Abdoli H, Houshmand B, Nadim A, Hosseini M (2006) Evaluation of deltamethrin-im¬pregnated bed nets and curtains for con¬trol of zoonotic cutaneous leish¬man¬iasis in. Bull Soc Pathol Exot. 99(1): 43–48.

Nilforoushzadeh MA, Tahmores J, Ataei B, Jaafary F (2002) Evaluation of in¬tegrated pest management method on controlling zoonotic Cutaneous Leish¬maniasis in Emamzadeh Agha Ali Ab¬bas, Natanz County, Isfahan Province, 1996–1998. Iran J Dermatol. 6(2): 78–83.

Doroodgar A, Mahbobi S, Nemetian M, Sayyah M, Doroodgar M (2009) An epidemiological study of cutaneous leishmaniasis in Kashan (2007–2008). Koomesh. 10(3): 177–184.

Ahmadi NA, Ghafarzadeh M, Jalali Ga-loosang A, Gholami Parizad E (2013) An epidemiological study of Cuta¬ne¬ous Leishmaniasis with emphasis on incidence rate in Kashan, Isfahan Prov¬ince. Scientific J Ilam Univ Med Sci. 21(2): 1–9 (In Persian).

Ebadi M, Hejazi SH (2003) The epide-miological study of cutaneous Leish-maniasis situation in the students of primary school in Isfahan Borkhar re¬gion. J Kerman Univ Med Sci. 10(2): 92–98.

Yaghoobi-Ershadi M, Hanafi A, Akha-van A, Zahraei Ramazani A, Mohe-bali M (1999) Cutaneous leishmania¬sis in Ardestan Town. Hakim Res J. 1(3): 206–215.

Doroudgar A, Dehghani R, Hooshyar H, Sayyah M (1996) Study of the prev-alence of the cutaneous Leishmania-sis in south-east part of Kashan. J Kerman Univ Med Sci. 3(2): 80–86.

Nadim A, Aflatoonian MR (1995) An-throponotic cutaneous leishmaniasis in the city of Bam, southeast Iran. Iran J Public Health. 24(1–2): 15–24.

Sharifi I, Nakhaei N, Aflatoonian M, Parizi MH, Fekri A, Safizadeh H, Shirzadi M, Gooya M, Khamesipour A, Nadim A (2011) Cutaneous leish-maniasis in bam: a comparative eval¬u¬ation of pre- and post-earthquake years (1999–2008). Iran J Public Health. 40(2): 49–56.

Yaghoobi-Ershadi MR (1977) Cutene-ous leishmaniasis in Kerman. [MSPH theses]. School of Public Health, Tehran University, Iran.

Mirzaei M, Sharifi I, Poursmaelian S (2012) A new focus of anthroponotic cutaneous leishmaniasis and identi-fica¬tion of parasite species by nested PCR in Jiroft, Iran. Comp Clin Path. 21(5): 1071–1075.

Aflatoonian MR, Sharifi I, Hakimi Parizi M, Fekri AR, Aflatoonian B, Sharifi M, Khosravi A, Khamesipour A, Shar¬ifi H (2014) A prospective cohort study of cutaneous leishmaniasis risk and opium addiction in south eastern

Iran. PLoS One. 9(2): e89043.

Sharifi I, Fekri AR, Aflatonian MR, Nadim A, Nikian Y, Kamesipour A (1998) Cutaneous leishmaniasis in primary school children in the south-eastern Ira-nian city of Bam, 1994–95. Bull World Health Organ. 76(3): 289–293.

Sharifi I, Poursmaelian S, Aflatoonian MR, Ardakani RF, Mirzaei M, Fekri AR, Khamesipour A, Parizi MH, Harandi MF (2011) Emergence of a new focus of anthroponotic cutane-ous leishmaniasis due to Leishmania tropica in rural communities of Bam District after the earthquake, Iran. Trop Med Int Health. 16(4): 510–513.

Aflatoonian MR, Sharifi I, Poursmaelian S, Hakimi-Parizi M, Ziaali N (2013) The Emergence of Anthroponotic Cu¬taneous Leishmaniasis Following the Earthquake in Southern Villages of Bam District, southeastern Iran, 2010. J Arthropod Borne Dis. 7(1): 8–14.

Nadim A, Motabar M, Houshmand B, Keyghobadi K, Aflatonian MR (1995) Evaluation of pyrethroid impregnated bednets for control of anthroponotic cutaneous leishmaniasis in Bam (Is¬lam¬ic Republic of Iran), WHO/LEISH/95. 37: Geneva. p. 21.

Sharifi I, Aflatoonian MR, Aflatoonian B, Kermanizadeh A (2015) The severity of cutaneous leishmaniasis before and after the earthquake in Bam, south¬east¬ern Iran. J Parasit Dis. 39(4): 741–744.

Aflatoonian MR, Sharifi I (2011) The Epidemiology of cutaneous leish-man¬iasis in the city and suburb of Bam in 2010: Active case-finding, treatment and health education of the school children. Iran J Epidemiol. 7(3): 52–57.

Aflatoonian MR, Sharifi I (2010) Preva¬lence rate of cutaneous leishmaniasis in Bam District during 20 Years (1988–2007). J Kerman Univ Med Sci. 17(4): 297–306.

Mirzadeh A, Hejazi Zadeh B, Mesgar pour B, Golezar A, Halakooiiy Nayini K (2008) The process of development of high-risk centers of cutaneous leish¬maniasis in the city of Kerman in 2002–2005 years andevaluation of efec¬tive environmental factors by using GIS. Iran J Epidemiol. 4(3 and 4): 5–17.

Aflatoonian MR, Sharifi I, Aflatoonian B (2014) The Effects of Prevention Knowledge Compared to the Im-prove¬ment of Housing Conditions in Con¬trol of Anthroponotic Cutaneous Leish¬maniasis: a Natural Experience of Earth¬quake in Bam/Iran. J Kerman Univ Med Sci. 21(3): 247–258.

Aflatoonian MR, Sharifi I (2007) Prev-alence of Cutaneous Leishmaniasis in School Children in Bam and Bara-wat. Iran in 2006. J Kerman Univ Med Sci. 14(2): 82–89.

Akhavan AA, Yaghoobi-Ershadi MR, Ha¬sibi F, Jafari R, Abdoli H, Arandian MH, Soleimani H, Zahraei-Ramazani AR, Mohebali M, Hajjaran H (2007) Emergence of cutaneous leish¬man¬ia-sis due to Leishmania major in a new focus of southern Iran. J Arthropod Borne Dis. 1(1): 1–8.

Aghaei-Afshar A, Vatandoost H, Sharifi I, Rassi Y, Abai MR, Oshaghi MA, Yaghoobi-Ershadi MR, Rafizadeh S (2013) First determination of impact and outcome indicators following in¬door residual spraying (IRS) with del-tamethrin in a new focus of anthro¬pon¬otic cutaneous leishmaniasis (ACL) in Iran. Asian Pac J Trop Med. 3(1): 5–9.

Khosravi A, Sharifi I, Dortaj E, Aghaei Afshar A, Mostafavi M (2013) The pre¬sent status of cutaneous leishmania¬sis in a recently emerged focus in South-west of Kerman Province, Iran. Iran J Public Health. 42(2): 182–187.

Sharifi I, Zemani F, Aflatoonian MR, Fekri AR (2008) A report of cutaneous leish-maniasis epidemic and its probable caus¬ative factors in Baft District, Ker¬man Province. Iran J Epidemiol. 4(1): 53–58.

Mahmoudvand H, Mohebali M, Sharifi I, Keshavarz H, Hajjaran H, Ak-houndi B, Jahanbakhsh S, Zarean M, Javadi A (2011) Epidemiological as-pects of visceral leishmaniasis in Baft District, Kerman Province, Southeast of Iran. Iran J Parasitol. 6(1): 1–11.

Barati M, Parizi MHD, Sharifi I (2008) Epidemiological and Clinical aspects of kala-azar in hospitalized children of Kerman Province, during 1991–2006. J Kerman Univ Med Sci. 15(2): 148–155.

Hamzavi Y, Khademi N (2015) Trend of cutaneous leishmaniasis in Kerman-shah Province, west of iran from 1990 to 2012. Iran J Parasitol. 10(1): 78–86.

Nazari N, Faraji R, Vejdani M, Mekaeili A, Hamzavi Y (2012) Prevalence of Cutaneous leishmaniases in Pations referred to Kermanshah hygienic cen¬ters (2006–2008) Zahedan. J Res Med Sci. 14(8): 77–79.

Hamzavi Y, Khademi N (2013) The Ana¬lytical study of Cutaneous Leish¬maniasis in Kermanshah (2011–2012). J Kermanshah Univ Med Sci. 17(9): 582–589.

Hamzavi Y, Hamzeh B, Mohebali M, Akhoundi B, Ajhang K, Khademi N, Ghadiri K, Bashiri H, Pajhouhan M (2012) Human visceral leishmaniasis in Kermanshah Province, Western Iran, during 2011–2012. Iran J Parasitol. 7 (4): 49–56.

Alavinia S, Arzamani K, Reihani M, Jafari J (2009) Some epidemiological aspects of cutaneous leishmaniasis in Northern Khorasan Province, Iran. J Arthropod Borne Dis. 3(2): 50–54.

Torabi V, Mohebali M, Edrissian GH, Keshavarz H, Mohajery M, Hajaran H, Akhoondi B, Sanaati A, Zarei Z, Delshad A (2007) Seroepidemiology of visceral leishmaniasis by DAT in Bojnord-North Khorasan. Iran J Ep-idemiol. 4(3 and 4): 43–50.

Sattar Pagheh A, Fakhar M, Sharif M, Danesh V, Ahmadi Z (2013) Epide-mi¬ological Survey of Cutaneous Leish¬maniasis due to Leishmania tropica in a New Focus in Khorasan Razavi Prov¬ince. J Mazandaran Univ Med Sci. 23(103): 47–53.

Moosa-Kazemi SH, Yaghoobi-Ershadir MR, Akhavan AA, Abdoli H, Zahraei-Ramazani AR, Jafari R, Houshmand B, Nadim A, Hosseini M (2007) Deltame¬thrin-impregnated bed nets and cur¬tains in an anthroponotic cutaneous leish¬man¬iasis control program in northeast¬ern Iran. Ann Saudi Med. 27(1): 6–12.

Saadabadi F, Mohajery M, Poostchi E, Shamsian SAA (2013) Identification of Leishmania species causing cuta-neous leishmaniasis using Random Am-plified Polymorphic DNA (RAPD-PCR) in Kharve, Iran. Reports of Bio¬chemistry and Molecular Biology. 1 (2): 69–73.

Hassanpour K, Aghamollaei H, Golpich M, Amani J, Taheri A, Farnoosh G (2014) Molecular epidemiological study of cutaneous leishmaniasis in the east north of Iran. Asian Pac J Trop Dis. 4: 540–544.

Hoseini Farash BR, Mohajery M, Shamsian AA, Rezaie A (2011) Iden-tification of Leishmania species caus¬ing cutaneous Leishmaniasis by PCR method in Torghabeh-Shandiz during 2009–2010. Forth Congress of Labor¬atory and Clinic, 2011 December 21–23, Tehran, Iran.

Khajedaluee M, Yazdanpanah M, Seyed Nozadi SM, Fata A, Juya MR, Ma¬soudi MH, Najaf Najafi M (2014) Epi¬demiology of cutaneous leish¬man-iasis in Razavi Khorasan in 2011. Med-ical J Mashhad Univ Med sci. 57(4): 647–654.

Mohajery M, Hajaran H, Shamsian A, Tavakol Afshari J, Saadabadi F (2008) Identification of cutaneous leishman¬iasis species by RAPD-PCR in Ney¬shabur. Medical J Mashhad Univ Med sci. 51(100): 79–86.

Yaghoobi-Ershadi MR, Akhavan AA, Zahraei-Ramazani AV, Abai MR, Ebrahi¬mi B, Vafaei-Nezhad R, Hanafi-Bojd AA, Jafari R (2003) Epide¬mi¬o-logical study in a new focus of cuta-neous leishmaniasis in the Islamic Re¬public of Iran. Eastern Mediterranean health journal = La revue de sante de la Mediterranee orientale = al-Majallah al-sihhiyah li-sharq al-mutawassit. 9 (4): 816–826.

Karimi Zarchi AA, Mahmodzadeh A, Vatani H, Shirbazo S (2004) Epide-mi¬ological study of Cutaneous Leishman¬ia¬sis in Sarakhs District. J Shahid Se¬doghi Univ Med Sci. 12(1): 30–35.

Sahabi Z, Mohajery M, Seyedi Rashti M (1999) Fauna of arthropods vec-tors and their medical importance in the free trade zone Sarakhs ferns, sand flies and leishmaniasis. Hakim Res J. 2(3): 177–182.

Akbari E, Mayvaneh E, Entezari A, Nazari M (2014) Survey of the Role of Bioclimatic Factors in the Out-break of Cutaneous Leishmaniasis. Iran J Epidemiol. 10(3): 65–74.

Karamian M, Bojd F, Sedigh M, Hem-mati M, Saadatjoo A, Barati DA (2013) Molecular identification of cu¬taneous leishmaniasis agents in Bir¬jand, Iran. J Birjand Univ Med Sci. 20(2): 183–190.

Kassiri H, Shemshad K, Kassiri A, Sho-jaee S, Sharifinia N, Shemshad M (2012) Clinical laboratory and epide¬miological research on cutaneous leish¬maniasis in the south west of Iran. Ar¬chives of Clinical Infectious Dis¬eas¬es. 7(4): 128–131.

Kassiri H, Shojaei S, Kolahkaji K (2012) Epidemiological status of cutaneous leishmaniasis in Behbahan County, Khuzestan Province, Southwestern Iran. Int J Infect Dis. 16(Supplement 1): e348.

Kassiri H, Lotfi M, Farajifard P, Kassiri E (2014) Laboratory diagnosis, clinical manifestations, epidemiological situa¬tion and public health importance of cutaneous leishmaniasis in Shushtar County, Southwestern Iran. J Acute Disease. 3(2): 93–98.

Kassiri H, Feizhaddad MH, Abdeh-panah M (2014) Morbidity, surveillance and epidemiology of scorpion sting, cuta¬ne¬ous leishmaniasis and pediculosis capitis in Bandar-Mahshahr County, Southwestern Iran. J Acute Disease. 3(3): 194–200.

Vazirianzadeh B, Hoseini S, Pour Rezaee S, Gardani H, Amraee K (2014) Prevalence of Cutaneous Leishman-ia¬sis in Ramshir, Iran, An Epidemi-ological Study. International Ar-chives of Health Sciences. 1(1): 41–37.

Kassiri H, Shemshad K, Lotfi M, Shemshad M (2013) Relationship Trend Analysis of of Cutaneous Leish¬maniasis Prevalence and Climato¬log¬ical Variables in Shush County, South-West of Iran (2003–2007). Acad J En¬tomol. 6(2): 79–84.

Spotin A, Rouhani S, Parvizi P (2014) The associations of Leishmania major and Leishmania tropica aspects by focusing their morphological and mo¬lecular features on clinical appear¬ances in Khuzestan Province, Iran. Bio Med Res Int. 2014: 913510.

Ghasemian M, Maraghi S, Samar¬bafza-deh AR, Jelowdar A, Kalantari M (2011) The PCR-based detection and identification of the parasites causing human cutaneous leishmaniasis in the Iranian city of Ahvaz. Ann Trop Med Parasitol. 105(3): 209–215.

Kassiri H, Shemshad K, Shojaee S (2013) The incidence rate of cutaneous leish¬maniasis in Behbahan County of Khuzestan Province, Southwest of Iran. Jundishapur J Microbiol. 6(5): e7045.

Nejati J, Mojadam M, Bojd H, Ali A, Keyhani A, Habibi Nodeh F (2014) An epidemiological study of Cuta-neous Leishmaniasis in Andimeshk (2005–2010). Scientific J Ilam Univ Med Sci. 21(7): 94–101.

Behbahani A, Ahmadi S, Latifi SM, Sadeghi M (2012) Study of the fre-quency of Cutaneous Leishmaniasis in Omidieh District, Khouzestan Prov¬ince, Southwest of Iran (2008–2010). Jundishapur J Health Sci. 4(4): 37–46.

Kassiri H, Mortazavi SH, Kazemi S (2011) The epidemiological study of cutaneous leishmaniasis in Khorram-shahr City, Khuzestan Province, South¬west of Iran. Jundishapur J Health Sci. 3(2): 11–20.

Sarkari B, Pedram N, Mohebali M, Moshfe AA, Zargar MA, Akhoundi B, Shirzadi MR (2010) Seroepide¬mi-ological study of visceral leishman-iasis in Booyerahmad district, south-west Islamic Republic of Iran. East-ern Mediterranean health journal = La re-vue de sante de la Mediterranee ori-entale = al-Majallah al-sihhiyah li-sharq al-mutawassit. 16(11): 1133–1136.

Sarkari B, Moshfe AA, Pedram N, Zargar MA, Yazdanpanah B, Akhoundi B, Hasani Z, Mohebali M (2007) Sero¬log¬i¬cal Study of Visceral Leishman¬iasis in Boyer Ahmad Township in 2005. Armaghane-Danesh. 12(2): 69–77.

Kheirandish F, Chegeni Sharafi A, Kazemi B, Mohebali M, Sarlak A, Tarahi MJ, Holakouee K, Hajaran H (2013) Iden¬tification of Leishmania species using PCR assay on giemsa-stained slides prepared from cutaneous leishman¬iasis patients. Iran J Parasitol. 8(3): 382–388.

Amraee K, Rastegar HA, Beiranvand E (2013) An epidemiological study of cutaneous leishmaniasis in Pole¬dokhtar District, Lorestan Province, Southwest¬ern of Iran, 2001–2011. Jundishapur J Health Sci. 5(1): 55–62.

Ahmadi NA, Modiri M, Mamdohi S (2013) First survey of cutaneous leish¬maniasis in Borujerd county, western Islamic Republic of Iran. Eastern Med¬iterranean Health J = La revue de sante de la Mediterranee orientale = al-Majal¬lah al-sihhiyah li-sharq al-mutawas¬sit. 19(10): 847–853.

Chegeni-Sharafi A, Amani H, Kayedi MH, Yarahahmadi A, Saki M, Mehrdad M, Nasiri E (2011) Epidemiological sur¬vey of cutaneous leishmaniasis in Lorestan Province (Iran) and introduction of dis¬ease transmission in new local areas. J Ilam Univ Med Sci. 19(1):54–60. [In Persian].

Chegeni-Sharafi A, Ourmazdi H, Mohe¬bali M, Akhlaghi L, Sharafi MM, Akhondi B (2005) Seroepidemio¬log¬ical study of Visceral Leishmaniasis (human infection) in east Miankooh area in Lorestan Province by Direct Agglutination Test (DAT). Yafte J Med Sci. 7(3 and 4): 31–35.

Rostami MN, Saghafipour A, Vesali E (2013) A newly emerged cutaneous leishmaniasis focus in central Iran. Int J Infect Dis. 17(12): e1198–e1206.

Akhavan AA, Yaghoobi-Ershadi MR, Mehdipour D, Abdoli H, Farzinnia B, Mohebali M, Hajjaran H (2003) Ep¬idemic outbreak of cutaneous leish¬man¬iasis due to leishmania major in Ghanavat Rural District, Qom Prov¬ince, Central Iran. Iran J Public Health. 32(4): 35–41.

Saghafipour A, Rassi Y, Abai MR, Oshaghi MA, Farzinnia B, Mostafavi R, Karimian F (2013) Outbreak of Zoonotic Cutaneous Leishmaniasis: A Report. Arch Hyg Sci. 2(2): 45–54.

Saghafipour A, Amir A, Rassi Y, Mo-stafavi R (2012) Epidemiology of cu¬taneous leishmaniasis in Qom. J Qom Univ Med Sci. 6(1): 83–88.

Mohammadi Azni S, Nokandeh Z, Khorsan¬di AA, Sanei Dehkordi AR (2010) Epidemiology of cutaneous leishmaniasis in Damghan. Iran J Mil Med. 12(3): 131–135.

Mohammadi Azni s, Rassi Y, Oshaghi MA, Yaghoobi-Ershdi M, Mohebali M, Abai MR, Mohtarami F, Nokandeh Z, Rafizadeh S, Khojami GM (2011) Determination of parasite species of cutaneous leishmaniasis using Nested PCR in Damghan-Iran, during 2008. J Gorgan Univ Med Sci. 13(1): 59–65.

Mohammadi Azni S, Nokandeh Z, Sanei Dehkordi AR (2010) Control of rural cutaneous leishmaniasis in Damghan in 2005–2006. Iran J Infect Dis. 15 (48): 29–32.

Rafati N, Shapouri Moghadam M, Ghor¬bani R (2007) Epidemiological study of cutaneous Leishmaniasis in Damghan (2000–2006). Scientific J Semnan Univ Med Sci. 8(4): 247–253.

Fazaeli A, Fouladi B, Hashemi-Shahri SM, Sharifi I (2008) Clinical features of cu¬taneous leishmaniasis and direct PCR-based identification of parasite spe-cies in a new focus in southeast of Iran. Iran J Public Health. 37(3): 44–51.

Fazaeli A, Fouladi B, Sharifi I (2009) Emergence of cutaneous leishman-iasis in a border area at south-east of Iran: an epidemiological survey. J Vector Borne Dis. 46(1): 36–42.

Fouladi B, Sharifi I, Hashemi SS, Morad GH, Sarabandi NA, Ebrahimzadeh A, Fazaeli A (2007) Evaluation of a direct PCR in comparison with routine microscopy and in vitro culture for diagnosis of cutaneous leishmaniasis. Zahedan J Res Med Sci. 9(3): 9–15.

Salehzadeh A, Seyedi Rashti M (1996) Cutaneous leishmaniasis in North of Tehran. Scientific J Hamadan Univ Med Sci. 4(1): 34–39.

Abadi M (2004) Survey the situation of anthroponotic Cutaneous leishmania¬sis in North-West of Tehran. [PhD dis¬sertation]. Tehran Islamic Azad uni¬ver¬sity, Iran.

Yaghoobi-Ershadi MR, Hanafi-Bojd AA, Javadian E, Jafari R, Zahraei-Ram¬azani AR, Mohebali M (2002) A new focus of cutaneous leishmaniasis caused by Leishmania tropica. Saudi Med J. 23 (3): 291–294.

Yaghoobi-Ershadi MR, Jafari R, Hanafi-Bojd AA (2004) A new epidemic focus of zoonotic cutaneous leishmaniasis in central Iran. Ann Saudi Med. 24(2): 98–101.

Jaafary R, Mohebali M, Dehghan Dehna¬vi AR, Soleimani H, Akhavan AA, Haja¬ran H, Dehghan shadkam A, Fatahi J (2007) Epidemiological status of cu¬taneous leishmaniasis in Bafgh City, Yazd Province 2005. J Shahid Sa¬doghi Univ Med Sci. 15(2): 76–83.

Mozafari GH, Bakhshi Zadeh F (2011) Analysis the Roll of bioclimatic Fac-tors in Prevalence of Cutaneous Leish¬maniasis in Yazd-Ardakan plain Geog¬raphy and Development J. 23: 185–202.

Hanafi Bojd AA, Dehghani Tafti AA, Jafari R, Ehrampoosh MH (2003) Ef¬ficacy of control program of zoonotic cutaneous leishmaniasis in a new focus of the disease. Medical J Mashhad Univ Med sci. 46(80): 19–25.

Yaghoobi-Ershadi MR, Marvi Moghadam N, Jaafary R, Akhavan A, Soleimani H, Zahraei Ramazani AR, Arandian MH, Dehghan Dehnavi AR (2008) Study of certain epidemiological as-pects of cutaneous Leishmaniasis in Khatam County, Yazd Province, Iran. J Shahid Sedoghi Univ Med Sci. 15 (4): 47–52.

Werneck G, Costa C, Walker A, David J, Wand M, Maguire J (2007) Multi-level modelling of the incidence of visceral leishmaniasis in Teresina, Bra¬zil. Epidemiol Infect. 135(2): 195–201.

Signorini M, Cassini R, Drigo M, di Re¬galbono AF, Pietrobelli M, Montarsi F, Stensgaard AS (2014) Ecological niche model of Phlebotomus pernicio¬sus, the main vector of canine leish¬man¬iasis in north-eastern Italy. Ge¬o¬spat Health. 9(1): 193–201.

Mokhtari M, Miri M, Nikoonahad A, Jalilian A, Naserifar R, Ghaffari HR, Kazembeigi F (2016) Cutaneous leish¬maniasis prevalence and morbidity based on environmental factors in Ilam, Iran: Spatial analysis and land use regression models. Acta Trop. 163: 90–97.

Elnaiem DEA, Schorscher J, Bendall A, Obsomer V, Osman ME, Mekkawi AM, Connor SJ, Ashford RW, Thom¬son MC (2003) Risk mapping of vis¬ceral leishmaniasis: the role of local variation in rainfall and altitude on the presence and incidence of Kala-Azar in eastern Sudan. Am J Trop Med Hyg. 68(1): 10–17.

Karimi A, Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Akhavan AA, Ghezel-bash Z (2014) Spatial and temporal distributions of phlebotomine sand flies (Diptera: Psychodidae), vectors of leishmaniasis, in Iran. Acta Trop. 132: 131–139.

Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Haghdoost AA, Akhavan AA, Rassi Y, Karimi A, Charrahy Z (2015) Mod¬eling the distribution of cutaneous leish¬man¬ia-sis vectors (Psychodidae: Phlebotom¬inae) in Iran: a potential transmission in disease prone areas. J Med Ento¬mol. 52(4): 557–565.

Gholamrezaei M, Mohebali M, Hanafi-Bojd AA, Sedaghat MM, Shirzadi MR (2016) Ecological Niche Modeling of main reservoir hosts of zoonotic cu¬taneous leishmaniasis in Iran. Acta Trop. 160: 44–52.

Oshaghi M, Ravasan NM, Javadian E, Rassi Y, Sadraei J, Enayati A, Vatan¬doost H, Zare Z, Emami S (2009) Application of predictive degree day model for field development of sandfly vectors of visceral leishmaniasis in northwest of Iran. J Vector Borne Dis. 46(4): 247–255.

Shirzadi MR, Mollalo A, Yaghoobi-Ershadi MR (2015) Dynamic rela-tions between incidence of zoonotic cutaneous leishmaniasis and climatic factors in Golestan Province, Iran. J Arthropod Borne Dis. 9(2): 148–160.

Sudhakar S, Srinivas T, Palit A, Kar SK, Battacharya SK (2006) Mapping of risk prone areas of Kala-Azar (Visceral leishmaniasis) in parts of Bihar State, India: an RS and GIS approach. J Vec¬tor Borne Dis. 43(3): 115–122.

Menezes JA, Ferreira EdC, Andrade-Filho JD, Sousa AMd, Morais MHG, Rocha AMS, Machado-Coelho GLL, Lima FP, Madureira AP, Garcia TC (2015) An Integrated Approach Using Spatial Analysis to Study the Risk Factors for Leishmaniasis in Area of Recent Transmission. Bio Med Res Int. 2015: 621854.

Files	XML PDF (1024KB)
Issue	Vol 12 No 1 (2018)
Section	Original Article
Keywords
Leishmaniasis GIS Remote sensing Environmental variables Nonlinear regression

Rights and permissions
	This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

How to Cite

Golpayegani A, Moslem AR, Akhavan AA, Zeydabadi A, Mahvi AH, Allah-Abadi A. Modeling of Environmental Factors Affecting the Prevalence of Zoonotic and Anthroponotic Cutaneous, and Zoonotic Visceral Leishmaniasis in Foci of Iran: A Remote Sensing and GIS Based Study. J Arthropod Borne Dis. 2018;12(1):41-66.

Vancouver

Download Citation