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Climate and environmental factors affecting the incidence of cutaneous leishmaniasis in Isfahan, Iran

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11 April 2024 Editor's Note: Readers are alerted that the concerns have been raised with this article. Editorial action will be taken as appropriate once this matter is resolved and all parties have been given an opportunity to respond in full.

Abstract

Cutaneous leishmaniasis (CL) is a vector-borne human disease caused by Leishmania, a parasite transmitted by sand flies. CL is endemic in the Isfahan Province, Iran. This study was designed to identify the climate and environmental factors associated with CL incidence in Isfahan Province. Data included incident cases of CL, climate, and environmental factors, which were collected across 23 districts of province from 2007 to 2015. Analyses were performed with generalized linear models (GLMs) to fit a function to the relationships between the response and predictors. We used negative binomial regression due to over-dispersed distribution of CL cases. The effects of all seven climate and environmental factors were found to be significant (all p < 0.01), and the model explained 40% of the deviance of CL incidence. There was a positive relation between mean temperature, relative humidity, and slope of area with disease incidence; however, negative association was demonstrated between maximum wind speed, rainfall, altitude, and vegetation cover with CL incidence. Cutaneous leishmaniasis continues to be a widespread challenge, especially in northwestern parts of Iran. Climate and environmental factors should be considered when selecting the most appropriate strategies for preventing and controlling CL.

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  • 11 April 2024

    Editor's Note: Readers are alerted that the concerns have been raised with this article. Editorial action will be taken as appropriate once this matter is resolved and all parties have been given an opportunity to respond in full.

References

  • Ali-Akbarpour M, Mohammadbeigi A, Tabatabaee SHR, Hatam G (2012) Spatial analysis of eco-environmental risk factors of cutaneous leishmaniasis in southern Iran. J Cutan Aesthet Surg 5:30

    Article  Google Scholar 

  • Alvar J, Vélez ID, Bern C, Herrero M, Desjeux P, Cano J, Jannin J, Boer M, the WHO Leishmaniasis Control Team (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7(5):e35671. https://doi.org/10.1371/journal.pone.0035671

    Article  CAS  Google Scholar 

  • Amoli GM (2011) GIS-based risk map analysis of leishmaniasis disease in Isfahan, Iran. In: Business, Engineering and Industrial Applications (ISBEIA), 2011 I.E. Symposium on IEEE, pp 275–280

  • Asaei S (2014) Iran’s excellent primary health care system United Nation International Children Emergency Fund (UNICEF) (online) (cited 2011 March 20). Available from URL: www.unicef.org/iran

  • Ashford R, Bray M, Hutchinson M, Bray R (1973) The epidemiology of cutaneous leishmaniasis in Ethiopia. Trans R Soc Trop Med Hyg 67(4):568–601. https://doi.org/10.1016/0035-9203(73)90088-6

    Article  CAS  Google Scholar 

  • Bonham-Carter GF (2014) Geographic information systems for geoscientists: modelling with GIS. Vol 13. Elsevier

  • Shafaghi C (2007) The geography of Isfahan. Isfahan University, Isfahan

    Google Scholar 

  • Cardenas R, Sandoval CM, Rodriguez-Morales AJ, Franco-Paredes C (2006) Impact of climate variability in the occurrence of leishmaniasis in northeastern Colombia. Am J Trop Med Hyg 75(2):273–277

    Article  Google Scholar 

  • Chelbi I, Kaabi B, Bejaoui M, Derbali M, Zhioua E (2009) Spatial correlation between Phlebotomus papatasi Scopoli (Diptera: Psychodidae) and incidence of zoonotic cutaneous leishmaniasis in Tunisia. J Med Entomol 46:400–402

    Article  CAS  Google Scholar 

  • Christensen HA, Fairchild GB, Herrer A, Johnson CM, Young DG, de Vásquez AM (1983) The ecology of cutaneous leishmaniasis in the Republic of Panama. J Med Entomol 20(5):463–484. https://doi.org/10.1093/jmedent/20.5.463

    Article  CAS  Google Scholar 

  • Davami MH et al (2013) Molecular survey on detection of leishmanial infection in rodent reservoirs in Jahrom District, southern Iran. J Arthropod Borne Dis 8:139–146

    Google Scholar 

  • de Vries HJ, Reedijk SH, Schallig HD (2015) Cutaneous leishmaniasis: recent developments in diagnosis and management. Am J Clin Dermatol 16(2):99–109. https://doi.org/10.1007/s40257-015-0114-z

    Article  Google Scholar 

  • Doxaran D, Froidefond J-M, Castaing P, Babin M (2009) Dynamics of the turbidity maximum zone in a macrotidal estuary (the Gironde, France): observations from field and MODIS satellite data. Estuar Coast Shelf Sci 81(3):321–332. https://doi.org/10.1016/j.ecss.2008.11.013

    Article  Google Scholar 

  • Gage KL, Burkot TR, Eisen RJ, Hayes EB (2008) Climate and vectorborne diseases. Am J Prev Med 35(5):436–450. https://doi.org/10.1016/j.amepre.2008.08.030

    Article  Google Scholar 

  • Gálvez R, Descalzo MA, Miró G, Jiménez MI, Martín O, Dos Santos-Brandao F, Guerrero I, Cubero E, Molina R (2010) Seasonal trends and spatial relations between environmental/meteorological factors and leishmaniosis sand fly vector abundances in central Spain. Acta Trop 115(1-2):95–102. https://doi.org/10.1016/j.actatropica.2010.02.009

    Article  Google Scholar 

  • Gardner W, Mulvey EP, Shaw EC (1995) Regression analyses of counts and rates: Poisson, overdispersed Poisson, and negative binomial models. Psychol Bull 118(3):392–404. https://doi.org/10.1037/0033-2909.118.3.392

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Gohari A, Eslamian S, Abedi-Koupaei J, Bavani AM, Wang D, Madani K (2013) Climate change impacts on crop production in Iran’s Zayandeh-Rud River. Basin. Sci Total Environ 442:405–419. https://doi.org/10.1016/j.scitotenv.2012.10.029

    Article  CAS  Google Scholar 

  • Guernaoui S, Boumezzough A, Laamrani A (2006) Altitudinal structuring of sand flies (Diptera: Psychodidae) in the High-Atlas mountains (Morocco) and its relation to the risk of leishmaniasis transmission. Acta Trop 97:346–351

    Article  CAS  Google Scholar 

  • Han W, Di L, Zhao P, Shao Y (2012) DEM Explorer: an online interoperable DEM data sharing and analysis system. Environ Model Softw 38:101–107. https://doi.org/10.1016/j.envsoft.2012.05.015

    Article  Google Scholar 

  • Hanafi-Bojd AA, Yaghoobi-Ershadi MR, Haghdoost AA, Akhavan AA, Rassi Y, Karimi A, Charrahy Z (2015) Modeling the distribution of cutaneous leishmaniasis vectors (Psychodidae: Phlebotominae) in Iran: a potential transmission in disease prone areas. J Med Entomol 52(4):557–565. https://doi.org/10.1093/jme/tjv058

    Article  Google Scholar 

  • Hilbe JM (2011) Negative binomial regression. Cambridge University Press, DOI: https://doi.org/10.1017/CBO9780511973420

  • Holakouie-Naieni K, Mostafavi E, Boloorani AD, Mohebali M, Pakzad R (2017) Spatial modeling of cutaneous leishmaniasis in Iran from 1983 to 2013. Acta Trop 166:67–73

    Article  Google Scholar 

  • Karami M, Doudi M, Setorki M (2013) Assessing epidemiology of cutaneous leishmaniasis in Isfahan. Iran. J Vector Borne Dis 50:30

    Google Scholar 

  • Kasap ÖE, Belen A, Kaynas S, Simsek FM, Biler L, Ata N, Alten B (2009) Activity patterns of sand fly (Diptera: Psychodidae) species and comparative performance of different traps in an endemic cutaneous leishmaniasis focus in Cukurova Plain, southern Anatolia, Turkey. Acta Vet Brno 78(2):327–335. https://doi.org/10.2754/avb200978020327

    Article  Google Scholar 

  • Lemma A, Foster W, Gemetchu T, Preston P, Bryceson A, Minter D (1969) Studies on leishmaniasis in Ethiopia: I.—preliminary investigations into the epidemiology of cutaneous leishmaniasis in the highlands. Ann Trop Med Parasitol 63(4):455–472. https://doi.org/10.1080/00034983.1969.11686649

    Article  CAS  Google Scholar 

  • Maroli M, Gradoni L, Oliva G, Castagnaro M, Crotti A, Lubas G, Paltrinieri S, Roura X, Zini E, Zatelli A (2010) Guidelines for prevention of leishmaniasis in dogs. J Am Vet Med Assoc 236(11):1200–1206. https://doi.org/10.2460/javma.236.11.1200

    Article  CAS  Google Scholar 

  • Matos Guedes H, Carvalho R, Oliveira Gomes D, Rossi-Bergmann B, De-Simone S (2008) Oligopeptidase B-2 from Leishmania amazonensis with an unusual C-terminal extension. Acta Parasitol 53:197–204

    Article  Google Scholar 

  • Medlock JM, Hansford KM, Bortel WV, Zeller H, Alten B (2014) A summary of the evidence for the change in European distribution of phlebotomine sand flies (Diptera: Psychodidae) of public health importance. J Vector Ecol 39(1):72–77. https://doi.org/10.1111/j.1948-7134.2014.12072.x

    Article  Google Scholar 

  • Mokhtari M, Miri M, Nikoonahad A, Jalilian A, Naserifar R, Ghaffari HR, Kazembeigi F (2016) Cutaneous leishmaniasis prevalence and morbidity based on environmental factors in Ilam, Iran: spatial analysis and land use regression models. Acta Trop 163:90–97. https://doi.org/10.1016/j.actatropica.2016.08.002

    Article  Google Scholar 

  • Mollalo A, Alimohammadi A, Shirzadi M, Malek M (2015) Geographic information system-based analysis of the spatial and spatio-temporal distribution of zoonotic cutaneous leishmaniasis in Golestan Province, north-east of Iran. Zoonoses Public Health 62(1):18–28. https://doi.org/10.1111/zph.12109

    Article  CAS  Google Scholar 

  • Moran PA (1948) The interpretation of statistical maps. J R Stat Soc Ser B Methodol 10:243–251

    Google Scholar 

  • Nikonahad A et al (2017) A time series analysis of environmental and metrological factors impact on cutaneous leishmaniasis incidence in an endemic area of Dehloran, Iran. Environ Sci Pollut Res:1–7

  • Nilforoushzadeh MA, Bidabadi LS, Hosseini SM, Nobari RF, Jaffary F (2014) Cutaneous leishmaniasis in Isfahan Province, Iran, during 2001–2011. J Skin Stem Cell 1:2

    Article  Google Scholar 

  • Oliveira EF, Fernandes CES, Silva EA, Brazil RP, Oliveira AG (2013) Climatic factors and population density of Lutzomyia longipalpis (Lutz & Neiva, 1912) in an urban endemic area of visceral leishmaniasis in midwest Brazil. J Vector Ecol 38:224–228

    Article  Google Scholar 

  • Oliver MA, Webster R (1990) Kriging: a method of interpolation for geographical information systems. Int J Geogr Inf Syst 4(3):313–332. https://doi.org/10.1080/02693799008941549

    Article  Google Scholar 

  • R Core Team (2016) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Rajesh K, Sanjay K (2013) Change in global climate and prevalence of visceral leishmaniasis. Int J Sci Res Publ 3:1–2

    Google Scholar 

  • Ryan JR, Mbui J, Rashid JR, Wasunna MK, Kirigi G, Magiri C, Kinoti D, Ngumbi PM, Martin SK, Odera SO, Hochberg LP, Bautista CT, Chan AS (2006) Spatial clustering and epidemiological aspects of visceral leishmaniasis in two endemic villages, Baringo District, Kenya. Am J Trop Med Hyg 74(2):308–317

    Article  Google Scholar 

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

    Google Scholar 

  • Singh KV (1999) Studies on the role of climatological factors in the distribution of phlebotomine sandflies (Diptera: Psychodidae) in semi-arid areas of Rajasthan. India. J Arid Environ 42(1):43–48. https://doi.org/10.1006/jare.1999.0499

    Article  Google Scholar 

  • Tarallo VD, Dantas-Torres F, Lia RP, Otranto D (2010) Phlebotomine sand fly population dynamics in a leishmaniasis endemic peri-urban area in southern Italy. Acta Trop 116(3):227–234. https://doi.org/10.1016/j.actatropica.2010.08.013

    Article  Google Scholar 

  • Tian H-Y, Bi P, Cazelles B, Zhou S, Huang SQ, Yang J, Pei Y, Wu XX, Fu SH, Tong SL, Wang HY, Xu B (2015) How environmental conditions impact mosquito ecology and Japanese encephalitis: an eco-epidemiological approach. Environ Int 79:17–24. https://doi.org/10.1016/j.envint.2015.03.002

    Article  Google Scholar 

  • Toumi A, Chlif S, Bettaieb J, Alaya NB, Boukthir A, Ahmadi ZE, Salah AB (2012) Temporal dynamics and impact of climate factors on the incidence of zoonotic cutaneous leishmaniasis in central Tunisia. PLoS Negl Trop Dis 6(5):e1633. https://doi.org/10.1371/journal.pntd.0001633

    Article  Google Scholar 

  • Valderrama A, Tavares MG, Andrade Filho JD (2011) Anthropogenic influence on the distribution, abundance and diversity of sandfly species (Diptera: Phlebotominae: Psychodidae), vectors of cutaneous leishmaniasis in Panama. Mem Inst Oswaldo Cruz 106(8):1024–1031. https://doi.org/10.1590/S0074-02762011000800021

    Article  Google Scholar 

  • Wan Z, Wang P, Li X (2004) Using MODIS land surface temperature and normalized difference vegetation index products for monitoring drought in the Southern Great Plains, USA. Int J Remote Sens 25:61–72

    Article  Google Scholar 

  • World Health Organization (2009) A human rights-based approach to neglected tropical diseases. http://www.who.int/tdr/publications/tdr-research-publications/human-rights/en/index.html [Accessed 14 March 2017]

  • World Health Organization (2016) Leishmaniasis http://www.who.int/mediacentre/factsheets/fs375/en/ [Accessed 14 March 2017]

  • World Health Organization (2010) Control of the leishmaniases: report of a meeting of the WHO expert committee on the control of leishmaniases. In: Control of the leishmaniases: report of a meeting of the WHO expert committee on the control of leishmaniases. World Health Organization,

  • Wu X, Lu Y, Zhou S, Chen L, Xu B (2016) Impact of climate change on human infectious diseases: empirical evidence and human adaptation. Environ Int 86:14–23. https://doi.org/10.1016/j.envint.2015.09.007

    Article  Google Scholar 

  • Yaghoobi-Ershadi MR (2016) Control of Phlebotomine sand flies in Iran: a review article. J Arthropod Borne Dis 10:429

    Google Scholar 

  • Yaghoobi-Ershadi MR, Javadian E (1995) Zoonotic cutaneous leishmaniasis to the north of Isfahan. Human infection in 1991. Bull Soc Pathol Exot 88(1):42–5

    CAS  Google Scholar 

  • Yan J, Wang L (2016) Suitability evaluation for products generation from multisource remote sensing data. Remote Sens 8(12):995. https://doi.org/10.3390/rs8120995

    Article  Google Scholar 

  • Zhang X, Friedl MA, Schaaf CB, Strahler AH, Hodges JCF, Gao F, Reed BC, Huete A (2003) Monitoring vegetation phenology using MODIS. Remote Sens Environ 84(3):471–475. https://doi.org/10.1016/S0034-4257(02)00135-9

    Article  Google Scholar 

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Acknowledgements

The authors wish to acknowledge the CDC departments of Isfahan and also CDC of Ministry of Health and Medical Education in Tehran, which provided disease incident data. We also acknowledge Tehran Meteorological Center for providing the climate data.

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Correspondence to Roghieh Ramezankhani.

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Ramezankhani, R., Sajjadi, N., Nezakati esmaeilzadeh, R. et al. Climate and environmental factors affecting the incidence of cutaneous leishmaniasis in Isfahan, Iran. Environ Sci Pollut Res 25, 11516–11526 (2018). https://doi.org/10.1007/s11356-018-1340-8

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