Hostname: page-component-cb9f654ff-d5ftd Total loading time: 0 Render date: 2025-08-07T05:27:57.712Z Has data issue: false hasContentIssue false
  • English
  • Français

Environmental and climatic risk factors of human cystic echinococcosis in the northeast of Iran

Published online by Cambridge University Press:  25 July 2025

R. Shafiei ,
A. Gholami ,
M.F. Farmad ,
M. Pakdaman ,
H.R. Shoraka ,
K. Arzamani ,
Z. Kanannejad  and
M.A. Ghatee Open the ORCID record for M.A. Ghatee [Opens in a new window]
R. Shafiei
Affiliation:
Vector-Borne Diseases Research Center, https://ror.org/0536t7y80 North Khorasan University of Medical Sciences , Bojnurd, Iran
A. Gholami
Affiliation:
Department of Pharmaceutical Nanotechnology, Faculty of Pharmacy, https://ror.org/01c4pz451 Tehran University of Medical Sciences , Tehran, Iran
M.F. Farmad
Affiliation:
Shahid Beheshti Hospital, School of Medical Sciences, https://ror.org/04sfka033 Mashhad University of Medical Sciences , Mashhad, Iran
M. Pakdaman
Affiliation:
https://ror.org/007jfm765 Imam Reza International University , Razavi Khorasan, Mashhad, Iran
H.R. Shoraka
Affiliation:
Public Health Group, School of Medical Sciences, Esfarayen Faculty of Medical Sciences, Esfahan, Iran
K. Arzamani
Affiliation:
Vector-Borne Diseases Research Center, https://ror.org/0536t7y80 North Khorasan University of Medical Sciences , Bojnurd, Iran
Z. Kanannejad*
Affiliation:
Allergy Research Center, https://ror.org/01n3s4692 Shiraz University of Medical Sciences , Shiraz, Iran
M.A. Ghatee*
Affiliation:
Professor Alborzi Clinical Microbiology Research Center, https://ror.org/01n3s4692 Shiraz University of Medical Sciences , Shiraz, Iran Department of Microbiology, School of Medicine, https://ror.org/037s33w94 Yasuj University of Medical Sciences , Yasuj, Iran
*
Corresponding authors: M.A. Ghatee and Z. Kanannejad; Emails: ghateea1980@gmail.com; zkanannejad@gmail.com
Corresponding authors: M.A. Ghatee and Z. Kanannejad; Emails: ghateea1980@gmail.com; zkanannejad@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Cystic echinococcosis (CE) is a significant zoonotic helminthic disease with considerable public health and economic impact in endemic regions. We aimed to analyse the climatic and environmental factors affecting the human CE cases in North Khorasan Province, northeast Iran. Using a geographic information system, we map the addresses of 316 hospitalised CE patients from 2012 to 2022 and examined the influence of climatic variables, altitude, and land cover on CE case distribution. Data were analysed using logistic regression models. Most patients were female (58.9%) and aged 21–60 years (67.4%), with liver involvement being the most common (57.3%). The multivariate model identified urban settings, irrigated and dry farms, soil temperature, and humidity as the most important geoclimatic determinants, respectively. In contrast, gardens, moderate and excellent rangelands, minimum, maximum, and mean air temperatures, and rainfall were only found to be significant factors in univariate models. High-risk areas for CE include urban and suburban regions, surrounding fields, and pastures where stray dogs and wild canids roam, livestock husbandries are present, and residents consume unsanitised vegetables. Additionally, areas with lower soil and weather temperatures and higher humidity conditions that may enhance the survival of E. granulosus eggs dispersed by canids were identified as high-risk zones. Health managers can use these findings to prioritise control programs and allocate limited resources to these areas, ultimately reducing the future incidence of CE.

Keywords

CEnortheast IranGISenvironmental factorsclimatic factors

Information

Type
Research Paper
Information
Journal of Helminthology , Volume 99 , 2025 , e79
Copyright
© The Author(s), 2025. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Atkinson, J. M., Gray, D. J., Clements, A. C. A., Barnes, T. S., McManus, D. P., & Yang, Y. R. (2012). Environmental changes impacting Echinococcus transmission: research to support predictive surveillance and control. Global Change Biology 19(3), 677–688. Portico. https://doi.org/10.1111/gcb.12088CrossRefGoogle ScholarPubMed
Barosi, R and Umhang, G (2024) Presence of Echinococcus eggs in the environment and food: a review of current data and future prospects. Parasitology 1–16. https://doi.org/10.1017/s0031182024000945.CrossRefGoogle Scholar
Borhani, M, Fathi, S, Lahmar, S, Ahmed, H, Abdulhameed, MF and Fasihi Harandi, M (2020) Cystic echinococcosis in the Eastern Mediterranean region: Neglected and prevailing! PLoS Negl Trop Dis 14(5), e0008114. https://doi.org/10.1371/journal.pntd.0008114.CrossRefGoogle ScholarPubMed
Cadavid Restrepo, AM, Yang, YR, McManus, DP, Gray, DJ, Giraudoux, P, Barnes, TS, Williams, GM, Soares, , Magalhães, RJ, Hamm, NA and Clements, AC (2016) The landscape epidemiology of echinococcoses. Infect Dis Poverty 5, 13. https://doi.org/10.1186/s40249-016-0109-x.CrossRefGoogle ScholarPubMed
Colombe, S, Togami, E, Gelaw, F, Antillon, M, Fuentes, R and Weinberger, DM (2017) Trends and correlates of cystic echinococcosis in Chile: 2001-2012. PLoS Negl Trop Dis 11(9), e0005911. https://doi.org/10.1371/journal.pntd.0005911.CrossRefGoogle ScholarPubMed
Cromley, EK (2003) GIS and disease. Annu Rev Public Health 24, 7–24. https://doi.org/10.1146/annurev.publhealth.24.012902.141019.CrossRefGoogle ScholarPubMed
Ebrahimipour, M, Budke, CM and Harandi, MF (2020) Control of Cystic Echinococcosis in Iran: Where Do We Stand? Trends Parasitol 36(7), 578–581. https://doi.org/10.1016/j.pt.2020.04.007.CrossRefGoogle ScholarPubMed
Ebrahimipour, M, Budke, CM, Najjari, M, Cassini, R and Asmarian, N (2016) Bayesian spatial analysis of the surgical incidence rate of human cystic echinococcosis in north-eastern Iran. Acta Trop 163, 80–86. https://doi.org/10.1016/j.actatropica.2016.08.003.CrossRefGoogle ScholarPubMed
Eslami, A and Hosseini, SH (1998) Echinococcus granulosus infection of farm dogs of Iran. Parasitol Res 84(3), 205–207. https://doi.org/10.1007/s004360050383.CrossRefGoogle ScholarPubMed
Fakhar, M, Karamian, M, Ghatee, MA, Taylor, WR, Pazoki Ghohe, H and Rasooli, SA (2017) Distribution pattern of anthroponotic cutaneous leishmaniasis caused by Leishmania tropica in Western Afghanistan during 2013-2014. Acta Trop 176, 22–28. https://doi.org/10.1016/j.actatropica.2017.07.028.CrossRefGoogle ScholarPubMed
Fasihi Harandi, M, Budke, CM and Rostami, S (2012) The monetary burden of cystic echinococcosis in Iran. PLoS Negl Trop Dis 6(11), e1915. https://doi.org/10.1371/journal.pntd.0001915.CrossRefGoogle ScholarPubMed
Firouzeh, N, Eslaminejad, T, Shafiei, R, Faridi, A and Fasihi, Harandi M (2021) Lethal in vitro effects of optimized chitosan nanoparticles against protoscoleces of Echinococcus granulosus. Journal of Bioactive and Compatible Polymers 36(3), 237–248.CrossRefGoogle Scholar
Flores, V, Viozzi, G, Rauque, C, Mujica, G, Herrero, E, Ballari, SA, Ritossa, L, Miori, G, Garibotti, G, Zacharias, DG, Treuque, J, Reissig, EC, Vázquez, G, Pierangeli, N and Lazzarini, L (2022) A cross-sectional study of free-roaming dogs in a Patagonian city: Their distribution and intestinal helminths in relation to socioeconomic aspects of neighborhoods. Vet Parasitol Reg Stud Reports 33, 100747. https://doi.org/10.1016/j.vprsr.2022.100747.Google Scholar
Ghatee, MA, Haghdoost, AA, Kooreshnia, F, Kanannejad, Z, Parisaie, Z, Karamian, M and Moshfe, A (2018) Role of environmental, climatic risk factors and livestock animals on the occurrence of cutaneous leishmaniasis in newly emerging focus in Iran. J Infect Public Health 11(3), 425–433. https://doi.org/10.1016/j.jiph.2017.12.004.CrossRefGoogle ScholarPubMed
Ghatee, MA, Nikaein, K, Taylor, WR, Karamian, M, Alidadi, H, Kanannejad, Z, Sehatpour, F, Zarei, F and Pouladfar, G (2020) Environmental, climatic and host population risk factors of human cystic echinococcosis in southwest of Iran. BMC Public Health 20(1), 1611. https://doi.org/10.1186/s12889-020-09638-w.CrossRefGoogle ScholarPubMed
Gholami, S, Tanzifi, A, Sharif, M, Daryani, A, Rahimi, MT, Mirshafiee, S and Sarvi, S (2018) Demographic aspects of human hydatidosis in Iranian general population based on serology: A systematic review and meta-analysis. Vet World 11(10), 1385–1396. https://doi.org/10.14202/vetworld.2018.1385-1396.CrossRefGoogle ScholarPubMed
Harriott, L, Gentle, M, Traub, R, Cobbold, R and Soares Magalhães, R (2019) Geographical distribution and risk factors for Echinococcus granulosus infection in peri-urban wild dog populations. Int J Parasitol Parasites Wildl 10, 149–155. https://doi.org/10.1016/j.ijppaw.2019.08.005.CrossRefGoogle ScholarPubMed
Heidari, Z, Sharbatkhori, M, Mobedi, I, Mirhendi, SH, Nikmanesh, B, Sharifdini, M, Mohebali, M, Zarei, Z, Arzamani, K and Kia, EB (2019) Echinococcus multilocularis and Echinococcus granulosus in canines in North-Khorasan Province, northeastern Iran, identified using morphology and genetic characterization of mitochondrial DNA. Parasit Vectors 12(1), 606. https://doi.org/10.1186/s13071-019-3859-z.CrossRefGoogle ScholarPubMed
Huang, D, Li, R, Qiu, J, Sun, X, Yuan, R, Shi, Y, Qu, Y and Niu, Y (2018) Geographical Environment Factors and Risk Mapping of Human Cystic Echinococcosis in Western China. Int J Environ Res Public Health 15(8). https://doi.org/10.3390/ijerph15081729.CrossRefGoogle ScholarPubMed
Jamshidi, A, Haniloo, A, Fazaeli, A and Ghatee, MA (2020) Effects of geographical and climatic factors on cystic echinococcosis in south-western Iran. J Helminthol 94, e175. https://doi.org/10.1017/s0022149x20000553.CrossRefGoogle ScholarPubMed
Kanannejad, AM, Ramshk, O and Khoramrooz, S (2020) Environmental and climatic factors influencing the occurrence and distri-bution of tuberculosis in southwest Iran: A GIS-based study. Acta Medica 36, 563.Google Scholar
Karamian, M, Haghighi, F, Hemmati, M, Taylor, WR, Salehabadi, A and Ghatee, MA (2017) Heterogenity of Echinococcus canadensis genotype 6 - the main causative agent of cystic echinococcosis in Birjand, Eastern Iran. Vet Parasitol 245, 78–85. https://doi.org/10.1016/j.vetpar.2017.08.018.CrossRefGoogle ScholarPubMed
Khalkhali, HR, Foroutan, M, Khademvatan, S, Majidiani, H, Aryamand, S, Khezri, P and Aminpour, A (2018) Prevalence of cystic echinococcosis in Iran: a systematic review and meta-analysis. J Helminthol 92(3), 260–268. https://doi.org/10.1017/s0022149x17000463.CrossRefGoogle ScholarPubMed
Khazaei, S, Rezaeian, S, Khazaei, Z, Goodarzi, E, Khazaei, S, Mohammadian, M, Salehiniya, H, Ayubi, E and Mohammadian-Hafshejani, A (2016) Epidemiological and clinical characteristics of patients with hydatid cysts in Khorasan Razavi province, from 2011 to 2014. Iran J Parasitol 11(3), 364–370.Google ScholarPubMed
Laws, GF (1968) Physical factors influencing survival of taeniid eggs. Exp Parasitol 22(2), 227–239. https://doi.org/10.1016/0014-4894(68)90097-0.CrossRefGoogle ScholarPubMed
Neumayr, A, Tamarozzi, F, Goblirsch, S, Blum, J and Brunetti, E (2013) Spinal cystic echinococcosis--a systematic analysis and review of the literature: part 2. Treatment, follow-up and outcome. PLoS Negl Trop Dis 7(9), e2458. https://doi.org/10.1371/journal.pntd.0002458.CrossRefGoogle ScholarPubMed
Piarroux, M, Gaudart, J, Bresson-Hadni, S, Bardonnet, K, Faucher, B, Grenouillet, F, Knapp, J, Dumortier, J, Watelet, J, Gerard, A, Beytout, J, Abergel, A, Wallon, M, Vuitton, DA, and Piarroux, R (2015) Landscape and climatic characteristics associated with human alveolar echinococcosis in France, 1982 to 2007. Euro Surveill 20(18). https://doi.org/10.2807/1560-7917.es2015.20.18.21118.CrossRefGoogle ScholarPubMed
Sánchez Thevenet, P, Alvarez, HM, Torrecillas, C, Jensen, O and Basualdo, JA (2019) Dispersion of Echinococcus granulosus eggs from infected dogs under natural conditions in Patagonia, Argentina. J Helminthol 94, e29. https://doi.org/10.1017/s0022149x19000038.CrossRefGoogle ScholarPubMed
Shafiei, R, Ghatee, MA, Jafarzadeh, F, Javanshir, Z and Karamian, M (2019) Genotyping and phylogenetic analysis of unusually located hydatid cysts isolated from humans in north-east Iran. J Helminthol 94, e64. https://doi.org/10.1017/s0022149x19000579.CrossRefGoogle ScholarPubMed
Shafiei, R, Mohajerzadeh, MS, Masomi, HFA, Tavakoli, M, Turki, H and Firouzeh, N (2024) discordance therapeutic protocol of cystic echinococcosis with WHO Guideline: A descriptive study based on liver ultra-sonographic data in North Khorasan province, northeastern of Iran. J Ultrasound Med 43(7), 1279–1287. https://doi.org/10.1002/jum.16452.CrossRefGoogle ScholarPubMed
Shafiei, R, Taghasi, F, Hashemi, SA, Panahi, Y, Arefkhah, N, Omidian, M, Arianfar, F, Mostafavi-Pour, Z and Sarkari, B (2021) Seroprevalence of cystic echinococcosis using recombinant antigen B-ELISA in North Khorasan province, northeast of Iran. Iran J Public Health 50(3), 592–597. https://doi.org/10.18502/ijph.v50i3.5605.Google ScholarPubMed
Shafiei, R, Teshnizi, SH, Kalantar, K, Gholami, M, Mirzaee, G and Mirzaee, F (2016) The seroprevalence of human cystic echinococcosis in Iran: A systematic review and meta-analysis study. J Parasitol Res 2016, 1425147. https://doi.org/10.1155/2016/1425147.CrossRefGoogle ScholarPubMed
Torgerson, PR, Shaikenov, BS, Rysmukhambetova, AT, Ussenbayev, AE, Abdybekova, AM and Burtisurnov, KK (2003) Modelling the transmission dynamics of Echinococcus granulosus in dogs in rural Kazakhstan. Parasitology 126(Pt 5), 417–424. https://doi.org/10.1017/s0031182003002932.CrossRefGoogle ScholarPubMed
Varcasia, A, Tanda, B, Giobbe, M, Solinas, C, Pipia, AP, Malgor, R, Carmona, C, Garippa, G and Scala, A (2011) Cystic echinococcosis in Sardinia: farmers’ knowledge and dog infection in sheep farms. Vet Parasitol 181(2–4), 335–340. https://doi.org/10.1016/j.vetpar.2011.05.006.CrossRefGoogle ScholarPubMed
Veit, P, Bilger, B, Schad, V, Schäfer, J, Frank, W and Lucius, R (1995) Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitology 110(Pt 1), 79–86. https://doi.org/10.1017/s0031182000081075.CrossRefGoogle ScholarPubMed
Wachira, TM, Macpherson, CN and Gathuma, JM (1991) Release and survival of Echinococcus eggs in different environments in Turkana, and their possible impact on the incidence of hydatidosis in man and livestock. J Helminthol 65(1), 55–61. https://doi.org/10.1017/s0022149x00010440.CrossRefGoogle ScholarPubMed
Wang, L, Wang, Z, Qin, M, Lei, J, Cheng, X, Yan, J, Gavotte, L and Frutos, R (2024) A regressive analysis of the main environmental risk factors of human echinococcosis in 370 counties in China. PLoS Negl Trop Dis 18(5), e0012131. https://doi.org/10.1371/journal.pntd.0012131.CrossRefGoogle ScholarPubMed
Yang, YR, Clements, AC, Gray, DJ, Atkinson, JA, Williams, GM, Barnes, TS and McManus, DP (2012) Impact of anthropogenic and natural environmental changes on Echinococcus transmission in Ningxia Hui Autonomous Region, the People’s Republic of China. Parasit Vectors 5, 146. https://doi.org/10.1186/1756-3305-5-146.CrossRefGoogle ScholarPubMed
Yin, J, Wu, X, Li, C, Han, J and Xiang, H (2022) The impact of environmental factors on human echinococcosis epidemics: spatial modelling and risk prediction. Parasit Vectors 15(1), 47. https://doi.org/10.1186/s13071-022-05169-y.CrossRefGoogle ScholarPubMed
Zeng, XM, Wang, LY, Wu, WP, Guan, YY and Fang, Q (2014) [Cluster analysis of cystic echinococcosis in non Tibetan Plateau regions]. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi 26(2), 180–183.Google ScholarPubMed