Abstract
Alveolar echinococcosis (AE) is a zoonosis caused by Echinococcus multilocularis, a heteroxenous parasite belonging to Cestoda class. AE is currently considered an important public health issue, but epidemiological and notably molecular data from several endemic countries, including Pakistan, are sparse. Here we report the first detection of Echinococcus multilocularis in wildlife from Pakistan after real-time PCR and sequencing confirmation in the faecal samples of three foxes from northern Kaghan and Siran regions. The occurrence is estimated at 4.4% (95% CI 0.9–12.4). In order to go further in the epidemiological investigations on E. multilocularis and due to the potential presence of other Echinococcus species, we suggest the need for further epidemiological surveys targeting E. multilocularis and E. granulosus sensu lato isolates from humans and intermediate hosts as well as definitive hosts from wildlife in Pakistan.
This is a preview of subscription content, log in via an institution to check access.
References
Ahmed H, Ali S, Afzal MS, Khan AA, Raza H, Shah ZH, Simsek S (2017) Why more research needs to be done on echinococcosis in Pakistan. Infect Dis Poverty 6(1):90. https://doi.org/10.1186/s40249-017-0309-z
Aikat BK, Bhusnurmath SR, Cadersa M, Chhuttani PN, Mitra SK (1978) Echinococcus multilocoularis infection in India: first case report proved at autopsy. Trans Royal Soc Trop Med Hyg 72:619–621. https://doi.org/10.1016/0035-9203(78)90015-9
Al-Attar HK, Al-Irhayin B, Al-Habbal MJ (1983) Alveolar hydatid disease of the liver: first case report from man in Iraq. Ann Trop Med Parasitol 77:595–597. https://doi.org/10.1080/00034983.1983.11811758
Ali I, Panni MK, Iqbal A, Munir I, Ahmad S, Ali A (2015) Molecular characterization of echinococcus species in Khyber Pakhtunkhwa, Pakistan. Acta Sci Vet 43:1–7
Ali SA, Akhtar T, Zaki MA, Safi WA et al (2013) Echinococcosis is an emerging public health problem in Pakistan. Int J O Med Pharmaceutical Sci 3(2):39–48
Alvarez Rojas CA, Kronenberg PA, Aitbaev S, Omorov RA, Abdykerimov KK, Paternoster G, Müllhaupt B, Torgerson P, Deplazes P (2020) Genetic diversity of Echinococcus multilocularis and Echinococcus granulosus sensu lato in Kyrgyzstan: the A2 haplotype of E. multilocularis is the predominant variant infecting humans. PLoS Negl Trop Dis 13;14(5):e0008242. https://doi.org/10.1371/journal.pntd.0008242
Bessonov AS (1998) Echinococcus multilocularis infection in Russia and neighbouring countries. Helmintholog 35:73–78
Budke CM, Campos-Ponce M, Qian W, Torgerson PR (2005a) A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan plateau. Vet Parasitol 127:43–49. https://doi.org/10.1016/j.vetpar.2004.08.024
Budke CM, Jiamin Q, Zinsstag J, Qian W, Torgerson PR (2004) Use of disability adjusted life years in the estimation of the disease burden of echinococcosis for a high endemic region of the Tibetan plateau. Am J Trop Med Hyg 71:56–64
Budke CM, Jiamin Q, Craig PS, Torgerson PR (2005b) Modeling the transmission of Echinococcus granulosus and Echinococcus multilocularis in dogs for a high endemic region of the Tibetan plateau. Int J Parasitol 35:163–170. https://doi.org/10.1016/j.ijpara.2004.10.026
Conraths FJ, Probst C, Possenti A, Boufana B, Saulle R, La Torre G et al (2017) Potential risk factors associated with human alveolar echinococcosis: systematic review and meta-analysis. PLoS Negl Trop Dis 11(7):e0005801. https://doi.org/10.1371/journal.pntd.0005801
Craig PS, Deshan L, Macpherson CNL, Dazhong S, Reynolds D et al (1992) A large focus of alveolar echinococcosis in Central China. Lancet 340:826–831. https://doi.org/10.1016/0140-6736(92)92693-a
Craig PS, Giraudoux P, Shi D, Bartholomot B, Barnish G, Delattre P, Quere JP, Harraga S, Bao G, Wang Y, Lu F, Ito A, Vuitton DA (2000) An epidemiological and ecological study of human alveolar echinococcosis transmission in South Gansu, China. Acta Trop 77:167–177. https://doi.org/10.1016/s0001-706x(00)00134-0
Craig PS (2006) Echinococcosis Working Group in China. Epidemiology of human alveolar echinococcosis in China. Parasitol Int 55(Suppl):S221–S225. https://doi.org/10.1016/j.parint.2005.11.034
Deplazes P, Rinaldi L, Alvarez Rojas CA, Torgerson PR, Harandi MF, Romig T, Antolova D, Schurer JM, Lahmar S, Cringoli G, Magambo J, Thompson RC, Jenkins EJ (2017) Global distribution of alveolar and cystic Echinococcosis. Advan in Parasitol 95:315–493. https://doi.org/10.1016/bs.apar.2016.11.001
Danson FM, Craig PS, Man W, Shi D, Giraudoux P (2004) Landscape dynamics and risk modeling of human alveolar echinococcosis. Photogramm Eng Remote Sens 70:359–366
Danson FM, Graham AJ, Pleydell DRJ, Campos-Ponce M, Giraudoux P, Craig PS (2003) Multi-scale spatial analysis of human alveolar echinococcosis risk in China. Parasitolog 127:133–141
Din JU, Nawaz MA (2010) Status of the Himalayan lynx in district Chitral, NWFP, Pakistan. J Anim Plant Sci 20:17–22
Din JU, Hameed S, Shah KA, Khan MA, Khan S, Ali M, Nawaz MA (2013) Assessment of canid abundance and conflict with humans in the Hindu Kush Mountain Range of Pakistan. Wildlife Biol Pract 9(2)
Ehsan M, Akhter N, Bhutto B, Arijo A, Gadahi JA (2017) Prevalence and genotypic characterization of bovine Echinococcus granulosus isolates by using cytochrome oxidase 1 (Co1) gene in Hyderabad, Pakistan. Vet Parasitol 239:80–85. https://doi.org/10.1016/j.vetpar.2017.04.006
Heywood VH (1995) Global biodiversity assessment. Cambridge University Press, Cambridge
Hussain I, Cheema AM, Khan AA (2003) Small rodents in the crop ecosystem of Pothwar Plateau, Pakistan. Wildl Res 30:269–274. https://doi.org/10.1071/WR01025
Geramizadeh B, Baghernezhad M (2016) Hepatic alveolar hydatid cyst: a brief review of published cases from Iran in the last 20 years. Hepat Mon 16(10):e38920. https://doi.org/10.5812/hepatmon.38920
Geramizadeh B, Nikeghbalian S, Malekhosseini SA (2012) Alveolar echinococcosis of the liver: report of three cases from different geographic areas of Iran. Hepat Mon 12(9):e6143. https://doi.org/10.5812/hepatmon.6143
Giraudoux P, Raoul F, Afonso E, Ziadinov I, Yang Y, Li L et al (2013a) Transmission ecosystems of Echinococcus multilocularis in China and Central Asia. Parasitolog 140:1655–1666. https://doi.org/10.1017/S0031182013000644
Giraudoux P, Zhao Y, Afonso E, Yan H, Knapp J, Rogan MT, Shi DZ, Jia WZ, Craig PS (2019) Long-term retrospective assessment of a transmission hotspot for human alveolar echinococcosis in midwest China. PLoS Negl Trop Dis 13(8):e0007701. https://doi.org/10.1371/journal.pntd.0007701
Giraudoux P, Craig PS, Delattre P, Bartholomot B, Bao G, Barnish G, Harraga S, Quéré JP, Raoul F, Wang YH, Shi D, Vuitton D (2003) Interactions between landscape changes and host communities can regulate Echinococcus multilocularis transmission. Parasitolog 127:121–131
Giraudoux P, Pleydell D, Raoul F, Quere JP, Wang Q, Yang YR, Vuitton DA, Qiu JM, Yang W, Craig PS et al (2006) Transmission ecology of Echinococcus multilocularis: what are the ranges of parasite stability among various host communities in China? Parasitol Int 55:237–246
Giraudoux P, Raoul F, Pleydell D, Li TY, Han XM, Qiu JM, Xie Y, Wang H, Ito A, Craig PS (2013b) Drivers of Echinococcus multilocularis transmission in China: host biodiversity, landscape or climate? PLoS Negl Trop Dis 7:e2045
Ito A, Nakao M, Sako Y (2007) Echinococcosis: serological detection of patients and molecular identification of parasites. Future Microbiol 2(4):439–449. https://doi.org/10.2217/17460913.2.4.439
Ito A, Romig T, Takahashi K (2003) Perspective on control options for Echinococcus multilocularis with particular reference to Japan. Parasitolog 127(suppl):S159–S172
Jiang WB, Liu N, Zhang GT, Renqing PC, Xie F, Li TY, Wang ZH, Wang XM (2012) Specific detection of Echinococcus spp. from the Tibetan fox (Vulpes ferrilata) and the red fox (V. vulpes) using copro-DNA PCR analysis. Parasitol Res 111:1531–1539. https://doi.org/10.1007/s00436-012-2993-8
Khan A, Ahmed H, Simsek S (2018b) Molecular epidemiology of Echinococcus species in Pakistan. Asian Pacific J Trop Med 11(S1):37
Khan A, Ahmed H, Budke CM (2019a) Echinococcosis in Pakistan: a call for research. Lancet Infect Dis 19:581. https://doi.org/10.1016/S1473-3099(19)30221-X
Khan A, Ahmed H, Khan H, Simsek S, Afzal MS, Kilinc SG, Noo N, Zahoor S, Afzal MS, Mansur H, Irum S, Simsek S (2018a) A retrospective analysis on the cystic Echinococcosis (CE) cases occured in northeastern Punjab Province, Pakistan. Korean J Parasitol 56:1–6
Khan A, Ahmed H, Simsek S (2019b) Make headway for echinococcosis; take along the ignored cases. Iranian J Parasitol 14:497–498 https://pubmed.ncbi.nlm.nih.gov/31673272
Khan A, Ahmed H, Simsek S (2019c) War, migration, refugees and cystic Echinococcosis. Travel Med Infect Dis (28):111–112. https://doi.org/10.1016/j.tmaid.2018.09.012
Khan A, Ahmed H, Simsek S, Afzal MS, Cao J (2020a) Spread of cystic echinococcosis in Pakistan due to stray dogs and livestock slaughtering habits: research priorities and public health importance. Front Public Health 7:412. https://doi.org/10.3389/fpubh.2019.00412
Khan A, Ahmed H, Simsek S, Liu H, Yin J, Wang Y, Shen Y, Cao J (2020b) Molecular characterization of human Echinococcus isolates and the first report of E. canadensis (G6/G7) and E. multilocularis from the Punjab Province of Pakistan using sequence analysis. BMC Infect Dis 20(1):262. https://doi.org/10.1186/s12879-020-04989-6
Khuroo MS, Datta DV, Khoshy A, Mitra SK, Chhuttani PN (1980) Alveolar hydatid disease of the liver with Budd-Chiari syndrome. Postgrad Med J 56:197–201. https://doi.org/10.1136/pgmj.56.653.197
Kim SJ, Kim JH, Han SY, Kim YH, Cho JH, Chai JY, Jeong JS (2011) Recurrent hepatic alveolar echinococcosis: report of the first case in Korea with unproven infection route. Korean J Parasitol 49(4):413–418. https://doi.org/10.3347/kjp.2011.49.4.413
Knapp J, Umhang G, Poulle ML, Millon L (2016) Development of a real-time PCR for a sensitive one-step coprodiagnosis allowing both the identification of carnivore feces and the detection of Toxocara spp. and Echinococcus multilocularis. Appl Environ Microbiol 2016 82(10):2950–2958. https://doi.org/10.1128/AEM.03467-15
Lass A, Ma L, Kontogeorgos I, Xueyong Z, Li X, Karanis P (2020) Contamination of wastewater with Echinococcus multilocularis-possible implications for drinking water resources in the QTP China. Water Res 170:115334. https://doi.org/10.1016/j.watres.2019.115334
Latif AA, Tanveer A, Maqbool A, Siddiqi N, Kyaw-tanner M, Traub RJ (2010) Morphological and molecular characterization of Echinococcus granulosus in livestock and humans in Punjab, Pakistan. Vet Parasitol 170(1–2):44–49. https://doi.org/10.1016/j.vetpar.2010.02.003
Molur S (2008) Alticola argentatus. The IUCN red list of threatened species 2008. Available: https://doi.org/10.2305/IUCN.UK.2008.RLTS.T949A13097559.en Accessed: 10 June 2015
Mirzanejad-Asl H (2019) Echinococcus contamination ratio and its r elated risk factors in Moghan plain, northwest of Iran. Trop Parasitol 9(2):83–87
Muqaddas H, Arshad M, Ahmed H, Mehmood N, Khan A, Simsek S (2019) Retrospective study of cystic Echinococcosis (CE) based on hospital record from five major metropolitan cities of Pakistan. Acta Parasitol 64(4):866–872. https://doi.org/10.2478/s11686-019-00109-w
Oksanen A, Siles-Lucas M, Karamon J, Possenti A, Conraths FJ, Romig T, Boufana B (2016) The geographical distribution and prevalence of Echinococcus multilocularis in animals in the European Union and adjacent countries: a systematic review and meta-analysis. Parsites Vect 9(1):519. https://doi.org/10.1186/s13071-016-1746-4
Panhwar (1990) On uniqueness of Dadu District Sindh. J Sindhological Studies 2(23):32
Pleydell DRJ, Yang YR, Danson FM, Raoul F, Craig PS, McManus DP et al (2008) Landscape composition and spatial prediction of alveolar echinococcosis in Southern Ningxia, China. PLoS Negl Trop Dis 2:e287. https://doi.org/10.1371/journal.pntd.0000287
Roberts TJ (1997) The mammals of Pakistan, Revised edn. Oxford University Press, Karachi, Pakistan
Satoh M, Nakaya K, Nakao M et al (2005) Short report: Echinococcus multilocularis confirmed on Kunashiri Island, 15 kilometers from the eastern part of Hokkaido, Japan. Am J Trop Med Hyg 72(3):284–288 https://pubmed.ncbi.nlm.nih.gov/15772322
Shaikenov BS (2006) Distribution and ecology of Echinococcus multilocularis in Central Asia. Parasitol Int 55:S213–S219. https://doi.org/10.1016/j.parint.2005.11.033
Shaikenov BS, Torgerson PR (2002) Distribution of Echinococcus multilocularis in Kazakhstan. In Cestode Zoonoses: echinococcosis and cysticercosis: an emergent and global problem (ed. Craig, P. and Pawlowski, Z.), pp. 299–307. IOS Press, Amsterdam
Sheikh KM, Molur S (2004) (Eds.) Status and red list of Pakistan’s mammals. Based on the Conservation Assessment and Management Plan. IUCN, Pakistan. pp.312
Tang CT, Quian YC, Kang YM, Cui GW, Lu HC, Shu LM, Wang YH, Tang L (2004) Study on the ecological distribution of alveolar Echinococcus in Hulunbeier Pasture of Inner Mongolia, China. Parasitolog 128:187–194. https://doi.org/10.1017/s0031182003004438
Tang CT, Wang YH, Peng WF, Tang L, Chen D (2006) Alveolar Echinococcus species from Vulpes corsac in Hulunbeier, Inner Mongolia, China, and differential development of the metacestodes in experimental rodents. J Parasitolog 92:719–724. https://doi.org/10.1645/GE-3526.1
Torgerson PR, Keller K, Magnotta M, Ragland N (2010) The global burden of alveolar echinococcosis. PLoS Negl Trop Dis 4(6):e722. https://doi.org/10.1371/journal.pntd.0000722
Vaniscotte A, Raoul F, Poulle ML, Romig T, Dinkel A, Takahashi K, Guislain MH, Moss J, Tiaoying L, Wang Q, Qi J, Craig PS, Giraudoux P (2011) Role of dog behaviour and environmental fecal contamination in transmission of Echinococcus multilocularis in Tibetan communities. Parasitolog 138:1316–1329. https://doi.org/10.1017/S0031182011000874
Veit P, Bilger B, Schad V, Schäfer J, Frank W, Lucius R (1995) Influence of environmental factors on the infectivity of Echinococcus multilocularis eggs. Parasitolog 110:79–86. https://doi.org/10.1017/s0031182000081075
Wang Q, Vuitton DA, Qiu JM, Giraudoux P, Xiao YF, Schantz PM, Raoul F, Li TY, Yang W, Craig PS (2004) Fenced pasture: a possible risk factor for human alveolar echinococcosis in Tibetan pastoralist communities of Sichuan, China. Act Trop 90:285–293. https://doi.org/10.1016/j.actatropica.2004.02.004
Wang Q, Vuitton DA, Xiao YF, Budke CM, Campos-Ponce M, Schantz PM, Raoul F, Yang W, Craig PS, Giraudoux P (2006) Pasture types and Echinococcus multilocularis, Tibetan communities. Emerg Infect Dis 12:1008–1010. https://doi.org/10.3201/eid1206.041229
Waqas A, Athar H (2019) Recent decadal variability of daily observed temperatures in Hindukush, Karakoram and Himalaya region in northern Pakistan. Clim Dyn 52:6931–6951. https://doi.org/10.1007/s00382-018-4557-9
Wu W, Wang H, Wang Q, Zhou X, Wang L, Zheng C et al (2018) A nationwide sampling survey on echinococcosis in China during 2012–2016. Chin J Parasitol Parasit Dis 1:1–14
Yamamoto N, Kishi R, Katakura Y, Miyake H (2001) Risk factors for human alveolar echinococcosis: a case-control study in Hokkaido, Japan. Ann Trop Med Parasitol 95(7):689–696. https://doi.org/10.1080/00034980120103252
Zhang W, Zhang Z, Wu W et al (2015) Epidemiology and control of echinococcosis in central Asia, with particular reference to the People’s Republic of China. Acta Trop 141(Pt B):235–243. https://doi.org/10.1016/j.actatropica.2014.03.014
Ziadinov I, Deplazes P, Mathis A, Mutunova B, Abdykerimov K, Nurgaziev R, Torgerson PR (2010) Frequency distribution of Echinococcus multilocularis and other helminths of foxes in Kyrgyzstan. Vet Parasitol 171(3–4):286–292. https://doi.org/10.1016/j.vetpar.2010.04.006
Ziadinov I, Mathis A, Trachsel D, Rysmukhambetova AT, Abdyjaparov TA, Kuttubaev OT, Deplazes P, Torgerson PR (2008) Canine echinococcosis in Kyrgyzstan: epidemiology and transmission analysis incorporting diagnostic uncertainty. Int J Parasitol 38:1179–1190
Acknowledgements
The authors are thankful to the staff members of the KPK province Wildlife Department for their help during sampling.
Author information
Authors and Affiliations
Contributions
AK and ZU collected the samples from the field under the supervision of IU and SM. AK conceived the study and both HA and GU supervised the analysis. AK collected the data and wrote the paper following discussions with HA, SA and GU. VB did the molecular analysis under the supervision of GU and FB. GU also revised the paper and improved the technical quality of the manuscript. All the authors approved the final version of the paper.
Corresponding authors
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Bruno Gottstein
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Khan, A., Umhang, G., Ullah, Z. et al. Investigation of Echinococcus multilocularis in foxes and dogs in Pakistan by detection of copro-DNA. Parasitol Res 120, 731–737 (2021). https://doi.org/10.1007/s00436-020-07001-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-020-07001-x