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Global prevalence of Strongyloides stercoralis in dogs: A systematic review and meta-analysis

Published online by Cambridge University Press:  21 February 2022

Tahmineh Gorgani-Firouzjaee Open the ORCID record for Tahmineh Gorgani-Firouzjaee [Opens in a new window] ,
Narges Kalantari Open the ORCID record for Narges Kalantari [Opens in a new window] ,
Mohammad Chehrazi ,
Salman Ghaffari Open the ORCID record for Salman Ghaffari [Opens in a new window]  and
Shaysteh Shahdin
Tahmineh Gorgani-Firouzjaee
Affiliation:
Department of Mycology and Parasitology, School of Medicine, Babol University of Medical Sciences, Babol, Iran
Narges Kalantari*
Affiliation:
Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran
Mohammad Chehrazi
Affiliation:
Department of Biostatistics and Epidemiology, School of Health Science, Babol University of Medical Sciences, Babol, Iran
Salman Ghaffari
Affiliation:
Department of Mycology and Parasitology, School of Medicine, Babol University of Medical Sciences, Babol, Iran
Shaysteh Shahdin
Affiliation:
Department of Laboratory Sciences, Faculty of Paramedical Sciences, Babol University of Medical Sciences, Babol, Iran
*
Author for correspondence: Narges Kalantari, Fax.: +981132 238 284. E mail: nfkala@gmail.com
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Abstract

Strongyloides stercoralis is an intestinal parasitic helminth that mainly affects humans and dogs throughout the world. Canine strongyloidosis is generally characterized by asymptomatic infection, with fatal disease in cases of immunodeficiency. This study was conducted in order to evaluate the global prevalence of S. stercoralis in dogs. Six electronic databases were searched for this purpose. The random effects model and 95% confidence intervals (CI) were applied to determine the overall and subgroup pooled prevalence. Heterogeneity was assessed by Cochran's Q test and I2 statistic. In total, 56 datasets from 50 studies from 1,202 peer-reviewed papers were included in the current meta-analysis. 20,627 dogs were assessed in 27 countries across six World Health Organization (WHO) regions. The global prevalence of S. stercoralis infection among dogs was 6% (95% CI 4–8%; 868/20,627). According to WHO regions, the estimated prevalence ranges 2% to 11% as follows: Western Pacific (11%, 0–31%); Africa (9%, 2–19%); America (6%, 3–11%); South-East Asia (5%, 1–13%)’ Europe (3%, 2–5%); and Eastern Mediterranean (2%, 0–6%). The pooled prevalence of S. stercoralis infection in dog owners was 7% (1–18%). The prevalence of S. stercoralis infection in studies based on serological assays was significantly higher than other techniques (29%, 20–39%). Younger female dogs, less than one year old, from rural areas had higher prevalence rates than their male counterparts, with no statistically significant differences. From this review, it is concluded that the low global prevalence of S. stercoralis in dogs may be strongly associated with low sensitivity diagnostic methods applied in most studies leading to the underestimation of infection rates. Therefore, the improvement of diagnostic techniques is recommended for precise evaluation of the disease.

Keywords

CanineprevalenceStrongyloides stercoralis
Type
Review Article
Information
Journal of Helminthology , Volume 96 , 2022 , e11
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Ahmad, B, Khan, W, Yasmin, S, Mehmood, SA, Ahmed, S, Das, SN, Shah, M and Iqbal, R (2020) Prevalence of intestinal protozoans parasites of household dogs and risk perception of their zoonosis in district Swabi, Pakistan. Bioscience Research 17(3), 2223–2232.Google Scholar
Alvarado-Esquivel, C, Romero-Salas, D, Aguilar-Domínguez, M, Cruz-Romero, A, Ibarra-Priego, N and Pérez-de-León, AÁ (2015) Epidemiological assessment of intestinal parasitic infections in dogs at animal shelter in veracruz, Mexico. Asian Pacific Journal of Tropical Biomedicine 5(1), 34–39.CrossRefGoogle Scholar
Ardelean, AI., Suteu, E and Cozma, V (2005) Epidemiology of digestive helminthosis from urban area of Cluj-Napoca, Romania. In Sestras R (Ed.) Bulletin of the University of Agricultural Science and Veterinary Medicine, Vol 62, 2005: Veterinary Medicine, 322–339.Google Scholar
Awoke, E, Bogale, B and Chanie, M (2011) Intestinal nematode parasites of dogs: prevalence and associated risk factors. International Journal of Animal and Veterinary Advances 3(5), 374–3878.Google Scholar
Azian, MY, Sakhone, L, Hakim, SL, Yusri, MY, Nurulsyamzawaty, Y, Zuhaizam, AH, Rodi, IM and Maslawaty, MN (2008) Detection of helminth infections in dogs and soil contamination in rural and urban areas. Southeast Asian Journal of Tropical Medicine and Public Health 39(2), 205–212.Google ScholarPubMed
Basso, W, Grandt, LM, Magnenat, AL, Gottstein, B and Campos, M (2019) Strongyloides stercoralis infection in imported and local dogs in Switzerland: From clinics to molecular genetics. Parasitology Research 118(1), 255–266.CrossRefGoogle ScholarPubMed
Beknazarova, M, Whiley, H and Ross, K (2016) Strongyloidiasis: A disease of socioeconomic disadvantage. International Journal of Environmental Research and Public Health 13(5), e0007241.1-18.CrossRefGoogle ScholarPubMed
Beknazarova, M, Barratt, JLN, Bradbury, RS, Lane, M, Whiley, H and Ross, K (2019) Detection of classic and cryptic Strongyloides genotypes by deep amplicon sequencing: a preliminary survey of dog and human specimens collected from remote Australian communities. PLoS Neglected Tropical Diseases 13, e0007241.CrossRefGoogle ScholarPubMed
Buonfrate, D, Formenti, F, Perandin, F and Bisoffi, Z (2015) Novel approaches to the diagnosis of Strongyloides stercoralis infection. Clinical Microbiology and Infection 21(6), 543–552.CrossRefGoogle Scholar
Buonfrate, D, Requena-Mendez, A, Angheben, A, et al. (2018) Accuracy of molecular biology techniques for the diagnosis of Strongyloides stercoralis infection-A systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12, e0006229.CrossRefGoogle Scholar
Campos, DR, Oliveira, LC, De Siqueira, DF, Perin, LR, Campos, NC, Aptekmann, KP and Martins, IVF (2016) Prevalence and risk factors associated with endoparasitosis of dogs and cats in Espírito Santo, Brazil. Acta Parasitologica 61(3), 544–548.CrossRefGoogle ScholarPubMed
Dillard, KJ, Saari, SAM and Anttila, M (2007) Strongyloides stercoralis infection in a Finnish kennel. Acta Veterinaria Scandinavica 49(1), 37.CrossRefGoogle Scholar
Eydal, M and Skirnisson, K (2016) Strongyloides stercoralis found in imported dogs, household dogs and kennel dogs in Iceland. Icelandic Agricultural Sciences 29(1), 39–51.CrossRefGoogle Scholar
Fang, F, Li, J, Huang, T, Guillot, J and Huang, W (2015) Zoonotic helminths parasites in the digestive tract of feral dogs and cats in Guangxi, China. BMC Veterinary Research 11, 1–5.CrossRefGoogle ScholarPubMed
Ferreira, A, Goncalves-Pires, MRF, Silva, DAO, Goncalves, ALR and Costa-Cruz, JM (2006) Parasitological and serological diagnosis of Strongyloides stercoralis in domesticated dogs from southeastern Brazil. Veterinary Parasitology 136(2), 137–145.Google Scholar
Fontanarrosa, MF, Vezzani, D, Basabe, J and Eiras, DF (2006) An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Veterinary Parasitology 136(3–4), 283–295.CrossRefGoogle Scholar
Furuya-Kanamori, L, Barendregt, JJ and Doi, SAR (2018) A new improved graphical and quantitative method for detecting bias in meta-analysis. International Journal of Evidence-Based Healthcare 16(4), 195–203.CrossRefGoogle ScholarPubMed
Gonçalves, AL, Machado, GA, Gonçalves-Pires, MR, Ferreira-Júnior, A, Silva, DA and Costa-Cruz, JM (2007) Evaluation of strongyloidiasis in kennel dogs and keepers by parasitological and serological assays. Veterinary Parasitology 147(1–2), 132–139.CrossRefGoogle ScholarPubMed
G Selasie, D, Geyola, M., Dagne, E, Asmare, K and Mekuria, S (2013) Gastrointestinal helminthes in dogs and community perception on parasite zoonosis at Hawassa city, Ethiopia. Global Veterinaria 11(4), 432–440.Google Scholar
Harvey, TV, Tang, AM, da Paixao Sevá, A, Albano dos Santos, C, Santos Carvalho, SM, Magalhães da Rocha, CMB, Oliveira, BCM and Albuquerque, GR (2020) Enteric parasitic infections in children and dogs in resource-poor communities in northeastern Brazil: identifying priority prevention and control areas. PLOS Neglected Tropical Diseases 14, e0008378.CrossRefGoogle ScholarPubMed
Hernández-Camacho, N, Pineda-López, R, López-González, CA and Jones, RW (2011) Nematodes parasites of the gray fox (urocyon cinereoargenteus schreber, 1775) in the seasonally dry tropical highlands of central Mexico. Parasitology Research 108(6), 1425–1429.CrossRefGoogle ScholarPubMed
Iatta, R, Buonfrate, D, Paradies, P, et al. (2019) Occurrence, diagnosis and follow-up of canine strongyloidiosis in naturally infected shelter dogs. Parasitology 146(2), 246–252.CrossRefGoogle ScholarPubMed
Jaleta, TG, Zhou, S, Bemm, FM, Schär, F, Khieu, V, Muth, S, Odermatt, P, Lok, JB and Streit, A (2017) Different but overlapping populations of Strongyloides stercoralis in dogs and humans-dogs as a possible source for zoonotic strongyloidiasis. PLoS Neglected Tropical Diseases 11, e0005752.CrossRefGoogle ScholarPubMed
Jariwala, S, Redding, L and Hewitt, D (2017) The severely under-recognized public health risk of strongyloidiasis in North American cities—A One health approach. Zoonoses and Public Health 64(8), 579–588.CrossRefGoogle ScholarPubMed
Jaskoski, BJ (1971) Intestinal parasites of well cared for dogs. American Journal of Tropical Medicine and Hygiene 20(1), 441–444.CrossRefGoogle ScholarPubMed
Kalantari, N, Chehrazi, M, Ghaffari, S and Gorgani-Firouzjaee, T (2020) Serological assays for the diagnosis of Strongyloides stercoralis infection: a systematic review and meta-analysis of diagnostic test accuracy. Transactions of the Royal Society of Tropical Medicine and Hygiene 114(6), 459–469.CrossRefGoogle Scholar
Kidima, W (2019) Prevalence of zoonotic parasites in stray dogs in rural communities Tanzania. Tanzania Journal of Science 45(1), 93–100.Google Scholar
Kostopoulou, D, Claerebout, E, Arvanitis, D, Ligda, P, Voutzourakis, N, Casaert, S and Sotiraki, S (2017) Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: the scenario of Crete. Greece. Parasites and Vectors 10(1), 43–43.CrossRefGoogle ScholarPubMed
Mandarino-Pereira, A, de Souza, FS, Lopes, CW and Pereira, MJ (2010) Prevalence of parasites in soil and dog feces according to diagnostic tests. Veterinary Parasitology 170(1–2), 176–181.CrossRefGoogle ScholarPubMed
Martins, CM, Barros Cda, C, Bier, D, Marinho, AP, Figueiredo, JM, Hoffmann, JL, Molento, MB and Biondo, AW (2012) Dog parasite incidence and risk factors, from sampling after one-year interval, in Pinhais, Brazil. Revista Brasileira de Parasitologia Veterinaria 21(2), 101–106.CrossRefGoogle ScholarPubMed
Meloni, BP, Thompson, RC, Hopkins, RM, Reynoldson, JA and Gracey, M (1993) The prevalence of Giardia and other intestinal parasites in children, dogs and cats from aboriginal communities in the Kimberley. Medical Journal of Australia 158(3), 157–159.CrossRefGoogle ScholarPubMed
Merga, T and Sibhat, B (2015) Prevalence of gastrointestinal helminth parasites of dogs and associated risk factors in Adama town, Central Ethiopia. Ethiopian Veterinary Journal 19(2), 91–103.CrossRefGoogle Scholar
Mircean, V, Györke, A and Vasile, C (2011) Prevalence and risk factors of Giardia duodenalis in dogs from Romania. Veterinary Parasitology 184(2–4), 325–329.CrossRefGoogle ScholarPubMed
Mulugeta, Y (2019) Intestinal parasites in dogs and humans, environmental egg contamination and risk of human infection with zoonotic helminth parasites from dog in Hosanna town. International Journal of Biomedical Materials Research 7(1), 24–36.CrossRefGoogle Scholar
Munn, Z, Moola, S, Riitano, D and Lisy, K (2014) The development of a critical appraisal tool for use in systematic reviews addressing questions of prevalence. International Journal of Health Policy and Management 3(3), 123–128.CrossRefGoogle Scholar
Nagayasu, E, Aung, MPPTHH, Hortiwakul, T, et al. (2017) A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Scientific Reports 7(1). https://doi.org/10.1038/s41598-017-05049-x.CrossRefGoogle ScholarPubMed
Natalini, B, Gennuso, S, Beldomenico, PM, Rigonatto, T and Kowalewski, MM (2020) Parasitologic examination and associated risk factors of domestic dogs at the domestic–wildlife interface in the Iberá wetlands Ecoregion, Argentina. Veterinary Parasitology: Regional Studies and Reports 20. Epub ahead of print 29 January 2020.Google ScholarPubMed
O'Connell, A, Scott, I, Cogger, N, Jones, BR and Hill, KE (2019) Parasitic nematode and protozoa status of working sheepdogs on the North Island of New Zealand. Animals 9(3), 94.CrossRefGoogle ScholarPubMed
Opazo, A, Barrientos, C, María Sanhueza, A, Urrutia, N and Fernández, I (2019) Parasitic fauna in canines (Canis lupus familiaris) from a rural sector of the central region of Chile. Revista de Investigaciones Veterinarias del Perú 30, 330–338.CrossRefGoogle Scholar
Ortuño, A and Castellà, J (2011) Intestinal parasites in shelter dogs and risk factors associated with the facility and its management. Israel Journal of Veterinary Medicine 66, 103–107.Google Scholar
Ortuño, A, Scorza, V, Castellà, J and Lappin, M (2014) Prevalence of intestinal parasites in shelter and hunting dogs in Catalonia, Northeastern Spain. Veterinary Journal 199(3), 465–467.CrossRefGoogle Scholar
Papazahariadou, A, Founta, A, Papadopoulos, E, Chliounakis, S, Antoniadou-Sotiriadou, K and Theodorides, Y (2007) Gastrointestinal parasites of shepherd and hunting dogs in the Serres Prefecture, Northern Greece. Veterinary Parasitology 148(2), 170–173.CrossRefGoogle ScholarPubMed
Paradies, P, Iarussi, F, Sasanelli, M, Capogna, A, Lia, RP, Zucca, D, Greco, B, Cantacessi, C and Otranto, D (2017) Occurrence of strongyloidiasis in privately owned and sheltered dogs: clinical presentation and treatment outcome. Parasites and Vectors 10(1), 345–345.CrossRefGoogle ScholarPubMed
Paradies, P, Buonfrate, D, Iatta, R, et al. (2019) Efficacy of ivermectin to control Strongyloides stercoralis infection in sheltered dogs. Acta Tropica 190, 204–209.CrossRefGoogle ScholarPubMed
Perera, PK, Rajapakse, R and Rajakaruna, RS (2013) Gastrointestinal parasites of dogs in Hantana area in the Kandy District. Journal of the National Science Foundation of Sri Lanka 41(2), 81–91.CrossRefGoogle Scholar
Pumidonming, W, Salman, D, Gronsang, D, Abdelbaset, AE, Sangkaeo, K, Kawazu, S and Igarashi, M (2016) Prevalence of gastrointestinal helminth parasites of zoonotic significance in dogs and cats in lower Northern Thailand. Journal of Veterinary Medical Science 78(12), 1779–1784.CrossRefGoogle ScholarPubMed
Pumipuntu, N (2018) Detection for potentially zoonotic gastrointestinal parasites in long-tailed macaques, dogs and cattle at Kosamphi forest park, Maha Sarakham. Veterinary Integrative Sciences 16(2), 69–77.Google Scholar
Regidor-Cerrillo, J, Arranz-Solis, D, Moreno-Gonzalo, J, Pedraza-Diaz, S, Gomez-Bautista, M, Ortega-Mora, LM and Collantes-Fernandez, E (2020) Prevalence of intestinal parasite infections in stray and farm dogs from Spain. Revista Brasileira de Parasitologia Veterinaria 29(3). doi: 10.1590/s1984-29612020063.Google ScholarPubMed
Requena-Méndez, A, Chiodini, P, Bisoffi, Z, Buonfrate, D, Gotuzzo, E and Muñoz, J (2013) The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Neglected Tropical Diseases 7, e2002.CrossRefGoogle ScholarPubMed
Riggio, F, Mannella, R, Ariti, G and Perrucci, S (2013) Intestinal and lung parasites in owned dogs and cats from central Italy. Veterinary Parasitology 193(1–3), 78–84.CrossRefGoogle ScholarPubMed
Robinson, RD, Thompson, DL and Lindo, JF (1989) A survey of intestinal helminths of well-cared-for dogs in Jamaica, and their potential public health significance. Journal of Helminthology 63(1), 32–38CrossRefGoogle ScholarPubMed
Salvador, F, Treviño, B, Bosch-Nicolau, P, et al. (2020) Strongyloidiasis screening in migrants living in Spain: systematic review and meta-analysis. Tropical Medicine and International Health 25(3), 281–290.CrossRefGoogle ScholarPubMed
Sanchez-Thevenet, P, Carmena, D, Adell-Aledon, M, Dacal, E, Arias, E, Saugar, JM, Rodriguez, E and Dea-Ayuela, MA (2019) High prevalence and diversity of zoonotic and other intestinal parasites in dogs from eastern Spain. Vector-Borne and Zoonotic Diseases 19(12), 915–922.CrossRefGoogle ScholarPubMed
Sanpool, O, Intapan, PM, Rodpai, R, Laoraksawong, P, Sadaow, L, Tourtip, S, Piratae, S, Maleewong, W and Thanchomnang, T (2019) Dogs are reservoir hosts for possible transmission of human strongyloidiasis in Thailand: molecular identification and genetic diversity of causative parasite species. Journal of Helminthology 94, e110.CrossRefGoogle ScholarPubMed
Sauda, F, Malandrucco, L, Macri, G, Scarpulla, M, De Liberato, C, Terracciano, G, Fichi, G, Berrilli, F and Perrucci, S (2018) Leishmania infantum, Dirofilaria spp. and other endoparasite infections in kennel dogs in central Italy. Parasite 25(2). doi: 10.1051/parasite/2018001.CrossRefGoogle ScholarPubMed
Schaer, F, Inpankaew, T, Traub, R, et al. (2014) The prevalence and diversity of intestinal parasitic infections in humans and domestic animals in a rural Cambodian village. Parasitology International 63(4), 597–603.CrossRefGoogle Scholar
Schär, F, Trostdorf, U, Giardina, F, Khieu, V, Muth, S, Marti, H, Vounatsou, P and Odermatt, P (2013) Strongyloides stercoralis: Global distribution and risk factors. PLoS Neglected Tropical Diseases 7, e2288–e2288.CrossRefGoogle ScholarPubMed
Shoop, WL, Michael, BF, Eary, CH and Haines, HW (2002) Transmammary transmission of Strongyloides stercoralis in dogs. Journal of Parasitology 88(3), 536–539.CrossRefGoogle ScholarPubMed
Silva, GSD, Ferreira, FC, Romera, DM, Soares, VE and Bonuti, MR (2020) Larva migrans in Votuporanga, São Paulo, Brazil: where does the danger hide? Revista Brasileira de Parasitologia Veterinária 29(3), e004920.CrossRefGoogle Scholar
Štrkolcová, G, Goldová, M, Bocková, E and Mojžišová, J (2017) The roundworm Strongyloides stercoralis in children, dogs, and soil inside and outside a segregated settlement in Eastern Slovakia: Frequent but hardly detectable parasite. Parasitology Research 116(3), 891–900.CrossRefGoogle ScholarPubMed
Takano, Y, Minakami, K, Kodama, S, Matsuo, T and Satozono, I (2009) Cross infection of Strongyloides between humans and dogs in the Amami Islands, Japan. Tropical Medicine and Health 37(4), 149–152.CrossRefGoogle Scholar
Tamponi, C, Knoll, S, Tosciri, G, Salis, F, Dessi, G, Cappai, MG, Varcasia, A and Scala, A (2020) Environmental contamination by dog feces in touristic areas of Italy: parasitological aspects and zoonotic hazards. American Journal of Tropical Medicine and Hygiene 103(3), 1143–1149.CrossRefGoogle ScholarPubMed
Tull, A, Moks, E, Laurimaa, L, Keis, M and Suld, K (2020) Endoparasite infection hotspots in Estonian urban areas. Journal of Helminthology 94, e104.CrossRefGoogle Scholar
Utaaker, KS, Tysnes, KR, Krosness, MM and Robertson, LJ (2018) Not just a walk in the park: occurrence of intestinal parasites in dogs roaming recreational parks in Chandigarh, Northern India. Veterinary Parasitology: Regional Studies and Reports 14, 176–180.Google Scholar
Wells, G, Shea, B, O'Connell, D, Peterson, J, Welch, V, Losos, M and Tugwell, P (2000) The Newcastle–Ottawa Scale (NOS) for Assessing the Quality of Non-Randomized Studies in Meta-Analysis. Available at http://www.evidencebasedpublichealth.de/download/Newcastle_Ottowa_Scale_Pope_Bruce.pdf (accessed 2 August 2021).Google Scholar
Wright, I, Stafford, K and Coles, G (2016) The prevalence of intestinal nematodes in cats and dogs from Lancashire, north-west England. Journal of Small Animal Practice 57(8), 393–395.CrossRefGoogle Scholar
Zanzani, SA, Di Cerbo, AR, Gazzonis, AL, Genchi, M, Rinaldi, L, Musella, V, Cringoli, G and Manfredi, MT (2014) Canine fecal contamination in a metropolitan area (Milan, north-western Italy): Prevalence of intestinal parasites and evaluation of health risks. Scientific World Journal 2014, 132361. http://dx.doi.org/10.1155/2014/132361.CrossRefGoogle Scholar
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