Strongyloides stercoralis infection in imported and local dogs in Switzerland: from clinics to molecular genetics
Strongyloides stercoralis is a worldwide-distributed intestinal nematode affecting mainly humans and dogs. Canine strongyloidosis is generally characterised by diarrhoea, malabsorption and bronchopneumonia, and may be fatal in cases of impaired immunity. In recent years, molecular and epidemiological studies suggested that host-adapted populations of S. stercoralis with different zoonotic potential may exist. Clinical and subclinical cases of S. stercoralis infection have been increasingly diagnosed in imported (France, Belgium, Bulgaria) and locally born dogs in Switzerland, showing that this parasite is currently circulating in Europe. Three of these clinical cases will be described here. All three dogs presented severe disease, characterised by harsh diarrhoea, dehydration, vomiting, respiratory and/or neurologic signs, and needed intensive care and hospitalisation. One of these dogs was related to a Swiss breeding kennel, in which the infection was subsequently diagnosed in several other dogs. Faeces were analysed by three coproscopical methods including (i) the Baermann technique, which consistently identified the typical S. stercoralis first-stage larvae in both clinical and subclinical infections, (ii) the sedimentation-zinc chloride flotation and (iii) sodium acetate—acetic acid—formalin concentration (SAFC) methods, which allowed the additional identification of parasitic females and/or eggs in two of the clinical cases. Interestingly, S. stercoralis isolated from all three independent clinical cases exhibited an identical genetic background on the nuclear 18S rDNA (fragment involving hypervariable regions I and IV) and the mitochondrial cytochrome oxidase subunit I (cox1) loci, similar to that of zoonotic isolates from other geographical regions, and not to that of dog-adapted variants. Due to the clinical relevance and zoonotic potential of this parasite, the awareness of both diagnosticians and clinicians is strongly required.
KeywordsStrongyloidosis Animal transport Diarrhoea Genotyping Zoonosis Breeding kennel
We would like to acknowledge Liliane Krähenbühl, Larissa Hofmann and Christine Salvisberg for their excellent technical assistance and the dogs’ owners for their cooperation.
This study was supported by the Institute of Parasitology of the University of Bern.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
- Cvetkovikj A, Rashikj L, Celeska I, Atanaskova Petrov E, Angjelovski B, Cvetkovikj I, Jurhar Pavlova M, Stefanovska J (2018) First case of Strongyloides stercoralis infection in a dog in the Republic of Macedonia. Mac Vet Rev:41, i–iv 509. https://doi.org/10.1515/macvetrev-2017-0032
- Epe C, Ising-Volmer S, Stoye M (1993) Ergebnisse parasitologischer Kotuntersuchungen von Equiden, Hunden, Katzen und Igeln der Jahre 1984-1991 [Parasitological fecal studies of equids, dogs, cats and hedgehogs during the years 1984-1991]. Dtsch Tierarztl Wochenschr 100:426–428 [in German]Google Scholar
- Epe C, Coati N, Schnieder T (2004) Ergebnisse parasitologischer Kotuntersuchungen von Pferden, Wiederkäuern, Schweinen, Hunden, Katzen, Igeln und Kaninchen in den Jahren 1998-2002 [Results of parasitological examinations of faecal samples from horses, ruminants, pigs, dogs, cats, hedgehogs and rabbits between 1998 and 2002]. Dtsch Tierarztl Wochenschr 111:243–247 [in German]Google Scholar
- Hamnes IS, Davidson R, Øines Ø (2009) Strongyloides stercoralis påvist hos hund i Norgenfor første gang [Strongyloides stercoralis identified in dogs in Norway for the first time]. Norsk Veterinærtidsskrift 121:752 [in Norwegian]Google Scholar
- Hasegawa H, Sato H, Fujita S, Nguema PPM, Nobusue K, Miyagi K, Kooriyama T, Takenoshita Y, Noda S, Sato A, Morimoto A, Ikeda Y, Nishidaet T (2010) Molecular identification of the causative agent of human strongyloidiasis acquired in Tanzania. Dispersal and diversity of Strongyloides spp. and their hosts. Parasitol Int 59:407–413. https://doi.org/10.1016/j.parint.2010.05.007 CrossRefGoogle Scholar
- Iatta R, Buonfrate D, Paradies P, Cavalera MA, Capogna A, Iarussi F, Šlapeta J, Giorli G, Trerotoli P, Bisoffi Z, Otranto D (2018) Occurrence, diagnosis and follow-up of canine strongyloidiosis in naturally infected shelter dogs. Parasitology:1–7. https://doi.org/10.1017/S0031182018001312
- Jaleta TG, Zhou S, Bemm FM, Schär F, Khieu V, Muth S, Odermatt P, Lok JB, Streit A (2017) Different but overlapping populations of Strongyloides stercoralis in dogs and humans-dogs as a possible source for zoonotic strongyloidiasis. PLoS Negl Trop Dis 11(8):e0005752. https://doi.org/10.1371/journal.pntd.0005752 CrossRefGoogle Scholar
- Kostopoulou D, Claerebout E, Arvanitis D, Ligda P, Voutzourakis N, Casaert S, Sotiraki S (2017) Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations. The scenario of Crete, Greece. Parasit Vectors 10:43. https://doi.org/10.1186/s13071-017-1989-8 CrossRefGoogle Scholar
- Laymanivong S, Hangvanthong B, Insisiengmay B, Vanisaveth V, Laxachack P, Jongthawin J, Sanpool O, Thanchomnang T, Sadaow L, Phosuk I, Rodpai R, Maleewong W, Intapan PM (2016) First molecular identification and report of genetic diversity of Strongyloides stercoralis, a current major soil-transmitted helminth in humans from Lao People’s Democratic Republic. Parasitol Res 115:2973–2980. https://doi.org/10.1007/s00436-016-5052-z CrossRefGoogle Scholar
- Mansfield LS, Schad GA (1992) Ivermectin treatment of naturally acquired and experimentally induced Strongyloides stercoralis infections in dogs. J Am Vet Med Assoc 201:726–730Google Scholar
- Nagayasu E, Aung MPPTHH, Hortiwakul T, Hino A, Tanaka T, Higashiarakawa M, Olia A, Taniguchi T, SMT W, Ohashi I, Odongo-Aginya EI, Aye KM, Mon M, Win KK, Ota K, Torisu Y, Panthuwong S, Kimura E, Palacpac NMQ, Kikuchi T, Hirata T, Torisu S, Hisaeda H, Horii T, Fujita J, Htike WW, Maruyama H (2017) A possible origin population of pathogenic intestinal nematodes, Strongyloides stercoralis, unveiled by molecular phylogeny. Sci Rep 7:4844. https://doi.org/10.1038/s41598-017-05049-x CrossRefGoogle Scholar
- Nolan TJ (2001) Canine Strongyloidiasis [Available from: http://www.ivis.org/advances/Parasit.Bowman/Nolan.strongyloidiasis/chapter frm.asp?LA=I]. Accessed Nov. 2018
- Paradies P, Iarussi F, Sasanelli M, Antonio C, Lia RP, Zucca D, Greco B, Cantacessi C, Otranto D (2017) Occurrence of strongyloidiasis in privately owned and sheltered dogs. Clinical presentation and treatment outcome. Parasit Vector 10:345. https://doi.org/10.1186/s13071-017-2275-5 CrossRefGoogle Scholar
- Prosl H (1985) Zum Vorkommen von Strongyloides stercoralis bei Hunden in Österreich (Occurrence of Strongylides stercoralis infections in dogs in Austria). Mit Österr Ges Tropenmed Parasitol 7:129–134Google Scholar
- Sauda F, Malandrucco L, Macrì G, Scarpulla M, De Liberato C, Terracciano G, Fichi G, Berrilli F, Perruccia S (2018) Leishmania infantum, Dirofilaria spp. and other endoparasite infections in kennel dogs in Central Italy. Parasite 25:2. https://doi.org/10.1051/parasite/2018001
- Schad GA, Hellman ME, Muncey DW (1984) Strongyloides stercoralis. Hyperinfection in immunosuppressed dogs. Exp Parasitol 57:287–296Google Scholar
- Schad GA, Thompson F, Talham G, Holt D, Nolan TJ, Ashton FT, Lange AM, Bhopale VM (1997) Barren female Strongyloides stercoralis from occult chronic infections are rejuvenated by transfer to parasite-naive recipient hosts and give rise to an autoinfective burst. J Parasitol 83:785–791CrossRefGoogle Scholar
- Shoop WL, Michael BF, Eary CH, Haines HW (2002) Transmammary transmission of Strongyloides stercoralis in dogs. J Parasitol 88:536–539. https://doi.org/10.1645/0022-3395(2002)088[0536:TTOSSI]2.0.CO;2Google Scholar
- Štrkolcová G, Goldová M, Bocková E, 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. Parasitol Res 116:891–900. https://doi.org/10.1007/s00436-016-5362-1 CrossRefGoogle Scholar
- Tanaka H (1966) Genus Strongyloides. In: Morishita K, Komiya Y, Matsubayashi H (eds) Progress in medical parasitology in Japan, vol 3. Meguro Parasitological Museum, Tokyo, pp 589–638 https://drive.google.com/file/d/1Q624g7H_EftZ9z6JDVltkYULaM-9WsQm/view. Accessed Nov. 2018
- Zanzani SA, Di Cerbo AR, Gazzonis AL, Genchi M, Rinaldi L, Musella V, Cringoli G, Manfredi MT (2014) Canine fecal contamination in a metropolitan area (Milan, North-Western Italy). Prevalence of intestinal parasites and evaluation of health risks. Sci World J 2014:132361–132366. https://doi.org/10.1155/2014/132361 CrossRefGoogle Scholar