Skip to main content

Advertisement

Log in

Prevalence and molecular characterisation of Sarcocystis miescheriana and Sarcocystis suihominis in wild boars (Sus scrofa) in Italy

  • Protozoology - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

A sample of the diaphragm was collected from each of 100 wild boars legally hunted in the Val Grande National Park in north-western Italy and examined for the presence of Sarcocystis infection by histological and molecular methods. In histological sections, thick-walled sarcocysts consistent with those of Sarcocystis miescheriana were detected in 32 wild boars. Genomic DNA extracted from diaphragm samples was initially subjected to PCR amplification of the internal transcribed spacer 1 (ITS1) region, and 97 wild boars were found to harbour a Sarcocystis infection at this screening. Selected DNA samples were then subjected to PCR amplification and sequencing of the ITS1 region and the 18S and 28S ribosomal RNA (rRNA) genes of the nuclear ribosomal DNA unit, while all positive samples were subjected to PCR amplification of the mitochondrial cytochrome c oxidase subunit I (cox1) gene. S. miescheriana was identified in 97 wild boars (97%), while the zoonotic Sarcocystis suihominis was identified in one wild boar (1%), which also harboured S. miescheriana. Intra-specific sequence variation was found in all four DNA regions of S. miescheriana examined and in the 18S rRNA gene and ITS1 region of S. suihominis. The partial cox1 gene was amplified and sequenced from 72 isolates of S. miescheriana, yielding 43 haplotypes with pairwise sequence identities of 97.6–99.9%. These haplotypes were 79.1–79.8% identical with the cox1 sequence of S. suihominis. Phylogeny based on cox1 sequences placed S. miescheriana and S. suihominis as sister species within a clade comprising mainly Sarcocystis spp. of ruminants with felids as known or presumed definitive hosts. The same was true for the phylogeny based on 18S rRNA gene sequences.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Barrows PL, Prestwood AK, Green CE (1982) Experimental Sarcocystis suicanis infections: disease in growing pigs. Am J Vet Res 43:1409–1412

    CAS  PubMed  Google Scholar 

  • Bergmann V, Kinder E (1974) Elektronenmikroskopische Befunde an der Parasit-Wirt-Kontaktzone von Sarcocystis miescheriana in Muskelfasern des Schweines. Mh Vet-Med 29:956–958

    Google Scholar 

  • Bergmann V, Kinder E (1976) Elektronenmikroskopische Untersuchungen zur Wandstruktur von Sarcozysten in der Skelettmuskulatur von Wildschwein und Reh. Mh Vet-Med 31:785–788

    Google Scholar 

  • Boch J, Mannewitz U, Erber M (1978) Sarkosporidien bei Schlachtschweinen in Süddeutschland. Berl Münch Tierärztl Wochenschr 91:106–111

    CAS  PubMed  Google Scholar 

  • Boch J, Hennings R, Erber M (1980) Die wirtschaftliche Bedeutung der Sarkosporidiose (Sarcocystis suicanis) in der Schweinemast. Auswertung eines Feldversuches. Berl Münch Tierärztl Wochenschr 93:420–423

    CAS  PubMed  Google Scholar 

  • Boitani L, Mattei L (1991) Aging wild boar by tooth eruption. In: Spitz F, Janeau G, Gonzalez G, Aulagnier S (eds) Ongulés/Ungulates 91, Proceedings of the International Symposium "Ongulés/Ungulates 91", Toulouse, France, September 2-6, 1991, pp. 419–421

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al revisited. J Parasitol 83:575–583

    Article  CAS  Google Scholar 

  • Calero-Bernal R, Verma SK, Oliveira S, Yang Y, Rosenthal BM, Dubey JP (2015) In the United States, negligible rates of zoonotic sarcocystosis occur in feral swine that, by contrast, frequently harbour infections with Sarcocystis miescheriana, a related parasite contracted from canids. Parasitology 142:549–556. https://doi.org/10.1017/S0031182014001553

    Article  CAS  PubMed  Google Scholar 

  • Calero-Bernal R, Pérez-Martín JE, Reina D, Serrano FJ, Frontera E, Fuentes I, Dubey JP (2016) Detection of zoonotic protozoa Toxoplasma gondii and Sarcocystis suihominis in wild boars from Spain. Zoonoses Public Health 63:346–350. https://doi.org/10.1111/zph.12243

    Article  CAS  PubMed  Google Scholar 

  • Caspari K, Grimm F, Kühn N, Caspari NC, Basso W (2011) First report of naturally acquired clinical sarcocystosis in a pig breeding stock. Vet Parasitol 177:175–178. https://doi.org/10.1016/j.vetpar.2010.11.019

    Article  PubMed  Google Scholar 

  • Chen LY, Zhou BJ, Yang ZQ, Li CY, Attwood SW, Wang WL, Lei L, Sun XD, Zhang ZX (2007) Effects of frozen storage on the structure of sarcocysts in pig muscle and implications in taxonomic studies. Exp Parasitol 115:393–398. https://doi.org/10.1016/j.exppara.2006.10.003

    Article  PubMed  Google Scholar 

  • Claveria FG, De La Peña C, Cruz-Flores MJ (2001) Sarcocystis miescheriana infection in domestic pigs (Sus scrofa) in the Philippines. J Parasitol 87:938–939. https://doi.org/10.1645/0022-3395(2001)087[0938:SMIIDP]2.0.CO;2

  • Coelho C, Gomes J, Inácio J, Amaro A, Mesquita JR, Pires I, Lopes AP, Vieira-Pinto M (2015) Unraveling Sarcocystis miescheriana and Sarcocystis suihominis infections in wild boar. Vet Parasitol 212:100–104. https://doi.org/10.1016/j.vetpar.2015.08.015

    Article  PubMed  Google Scholar 

  • Damriyasa IM, Bauer C, Edelhofer R, Failing K, Lind P, Petersen E, Schares G, Tenter AM, Volmer R, Zahner H (2004) Cross sectional survey in pig breeding farms in Hesse, Germany: seroprevalence and risk factors of infections with Toxoplasma gondii, Sarcocystis spp. and Neospora caninum in sows. Vet Parasitol 126:271–286. https://doi.org/10.1016/j.vetpar.2004.07.016

    Article  CAS  PubMed  Google Scholar 

  • Dubey JP (1976) A review of Sarcocystis of domestic animals and of other coccidia of cats and dogs. J Am Vet Med Ass 169:1061–1078

    CAS  Google Scholar 

  • Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2016) Sarcocystosis of animals and humans, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Erber M (1977) Möglichkeiten des Nachweises un der Differenzierung von zwei Sarcocystis-Arten des Schweines. Berl Münch Tierärztl Wochenschr 90:480–482

    CAS  PubMed  Google Scholar 

  • Erber M, Boch J (1976) Untersuchungen über Sarckosporidien des Schwarzwildes. Sporozystenausscheidung durch Hund, Fuchs und Wolf. Berl Münch Tierärztl Wochenschr 89:449–450

    CAS  PubMed  Google Scholar 

  • Fayer R, Esposito DH, Dubey JP (2015) Human infections with Sarcocystis species. Clin Microbiol Rev 28:295–311. https://doi.org/10.1128/CMR.00113-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Gazzonis AL, Villa L, Riehn K, Hamedy A, Minazzi S, Olivieri E, Zanzani SA, Manfredi MT (2018) Occurrence of selected zoonotic food-borne parasites and first molecular identification of Alaria alata in wild boars (Sus scrofa) in Italy. Parasitol Res 117:2207–2215. https://doi.org/10.1007/s00436-018-5908-5

    Article  PubMed  Google Scholar 

  • Gjerde B (2013) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. Int J Parasitol 43:579–591. https://doi.org/10.1016/j.ijpara.2013.02.004

    Article  CAS  PubMed  Google Scholar 

  • Gjerde B (2014a) Sarcocystis species in red deer revisited: with a re-description of two known species as Sarcocystis elongata n. sp. and Sarcocystis truncata n. sp. based on mitochondrial cox1 sequences. Parasitology 141:441–452. https://doi.org/10.1017/S0031182013001819

    Article  PubMed  Google Scholar 

  • Gjerde B (2014b) Molecular characterisation of Sarcocystis rileyi from a common eider (Somateria mollissima) in Norway. Parasitol Res 113:3501–3509. https://doi.org/10.1007/s00436-014-4062-y

    Article  PubMed  Google Scholar 

  • Gjerde B (2016) Molecular characterisation of Sarcocystis bovifelis, Sarcocystis bovini n. sp., Sarcocystis hirsuta and Sarcocystis cruzi from cattle (Bos taurus) and Sarcocystis sinensis from water buffaloes (Bubalus bubalis). Parasitol Res 115:1473–1492. https://doi.org/10.1007/s00436-015-4881-5

    Article  PubMed  Google Scholar 

  • Gjerde B, Dahlgren SS (2010) Corvid birds (Corvidae) act as definitive hosts for Sarcocystis ovalis in moose (Alces alces). Parasitol Res 107:1445–1453. https://doi.org/10.1007/s00436-010-2017-5

    Article  PubMed  Google Scholar 

  • Gjerde B, Josefsen TD (2015) Molecular characterisation of Sarcocystis lutrae n. sp. and Toxoplasma gondii from the musculature of two Eurasian otters (Lutra lutra) in Norway. Parasitol Res 114:873–886. https://doi.org/10.1007/s00436-014-4251-8

    Article  PubMed  Google Scholar 

  • Gjerde B, Giacomelli S, Bianchi A, Bertoletti I, Mondani H, Gibelli LR (2017a) Morphological and molecular characterization of four Sarcocystis spp., including Sarcocystis linearis n. sp., from roe deer (Capreolus capreolus) in Italy. Parasitol Res 116:1317–1338. https://doi.org/10.1007/s00436-017-5410-5

    Article  PubMed  Google Scholar 

  • Gjerde B, Luzón M, Alunda JM, de la Fuente C (2017b) Morphological and molecular characteristics of six Sarcocystis spp. from red deer (Cervus elaphus) in Spain, including Sarcocystis cervicanis and three new species. Parasitol Res 116:2795–2811. https://doi.org/10.1007/s00436-017-5590-z

    Article  PubMed  Google Scholar 

  • Gjerde B, Vikøren T, Hamnes IS (2017c) Molecular identification of Sarcocystis halieti n. sp., Sarcocystis lari and Sarcocystis truncata in the intestine of a white-tailed sea eagle (Haliaeetus albicilla) in Norway. Int J Parasitol Parasites Wildl 7:1–11. https://doi.org/10.1016/j.ijppaw.2017.12.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Göbel E, Katz M, Erber M (1978) Licht- und elektronenmikroskopische Untersuchungen zur Entwicklung von Muskelzysten von Sarcocystis suicanis in Hausschweinen nach experimenteller Infektion. Zbl Bakt Hyg I Abt Orig A 241:368–383

    Google Scholar 

  • Golubkov VI, Rybaltovskii OV, Kislyakova ZI (1974) Plotoyadnye - istochnik zarazheniya svinei sarkotsistami. (Carnivores—source of infection of swine with sarcocysts). (in Russian). Veterinariya 1974:85–86

  • González LM, Villalobos N, Montero E, Morales J, Sanz RA, Muro A, Harrison LJ, Parkhouse RM, Garate T (2006) Differential molecular identification of Taeniid spp. and Sarcocystis spp. cysts isolated from infected pigs and cattle. Vet Parasitol 142:95–101. https://doi.org/10.1016/j.vetpar.2006.06.009

    Article  CAS  PubMed  Google Scholar 

  • Heydorn AO (1977a) Beiträge zum Lebenszyklus der Sarkosporidien. IX. Entwicklungszyklus von Sarcocystis suihominis n. spec. Münch Tierärztl Wochenschr 90:218–224

    CAS  Google Scholar 

  • Heydorn AO (1977b) Sarkosporidien infiziertes Fleisch als mögliche Krankheitsursache für den Menschen. Arch Leb 28:27–31

    Google Scholar 

  • Heydorn AO, Weniger JH (1988) Einfluss einer akuten Sarcocystis suihominis-Infektion auf die Mastleitung von Absatzferkeln. Münch Tierärztl Wochenschr 101:307–310

    CAS  Google Scholar 

  • Hinaidy HK, Supperer R (1979) Sarkosporidienbefall des Schweines in Österreich. Wien Tierarztl Monatsschr 66:281–285

    Google Scholar 

  • Höchtl F, Lehringer S, Konold W (2005) “Wilderness”: what it means when it becomes a reality — a case study from the southwestern Alps. Land Urb Plan 70:85–95

  • Imre K, Sala C, Morar A, Imre M, Ciontu C, Chisali I, Dudu A, Matei M, Darabu G (2017) Occurrence and first molecular characterization of Sarcocystis spp. in wild boars (Sus scrofa) and domestic pigs (Sus scrofa domesticus) in Romania: public health significance of the isolates. Acta Trop 167:191–195. https://doi.org/10.1016/j.actatropica.2016.12.038

    Article  CAS  PubMed  Google Scholar 

  • Kaur M, Singh BB, Sharma R, Gill JP (2016) Pervasive environmental contamination with human feces results in high prevalence of zoonotic Sarcocystis infection in pigs in the Punjab, India. J Parasitol 102:229–232. https://doi.org/10.1645/15-828

    Article  CAS  PubMed  Google Scholar 

  • Kia EB, Mirhendi H, Rezaeian M, Zahabiun F, Sharbatkhori M (2011) First molecular identification of Sarcocystis miescheriana (Protozoa, Apicomplexa) from wild boar (Sus scrofa) in Iran. Exp Parasitol 127:724–726. https://doi.org/10.1016/j.exppara.2010.11.007

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870–1874

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187

    Article  CAS  Google Scholar 

  • Moré G, Maksimov A, Conraths FJ, Schares G (2016) Molecular identification of Sarcocystis spp. in foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) from Germany. Vet Parasitol 220:9–14. https://doi.org/10.1016/j.vetpar.2016.02.011

    Article  CAS  PubMed  Google Scholar 

  • Mugridge NB, Morrison DA, Jakel T, Heckeroth AR, Tenter AM, Johnson AM (2000) Effects of sequence alignment and structural domains of ribosomal DNA on phylogeny reconstruction for the protozoan family Sarcocystidae. Mol Biol Evol 17:1842–1853. https://doi.org/10.1093/oxfordjournals.molbev.a026285

    Article  CAS  PubMed  Google Scholar 

  • Poulsen CS, Stensvold CR (2014) Current status of epidemiology and diagnosis of human sarcocystosis. J Clin Microbiol 52:3524–3530. https://doi.org/10.1128/JCM.00955-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prakas P (2011) Diversity and ecology of Sarcocystis in Lithuanian game fauna. PhD thesis, Vilnius University, Vilnius, Lithuania

  • Rommel M, Heydorn AO (1972) Beiträge zum Lebenszyklus der Sarkosporidien. III. Isospora hominis (Railliet und Lucet, 1891) Wenyon, 1923, eine Dauerform der Sarkosporidien des Rindes und des Schweins. Münch Tierärztl Wochenschr 85:143–145

    CAS  Google Scholar 

  • Rommel M, Heydorn AO, Fischle B, Gestrich R (1974) Beiträge zum Lebenszyklus der Sarkosporidien. V. Weitere Endwirte der Sarkosporidien von Rind, Schaf und Schwein und die Bedeutung des Zwischenwirtes für die Verbreitung dieser Parasitose. Münch Tierärztl Wochenschr 87:392–396

    CAS  Google Scholar 

  • Saito M, Shibata Y, Kobayashi T, Kobayashi M, Kubo M, Itagaki H (1996) Ultrastructure of the cyst wall of Sarcocystis species with canine final host in Japan. J Vet Med Sci 58:861–867. https://doi.org/10.1292/jvms.58.861

    Article  CAS  PubMed  Google Scholar 

  • Saito M, Shibata Y, Ohno A, Kubo M, Shimura K, Itagaki H (1998) Sarcocystis suihominis detected for the first time from pigs in Japan. J Vet Med Sci 60:307–309. https://doi.org/10.1292/jvms.60.307

    Article  CAS  PubMed  Google Scholar 

  • Torretta E, Mosini A, Piana M, Tirozzi P, Serafini M, Puopolo F, Saino N, Balestrieri A (2017) Time partitioning in mesocarnivore communities from different habitats of NW Italy: insights into martens’ competitive abilities. Behaviour 154:241–266. https://doi.org/10.1163/1568539X-00003420

    Article  Google Scholar 

  • Yan W, Qian W, Li X, Wang T, Ding K, Huang T (2013) Morphological and molecular characterization of Sarcocystis miescheriana from pigs in the central region of China. Parasitol Res 112:975–980. https://doi.org/10.1007/s00436-012-3219-9

    Article  PubMed  Google Scholar 

  • Yang ZQ, Zuo YX, Yao YG, Chen XW, Yang GC, Zhang YP (2001) Analysis of the 18S rRNA genes of Sarcocystis species suggests that the morphologically similar organisms from cattle and water buffalo should be considered the same species. Mol Biochem Parasitol 115:283–288

    Article  CAS  PubMed  Google Scholar 

  • Yang ZQ, Li QQ, Zuo YX, Chen XW, Chen YJ, Nie L, Wei CG, Zen JS, Attwood SW, Zhang XZ, Zhang YP (2002) Characterization of Sarcocystis species in domestic animals using a PCR-RFLP analysis of variation in the 18S rRNA gene: a cost-effective and simple technique for routine species identification. Exp Parasitol 102:212–217

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the Comprensorio Alpino VCO1 of Verbania and their hunters for their help with the sampling of the wild boars.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bjørn Gjerde.

Ethics declarations

The wild boars used in the present study were legally hunted as part of an approved depopulation plan for the Val Grande National Park (see the section “Materials and methods” and Gazzonis et al. 2018 for details).

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Section Editor: David S. Lindsay

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 2304 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gazzonis, A.L., Gjerde, B., Villa, L. et al. Prevalence and molecular characterisation of Sarcocystis miescheriana and Sarcocystis suihominis in wild boars (Sus scrofa) in Italy. Parasitol Res 118, 1271–1287 (2019). https://doi.org/10.1007/s00436-019-06249-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-019-06249-2

Keywords

Navigation