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Sarcocystosis in Ruminants of Iran, as Neglected Food-Borne Disease: A Systematic Review and Meta-analysis

Abstract

Purpose

Sarcocystis is a zoonotic parasitic pathogen which endangers the safety of meat and meat products. This systematic review and meta-analysis aimed to evaluate the prevalence rate and status of Sarcocystis spp. in ruminants as important food sources in Iran.

Methods

Data were collected from papers indexed in five English language electronic databases (PubMed, Scopus, Web of Science, Science Direct, and Google Scholar) and four Persian electronic databases (IranMedex, SID, IranDoc, and Magiran) from January to April 2019. Papers were selected based on inclusion criteria. Data analysis was performed in StatsDirect statistical software, version 2.7.2.

Results

The searching process resulted in the identification of 73 studies. Data analyses revealed that the total prevalence (95% confidence intervals) of Sarcocystis spp. in Iranian ruminants was 74.40% (64.01–83.56). In addition, a significant association was also observed between sarcocystosis infection in Iranian ruminants and year, host, location, and diagnostic technique (P < 0.001).

Conclusions

According to our data, the prevalence of Sarcocystis infection in ruminants is relatively high. High pathogenicity of some Sarcocystis spp. and the negative impact that the spread of some parasites among ruminants can have on human and animal health necessitate the direction of more attention toward monitoring, controlling, and preventing sarcocystosis.

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References

  1. 1.

    Dubey JP, Calero-Bernal R, Rosenthal BM, Speer CA, Fayer R (2015) Sarcocystosis of animals and humans, 2nd edn. CRC Press, Boca Raton, Florida, USA

    Google Scholar 

  2. 2.

    Moré G, Abrahamovich P, Jurado S, Bacigalupe D, Marin JC, Rambeaud M, Venturini L, Venturini MC (2011) Prevalence of Sarcocystis spp. in Argentinean cattle. Vet Parasitol 177:162–165

    PubMed  Google Scholar 

  3. 3.

    Šlapeta JR, Modrý D, Votýpka J, Jirků M, Lukeš J, Koudela B (2003) Evolutionary relationships among cyst-forming coccidia Sarcocystis spp. (Alveolata: Apicomplexa: Coccidea) in endemic African tree vipers and perspective for evolution of heteroxenous life cycle. Mol Phylogenet Evol 27:464–475

    PubMed  Google Scholar 

  4. 4.

    Dubey JP, Saville WJA, Lindsay DS, Stich RW, Stanek JF, Speer CA, Rosenthal BM, Njoku CJ, Kwok OCH, Shen SK (2000) Completion of the life cycle of Sarcocystis neurona. J Parasitol 86:1276–1280

    CAS  PubMed  Google Scholar 

  5. 5.

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

    CAS  PubMed  Google Scholar 

  6. 6.

    Lau YL, Chang PY, Subramaniam V, Ng YH, Mahmud R, Ahmad AF, Fong MY (2013) Genetic assemblage of Sarcocystis spp. in Malaysian snakes. Parasit Vectors 6:257

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    Lindsay DS, Blagburn BL, Braund KG (1995) Sarcocystis spp. and sarcocystosis. Br Med J 5:249–254

    Google Scholar 

  8. 8.

    Levine ND (2018) The Protozoan Phylum Apicomplexa, vol 2. CRC Press, Boca Raton, Florida, USA

    Google Scholar 

  9. 9.

    Moré G, Schares S, Maksimov A, Conraths FJ, Venturini MC, Schares G (2013) Development of a multiplex real time PCR to differentiate Sarcocystis spp. affecting cattle. Vet Parasitol 197:85–94

    PubMed  Google Scholar 

  10. 10.

    Dehaghi MM, Fallahi M, Sami M, Radfar MH (2013) Survey of Sarcocystis infection in slaughtered sheep in Kerman Abattoir, Kerman. Iran Comp Clin Path 22:343–346

    Google Scholar 

  11. 11.

    Bahari P, Salehi M, Seyedabadi M, Mohammadi A (2014) Molecular identification of macroscopic and microscopic cysts of Sarcocystis in sheep in north khorasan province, iran. Int J Mol Cell Med 3:51–56

    CAS  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Dubey JP (2015) Foodborne and waterborne zoonotic sarcocystosis. Food Waterborne Parasitol 1:2–11

    Google Scholar 

  13. 13.

    Dubey JP, Speer CA, Charleston WAG (1989) Ultrastructural differentiation between sarcocysts of Sarcocystis hirsuta and Sarcocystis hominis. Vet Parasitol 34:153–157

    CAS  PubMed  Google Scholar 

  14. 14.

    Martínez-Navalón B, Anastasio-Giner B, Cano-Fructuoso M, Sanchez-Martínez P, Llopis-Morant A, Perez-Castarlenas B, Goyena E, de Larrea EBF (2012) Sarcocystis infection: a major cause of carcass condemnation in adult sheep in Spain. Spanish J Agric Res 10:388–392

    Google Scholar 

  15. 15.

    Nourollahi Fard SR, Asghari M, Nouri F (2009) Survey of Sarcocystis infection in slaughtered cattle in Kerman. Iran Trop Anim Health Prod 41:1633–1636. https://doi.org/10.1007/s11250-009-9358-z

    Article  PubMed  Google Scholar 

  16. 16.

    Ghisleni G, Robba S, Germani O, Scanziani E (2006) Identification and prevalence of Sarcocystis spp. cysts in bovine canned meat. Food Control 17:691–694

    Google Scholar 

  17. 17.

    Stojecki K, Karamon J, Sroka J, Cencek T (2012) Molecular diagnostics of Sarcocystis spp. infections. Pol J Vet Sci 15:589–596

    CAS  PubMed  Google Scholar 

  18. 18.

    Daptardar M, Singh BB, Aulakh RS, Gill JPS (2016) Prevalence and first molecular identification of Sarcocystis species in cattle and water buffaloes in India. Acta Parasitol 61:523–528

    CAS  PubMed  Google Scholar 

  19. 19.

    Hooshyar H, Abbaszadeh Z, Sharafati-Chaleshtori R, Arbabi M (2017) Molecular identification of Sarcocystis species in raw hamburgers using PCR-RFLP method in Kashan, central Iran. J Parasit Dis 41:1001–1005. https://doi.org/10.1007/s12639-017-0925-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Nourani H, Matin S, Nouri A, Azizi H (2010) Prevalence of thin-walled Sarcocystis cruzi and thick-walled Sarcocystis hirsuta or Sarcocystis hominis from cattle in Iran. Trop Anim Health Prod 42:1225–1227. https://doi.org/10.1007/s11250-010-9552-z

    Article  PubMed  Google Scholar 

  21. 21.

    Oryan A, Moghaddar N, Gaur SN (1996) The distribution pattern of Sarcocystis species, their transmission and pathogenesis in sheep in Fars Province of Iran. Vet Res Commun 20:243–253

    CAS  PubMed  Google Scholar 

  22. 22.

    Fayer R, Esposito DH, Dubey JP (2015) Human infections with Sarcocystis species. Clin Microbiol Rev 28:295–311

    PubMed  PubMed Central  Google Scholar 

  23. 23.

    Fayer R (2004) Sarcocystis spp. in human infections. Clin Microbiol Rev 17:894–902

    PubMed  PubMed Central  Google Scholar 

  24. 24.

    Franco CD, Schnittger L, Florin-Christensen M (2018) Sarcocystis. In: Florin-Christensen M, Schnittger L (eds) Parasitic protozoa of farm animals and pets. Springer, Cham, pp 103–124. https://doi.org/10.1007/978-3-319-70132-5_4

    Chapter  Google Scholar 

  25. 25.

    Agholi M, Shahabadi SN, Motazedian MH, Hatam GR (2016) Prevalence of enteric protozoan oocysts with special reference to Sarcocystis cruzi among fecal samples of diarrheic immunodeficient patients in Iran. Korean J Parasitol 54:339–344. https://doi.org/10.3347/kjp.2016.54.3.339

    Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Harris VC, van Vugt M, Aronica E, De Bree GJ, Stijnis C, Goorhuis A, Grobusch MP (2015) Human extraintestinal sarcocystosis: what we know, and what we don’t know. Curr Infect Dis Rep 17:42

    PubMed Central  Google Scholar 

  27. 27.

    Hajimohammadi B, Dehghani A, Ahmadi MM, Eslami G, Oryan A, Khamesipour A (2014) Prevalence and species identification of Sarcocystis in raw hamburgers distributed in Yazd, Iran using PCR-RFLP. J Food Qual Hazards Control 1:15–20

    CAS  Google Scholar 

  28. 28.

    Hosseini H, Khaksar R, Shemshadi B (2007) Study on infestation of raw hamburgers to Sarcocystis cyst in Tehran. Iran Nut Sci 4:65–70

    Google Scholar 

  29. 29.

    Prayson B, McMahon JT, Prayson RA (2008) Fast food hamburgers: what are we really eating? Ann Diagn Pathol 12:406–409

    PubMed  Google Scholar 

  30. 30.

    Khaniki GRJ, Kia EB (2006) Detection of Sarcocystis cysts from meat supplied for hamburger in Iran by histological method. J Med Sci 6:18–21. https://doi.org/10.3923/jms.2006.18.21

    CAS  Article  Google Scholar 

  31. 31.

    Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6:e1000097. https://doi.org/10.1371/journal.pmed1000097

    Article  Google Scholar 

  32. 32.

    Modesti PA, Reboldi G, Cappuccio FP, Agyemang C, Remuzzi G, Rapi S, Perruolo E, Parati G, Settings ESHWG on CVR in LR (2016) Panethnic differences in blood pressure in europe: a systematic review and meta-analysis. PLoS ONE 11:e0147601. https://doi.org/10.1371/journal.pone.0147601

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Anvari D, Sharif M, Sarvi S, Aghayan SA, Gholami S, Pagheh AS, Hosseini SA, Saberi R, NayeriChegeni T, Hosseininejad Z, Daryani A (2019) Seroprevalence of Toxoplasma gondii infection in cancer patients: a systematic review and meta-analysis. Microb Pathog 129:30–42. https://doi.org/10.1016/J.MICPATH.2019.01.040

    Article  PubMed  Google Scholar 

  34. 34.

    Siyadatpanah A, Anvari D, Emami Zeydi A, Hosseini SA, Daryani A, Sarvi S, Budke CM, Esmaeelzadeh Dizaji R, Mohaghegh MA, Kohansal MH, Dodangeh S, Saberi R, Gholami S (2019) A systematic review and meta-analysis for genetic characterization of human echinococcosis in Iran, an endemic country. Epidemiol Health 41:e2019024. https://doi.org/10.4178/epih.e2019024

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Saberi R, Sharif M, Sarvi S, Aghayan SA, Hosseini SA, Anvari D, Nayeri Chegeni T, Hosseininejad Z, Daryani A (2018) Is Toxoplasma gondii playing a positive role in multiple sclerosis risk? A systematic review and meta-analysis. J Neuroimmunol 322:57–62. https://doi.org/10.1016/j.jneuroim.2018.06.011

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Hosseininejad Z, Sharif M, Sarvi S, Amouei A, Hosseini SA, Nayeri Chegeni T, Anvari D, Saberi R, Gohardehi S, Mizani A, Sadeghi M, Daryani A (2018) Toxoplasmosis seroprevalence in rheumatoid arthritis patients: a systematic review and meta-analysis. PLoS Negl Trop Dis 12:e0006545. https://doi.org/10.1371/journal.pntd.0006545

    Article  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Chegeni TN, Sharif M, Sarvi S, Moosazadeh M, Montazeri M, Aghayan SA, Balalami NJ, Gholami S, Hosseininejad Z, Saberi R, Anvari D, Gohardehi S, Daryani A (2019) Is there any association between Toxoplasma gondii infection and depression? A systematic review and meta-analysis. PLoS ONE 14:e0218524. https://doi.org/10.1371/journal.pone.0218524

    CAS  Article  Google Scholar 

  38. 38.

    Gharagozlou MJ, Darakhshandeh.K, Bokaie.S, (2001) a survey of the sarcocystosis in cattle slaughtered at Hamedan abattoire using histopathological and enzyme digestion methods. J Vet Res 56:75–79

    Google Scholar 

  39. 39.

    Shekarforoush SS, Alikhani R (2003) The infection rate of Sarcocystis in slaughtered sheep in Isfahan by impression method. Pajouhesh Sazandegi 16:68–72

    Google Scholar 

  40. 40.

    Kajouri GA, Karimi I, Malekian M (2004) Microscopic and histopathological approaches to acquired complications of sheep heart in shahrekord slaughterhouse. Pajouhesh Sazandegi 17:24–30

    Google Scholar 

  41. 41.

    Hadadzadeh H, Raazi J, Khazraeinia P, Taheri M, Rasekh A (2004) Serological study on sarcosystosis in slaughtered buffaloes (Bubalus bubalis) using IFAT compare with meat inspection finding in ahvaz abattoir. J Vet Res 59:183–188

    Google Scholar 

  42. 42.

    Shekarforoush SS, Razavi SM, Dehghan SA, Sarihi K (2005) Prevalence of Sarcocystis species in slaughtered goats in Shiraz. Iran Vet Rec 156:418–420

    CAS  PubMed  Google Scholar 

  43. 43.

    Shekarforoush SS, Shakerian A, Hasanpoor MM (2006) Prevalence of Sarcocystis in slaughtered one-humped camels (Camelus dromedarius) in Iran. Trop Anim Health Prod 38:301–303

    CAS  PubMed  Google Scholar 

  44. 44.

    Bonyadian M, Meshki B (2006) Study on infestation of cow carcasses to Sarcocystis spp in slaughtered cows in Shahrekord by impression method. Pajouhesh Sazandegi 72:14–18

    Google Scholar 

  45. 45.

    Rassoli S, Nasiri M, Pashayan S, Ahari H (2006) Sarcocystosis in slaughtered animals examined by digestive method. J Comp Pathobiol 3:667–670

    Google Scholar 

  46. 46.

    Daryani A, Alaei R, Dehghan MH, Arab R, Sharif M, Ziaei H (2006) Survey of Sarcocystis infection in slaughtered sheep and buffaloes in Ardabil. Iran J Anim Vet Adv 5:60–62

    Google Scholar 

  47. 47.

    Arshad M, Dalimi A, Ghaffarifar F (2007) Comparative study on Sarcocystis diagnosis in meat of slaughtered sheep in Tabriz. Pajouhesh Sazandegi 75:68–72

    Google Scholar 

  48. 48.

    Valinezhad A, Oryan A, Ahmadi N (2008) Sarcocystis and its complications in camels (Camelus dromedarius) of eastern provinces of Iran. Korean J Parasitol 46:229–234. https://doi.org/10.3347/kjp.2008.46.4.229

    Article  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Paikari HA, Dalimi AH, Esmaeilzadeh M, Valizadeh M, Karimi GHR, Motamedi GHR, Abdi GM (2008) Identification of Sarcocystis species of slaughtered sheep in Qazvin ziaran slaughterhouse using PCR–RFLP. Modares J Med Sci 11:65–72

    Google Scholar 

  50. 50.

    Rasouli S, Rahmanpour K, Jafari K, Sahandi A (2009) Survey of Sarcocysteine protozoans contamination of meat of Bukan by digestion method. J Vet Med 3:71–75

    Google Scholar 

  51. 51.

    Dalimi AH, Arshad M, Ghaffarifar F (2009) Assessment of Sarcocystis infection in slaughtered goats by different methods. Pajouhesh Sazandegi 21:38–42

    Google Scholar 

  52. 52.

    Hosseini SR, Ataie A, Rahimi E, Jafarian M (2009) Prevalence of sarcocystosis in camel in Najafabad slaughter house. J Vet Pathobiol 1:41–47

    Google Scholar 

  53. 53.

    Hamidinejat H, Jalali MHR, Nabavi L (2010) Survey on Sarcocystis infection in slaughtered cattle in South–West of Iran, emphasized on evaluation of muscle squash in comparison with digestion method. J Anim Vet Adv 9:1724–1726. https://doi.org/10.3923/javaa.2010.1724.1726

    Article  Google Scholar 

  54. 54.

    Rasouli S, Rahmanpour K, Jafari K, Sahandi A (2010) Survey of Sarcocystis protozoal contamination of meat in Sanandaj city by digestion method. J Large Anim Clin Sci Res 3:71–75

    Google Scholar 

  55. 55.

    Dalimi Asl AH, Arshad M, Ghafarifar F (2010) Prevalence of Sarcocystis infection in slaughtered cattle in Tabriz abattoir. Sci Iran Vet J 6:64–69

    Google Scholar 

  56. 56.

    Oryan A, Ahmadi N, Mousavi SMM (2010) Prevalence, biology, and distribution pattern of Sarcocystis infection in water buffalo (Bubalus bubalis) in Iran. Trop Anim Health Prod 42:1513–1518. https://doi.org/10.1007/s11250-010-9601-7

    Article  PubMed  Google Scholar 

  57. 57.

    Dehaghi MM, Fathi S, Asl EN (2011) Survey of Sarcocystis infection in slaughtered goats in Kerman abattoir, southeast of Iran. J Anim Vet Adv 10:1205–1208. https://doi.org/10.3923/javaa.2011.1205.1208

    Article  Google Scholar 

  58. 58.

    Rahdar M, Salehi M (2011) The prevalence of Sarcocystis infection in slaughtered cattle and sheep using digestion method in Ahvaz city of Iran. Biochem Cell Arch 11:469–471

    Google Scholar 

  59. 59.

    Tabrizi SS (2011) Prevalence of thin-walled microscopic Sarcocystis in karaj cattle slaughterhouse. Shahid Bahonar University of Kerman. (D.V.M degree thesis)

  60. 60.

    Borjian A (2011) Identification of Sarcocystis species in cattle in Shahrekord region using PCR-RFLP method. Shahrekord University. (D.V.M degree thesis)

  61. 61.

    Rahimi E, Doosti A, Hosseini SR, Homayouni M, Abdizadeh R (2012) Identify of Sarcocytis hominis in cattle carcasses using PCR method. J Comp Pathobiol Iran 9:661–664

    Google Scholar 

  62. 62.

    Hosseini SR, Shakerian A, Tahamtan N (2012) Survey of Sarcocystis infection in slaughtered sheep in Isfahan, Qom and Shahre-Kord. Iran J Anim Vet Adv 11:2683–2686. https://doi.org/10.3923/javaa.2012.2683.2686

    Article  Google Scholar 

  63. 63.

    Vosoughi H, Hoghoughirad N, Rahbari S (2012) The comparision of macroscopic and microscopic methods for detection of Sarcocystis spp. in sheep in the slaughterhouses of lorestan province. J Large Anim Clin Sci Res 6:63–69

    Google Scholar 

  64. 64.

    Kargar Jahromi Z, Solhjoo K, Zareian Jahromi M, Kargar Jahromi H, Erfaniyan S, Esmi M (2012) Investigation of Sarcocystis infection in slaughtered goats in Jahrom Abattoir. J Fasa Univ Med Sci 2:163–167

    Google Scholar 

  65. 65.

    Shamsi M (2012) Prevalence of Thin-walled Microscopic Sarcocystis in Cattle Slaughtered in Kerman Slaughterhouse. Shahid Bahonar University of Kerman. (D.V.M degree thesis)

  66. 66.

    Hamidinejat H, Hekmatimoghaddam S, Jafari H, Sazmand A, Haddad Molayan P, Derakhshan L, Mirabdollahi S (2013) Prevalence and distribution patterns of Sarcocystis in camels (Camelus dromedarius) in Yazd province. Iran J Parasit Dis 37:163–165. https://doi.org/10.1007/s12639-012-0150-z

    Article  PubMed  Google Scholar 

  67. 67.

    Farhang-Pajuh F, Yakhchali M, Mardani K (2014) Molecular determination of abundance of infection with Sarcocystis species in slaughtered sheep of Urmia. Iran Vet Res Forum 5:181–186

    PubMed  Google Scholar 

  68. 68.

    Hajimohammadi B, Eslami G, Zohourtabar A, Dehghani A, Oryan A, Pourmirzaei Tafti H, Radouani F (2014) High occurrence of Sarcocystis Cysts in meat produced in Yazd, Central Iran. J Food Qual Hazards Control 1:95–101

    CAS  Google Scholar 

  69. 69.

    Salehi M, Bahari P, Vatanchian M (2014) First molecular identification of Sarcocystis ovicanis (Protozoa, Apicomplexa) in the brain of sheep in Iran. Iran J Parasitol 9:286–291

    PubMed  PubMed Central  Google Scholar 

  70. 70.

    Rassouli M, Ahmadpanahi J, Alvandi A (2014) Prevalence of Sarcocystis spp. and Hammondia spp. microcysts in esophagus tissue of sheep and cattle, emphasized on their morphological differences. Parasitol Res 113:3801–3805

    PubMed  Google Scholar 

  71. 71.

    Nourollahi-Fard SR, Kheirandish R, Sattari S (2015) Prevalence and histopathological finding of thin-walled and thick-walled Sarcocystis in slaughtered cattle of Karaj abattoir. Iran J Parasit Dis 39:272–275. https://doi.org/10.1007/s12639-013-0341-2

    Article  PubMed  Google Scholar 

  72. 72.

    Parandin F, Feizi F, Maghsood AH, Matini M, Roshan A, Fallah M (2015) A survey on Sarcocystis infection rate in slaughtered cattle and sheep by macroscopic inspection and pepsin digestion methods in Hamadan abattoir, iran, 2014. Avicenna J Clin Med 22:210–216

    Google Scholar 

  73. 73.

    Faghiri E (2015) Histopathologic study of cystic lesions of Sarcocystis parasites in cattle slaughtered in Zabol, Iran. Zabol University. (D.V.M degree thesis)

  74. 74.

    Kalantari N, Khaksar M, Ghaffari S, Hamidekish SM (2016) Molecular Analysis of Sarcocystis Spp. Isolated from Sheep (Ovis aries) in Babol area, Mazandaran Province. Northern Iran Iran J Parasitol 11:73–80

    PubMed  Google Scholar 

  75. 75.

    Mirzaei M, Rezaei H (2016) The role of sheep in the epidemiology of Sarcocystis spp. in Tabriz area northwest of Iran. J Parasit Dis 40:285–288. https://doi.org/10.1007/s12639-014-0495-6

    Article  PubMed  Google Scholar 

  76. 76.

    Mirzaei M, Rezaei H (2016) A survey on Sarcocystis spp. infection in cattle of Tabriz city. Iran J Parasit Dis 40:648–651. https://doi.org/10.1007/s12639-014-0551-2

    Article  PubMed  Google Scholar 

  77. 77.

    Askari F (2016) Molecular detection of Sarcocystis cruzi and Sarcocystis hominis species in cattle slaughtered in Tabriz abattoir by PCR-RFLP. University of Tabriz. (D.V.M degree thesis)

  78. 78.

    Salimi A (2016) Survey of Sarcocystis Infection in carcass of slaughtered sheep in Birjand slaughterhouse. Zabol University. (D.V.M degree thesis)

  79. 79.

    Ghafari S (2016) Molecular detection of Sarcocystis species in cattle slaughtered in Tabriz slaughterhouse by allele-specific PCR. University of Tabriz. (D.V.M degree thesis)

  80. 80.

    Abdollahzade S (2016) Molecular detection of Sarcocystis species in slaughtered sheep in Tabriz slaughterhouse using SSCP technique. University of Tabriz. (D.V.M degree thesis)

  81. 81.

    Rahdar M, Kardooni T (2017) Molecular identification of Sarcocystis spp. in sheep and cattle by PCR-RFLP from southwest of Iran. Jundishapur J Microbiol 10:e12798. https://doi.org/10.5812/jjm.12798

    CAS  Article  Google Scholar 

  82. 82.

    Rasouli S, Chors FM (2017) Prevalence of Sarcocystis in goat carcasses slaughtered at the industrial Abattoir of Urmia. Iran by Digestive method Mech Dev 145:S35. https://doi.org/10.1016/j.mod.2017.04.043

    Article  Google Scholar 

  83. 83.

    Emdadi M (2017) Molecular study of Sarcocystis species contamination in minced meat presented in Tabriz by PCR-SSCP. University of Tabriz. (D.V.M degree thesis)

  84. 84.

    Shahraki MK, Ghanbarzehi A, Dabirzadeh M (2018) Prevalence and histopathology of Sarcocystosis in slaughtered carcasses in southeast Iran. J Adv Vet Anim Res 5:381–386. https://doi.org/10.5455/javar.2018.e288

    Article  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Oryan A, Sharifiyazdi H, Khordadmehr M, Larki S (2011) Characterization of Sarcocystis fusiformis based on sequencing and PCR-RFLP in water buffalo (Bubalus bubalis) in Iran. Parasitol Res 109:1563–1570. https://doi.org/10.1007/s00436-011-2412-6

    Article  PubMed  Google Scholar 

  86. 86.

    Hamidinejat H, Razi Jalali MH, Gharibi D, Molayan PH (2015) Detection of Sarcocystis spp. in cattle (Bos taurus) and water buffaloes (Bubalus bubalis) in Iran by PCR-RFLP. J Parasit Dis 39:658–662. https://doi.org/10.1007/s12639-014-0426-6

    Article  PubMed  Google Scholar 

  87. 87.

    Motamedi GR, Dalimi A, Nouri A, Aghaeipour K (2011) Ultrastructural and molecular characterization of Sarcocystis isolated from camel (Camelus dromedarius) in Iran. Parasitol Res 108:949–954. https://doi.org/10.1007/s00436-010-2137-y

    Article  PubMed  Google Scholar 

  88. 88.

    Eslampanah M, Motamedi GHR, Dalimi A, Noori A, Habibi GHR, Aghaeepour KH, Niroumand M (2016) Study of camel and goat Sarcocystis by electron microscopic and PCR–RFLP. Vet Res Biol Prod 29:77–84

    Google Scholar 

  89. 89.

    Kalantari N, Bayani M, Ghaffari S (2013) Sarcocystis cruzi: First molecular identification from cattle in Iran. Int J Mol Cell Med 2:125–130

    PubMed  PubMed Central  Google Scholar 

  90. 90.

    Shekarforoush SS, Razavi SM, Abbasvali M (2013) First detection of Sarcocystis hirsuta from cattle in Iran. Iran J Vet Res 14:155–157

    Google Scholar 

  91. 91.

    Eslami G, Zohourtabar A, Mehrizi SR (2014) First molecular identification of Sarcocystis hirsuta in Iranian beef: a case report. J food Qual hazards Control 1:32–34

    CAS  Google Scholar 

  92. 92.

    Motamedi GR, Dalimi A, Aghaeipour K, Nouri A (2010) Ultrastructural and molecular studies on fat and thin macrocysts of Sarcocystis spp. isolated from naturally infected goats. Arch Razi Inst 65:91–97

    Google Scholar 

  93. 93.

    Dalimi AH, Jalosian F, Tahvildar biderouni F, Ghaffarifar F (2010) Identification of Sarcocystis gigantea by PCR- RFLP. J Vet Res 65:43–46

  94. 94.

    Hamidinejat H, Moetamedi H, Alborzi A, Hatami A (2014) Molecular detection of Sarcocystis species in slaughtered sheep by PCR-RFLP from south-western Iran. J Parasit Dis 38:233–237. https://doi.org/10.1007/s12639-012-0231-z

    Article  PubMed  Google Scholar 

  95. 95.

    Hatami A, Rashno Z, Hamidinejat H, Youssefi MR (2017) Molecular identification of macroscopic cysts of Sarcocystis in sheep in Babol, in the north of Iran. Trop Biomed 34:405–411

    Google Scholar 

  96. 96.

    Bunyaratvej S, Unpunyo P, Pongtippan A (2007) The Sarcocystis-cyst containing beef and pork as the sources of natural intestinal sarcocystosis in Thai people. Med J Med Assoc Thail 90:2128

    Google Scholar 

  97. 97.

    Latif BMA, Al-Delemi JK, Mohammed BS, Al-Bayati SM, Al-Amiry AM (1999) Prevalence of Sarcocystis spp. in meat-producing animals in Iraq. Vet Parasitol 84:85–90

    CAS  PubMed  Google Scholar 

  98. 98.

    Anvari D, Saadati D, Nabavi R, Alipour Eskandani M (2018) Epidemiology and molecular prevalence of Toxoplasma gondii in cattle Slaughtered in Zahedan and Zabol districts, South East of Iran. Iran J Parasitol 13:114–119

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Taylor MA, Coop RL, Wall RL (2007) Veterinary parasitology, 3rd edn. Blackwell, Oxford, UK

    Google Scholar 

  100. 100.

    Vangeel L, Houf K, Chiers K, Vercruysse J, D’herde K, Ducatelle R (2007) Molecular-based identification of Sarcocystis hominis in Belgian minced beef. J Food Prot 70:1523–1526

    CAS  PubMed  Google Scholar 

  101. 101.

    Saito M, Shibata Y, Kubo M, Sakakibara I, Yamada A, Itagaki H (1999) First isolation of Sarcocystis hominis from cattle in Japan. J Vet Med Sci 61:307–309

    CAS  PubMed  Google Scholar 

  102. 102.

    Wee S-H, Shin S-S (2001) Experimental induction of the two-host life cycle of Sarcocystis cruzi between dogs and Korean native calves. Korean J Parasitol 39:227

    CAS  PubMed  PubMed Central  Google Scholar 

  103. 103.

    Böttner A, Charleston WAG, Pomroy WE, Rommel M (1987) The prevalence and identity of Sarcocystis in beef cattle in New Zealand. Vet Parasitol 24:157–168

    PubMed  Google Scholar 

  104. 104.

    Vercruysse J, Fransen J, Van Goubergen M (1989) The prevalence and identity of Sarcocystis cysts in cattle in Belgium. J Vet Med Ser B 36:148–153

    CAS  Google Scholar 

  105. 105.

    Woldemeskel M, Gebreab F (1996) Prevalence of Sarcocystis in livestock of northwest Ethiopia. J Vet Med Ser B 43:55–58

    CAS  Google Scholar 

  106. 106.

    Ozturk G (1994) Incidence of ovine sarcospordiosis in the myocardium of sheep. Saglik Bilim Derg 8:66–69

    Google Scholar 

  107. 107.

    Dong H, Su R, Wang Y, Tong Z, Zhang L, Yang Y, Hu J (2018) Sarcocystis species in wild and domestic sheep (Ovis ammon and Ovis aries) from China. BMC Vet Res 14:377

    PubMed  PubMed Central  Google Scholar 

  108. 108.

    Abo-Shehada MN (1996) Age variations in the prevalence of sarcocystosis in sheep and goats from northern and central Jordan. Prev Vet Med 27:135–140

    Google Scholar 

  109. 109.

    Bittencourt MV, Meneses IDS, Ribeiro-Andrade M, de Jesus RF, de Araújo FR, Gondim LFP (2016) Sarcocystis spp. in sheep and goats: frequency of infection and species identification by morphological, ultrastructural, and molecular tests in Bahia. Brazil Parasitol Res 115:1683–1689

    PubMed  Google Scholar 

  110. 110.

    Kudi AC, Aganga AO, Ogbogu VC, Umoh JU (1991) Prevalence of Sarcocystis species in sheep and goats in northern Nigeria. Rev Elev Med Vet Pays Trop 44:59–60

    CAS  PubMed  Google Scholar 

  111. 111.

    Al-Hoot AS, Al-Qureishy SA, Al-Rashid K, Bashtar AR (2005) Microscopic study on Sarcocystis moulei from sheep and goats in Saudi Arabia. J Egypt Soc Parasitol 35:295–312

    CAS  PubMed  Google Scholar 

  112. 112.

    Srivastava PS, Kumar A, Sinha SRP, Sinha AK (1991) Morphological differentiation of caprine Sarcocystis species: evidence of occurrence of Sarcocystis hircicanis in India. Acta Protozool 30:61–62

    Google Scholar 

  113. 113.

    Muangyai M, Chalermchaikit T (1988) The incidence of Sarcocystis in cattle and buffaloes. Thai J Vet Med 18:319–326

    Google Scholar 

  114. 114.

    Mohanty BN, Misra SC, Panda DN, Panda MR (1995) Prevalence of Sarcocystis infection in ruminants in Orissa. Indian Vet J 72:1026–1030

    Google Scholar 

  115. 115.

    Huong LTT (1999) Prevalence of Sarcocystis spp. in water buffaloes in Vietnam. Vet Parasitol 86:33–39

    CAS  PubMed  Google Scholar 

  116. 116.

    Fukuyo M, Battsetseg G, Byambaa B (2002) Prevalence of Sarcocystis infection in meat-producing animals in Mongolia. Southeast Asian J Trop Med Public Health 33:490–495

    CAS  PubMed  Google Scholar 

  117. 117.

    Fatani A, Hilali M, Al-Atiya S, Al-Shami S (1996) Prevalence of Sarcocystis in camels (Camelus dromedarius) from Al-Ahsa, Saudi Arabia. Vet Parasitol 62:241–245

    CAS  PubMed  Google Scholar 

  118. 118.

    Hussein HS, Warrag M (1985) Prevalence of Sarcocystis in food animals in the Sudan. Trop Anim Health Prod 17:100–101

    CAS  PubMed  Google Scholar 

  119. 119.

    El Sayed I, Ruppanner R, Ismail A, Champagne CP, Assaf R (1992) Antibacterial and antiviral activity of camel milk protective proteins. J Dairy Res 59:169–175

    Google Scholar 

  120. 120.

    Dubey US, Lal M, Mittal A, Kapur S (2016) Therapeutic potential of camel milk. Emir J Food Agric 28:164–176. https://doi.org/10.9755/ejfa.2015-04-122

    Article  Google Scholar 

  121. 121.

    Pritt B, Trainer T, Simmons-Arnold L, Evans M, Dunams D, Rosenthal BM (2008) Detection of Sarcocystis parasites in retail beef: a regional survey combining histological and genetic detection methods. J Food Prot 71:2144–2147

    PubMed  Google Scholar 

  122. 122.

    Timchuk VF, Dan’shin NS, Dan’shina MS, Dik ĖN (1990) Breed-dependent resistance of cattle to Sarcocystis bovihominis infection. Biol Khim Nauk 1:40–43

    Google Scholar 

  123. 123.

    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

    CAS  PubMed  Google Scholar 

  124. 124.

    Banothu D, Manchukonda U, Rayulu VC (2017) Diagnosis of bovine sarcocystosis by immunoflourescent antibody technique. J Parasit Dis 41:795–798

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors thank all colleagues working in Parasitology Department at Mazandaran University of Medical Sciences, Sari, Iran.

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DA, SG, AD, SS, AS, and SAH conceived and designed the study, and SAH and AD critically revised the manuscript. DA, EN, MH, MRN, DS, RS, SAS, and ASP searched the literature; DA, EN, and MRN extracted the data. DA wrote the manuscript and performed the statistical analysis. SAS designed figures. All authors have read and approved the final manuscript.

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Correspondence to Seyed Abdollah Hosseini or Abolghasem Siyadatpanah.

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Anvari, D., Narouei, E., Hosseini, M. et al. Sarcocystosis in Ruminants of Iran, as Neglected Food-Borne Disease: A Systematic Review and Meta-analysis. Acta Parasit. 65, 555–568 (2020). https://doi.org/10.2478/s11686-020-00210-5

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Keywords

  • Sarcocystis spp.
  • Sarcocystosis
  • Ruminant
  • Iran
  • Systematic review and meta-analysis