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Journal of Parasitic Diseases

, Volume 41, Issue 3, pp 754–760 | Cite as

The role of Linguatula serrata nymph in transmission of enteric bacterial pathogens to internal organs in sheep

  • Bahador Hajimohammadi
  • Gilda Eslami
  • Sepideh Khalatbari-limaki
  • Mohammad Hasan Ehrampoush
  • Ahmad Oryan
  • Hengameh Zandi
  • Hamid Reza Dehghan
Original Article

Abstract

Linguatula serrata is a worldwide zoonotic parasite belong to phylum Athropoda. When the eggs are swallowed by intermediate host, the larvae are released in intestine and reach the mesenteric lymph nodes (MLNs) and occasionally liver, lungs, heart, kidneys, spleen, and other body organs by the blood and lymph circulation. There are a few evidences showing transmission of microorganisms by migrating L. serrata. The aim of this study was to determine the role of L. serrata nymph in transmission of enteric bacterial pathogens to internal organs of sheep. For this purpose 11 parasite positive and 11 parasite negative MLNs to L. serrata were obtained from the native slaughtered sheep and were examined microbiologically in terms of bacterial contamination. The average total bacterial count and Escherichia coli count in the parasite positive samples were respectively 6.7 and 3.3 times higher than parasite negative ones (P < 0.05). However no significant differences were found for Salmonella and intestinal enterococci between parasite positive/negative samples. This indicates that L. serrata nymphs play as vehicles for bacteria and so contaminate offal. L. serrata nymphs transfer some bacterial agents to internal organs and enhance post mortem spoilage of the infected organs. It is also able to transfer some bacterial pathogens to internal organs which could potentially be the etiology of severe infectious or even zoonotic diseases. Especially in some regions where the consumption of raw or semi-cooked lymph nodes and other visceral organs are common.

Keywords

Linguatula serrate Inoculative effect Mesenteric lymph nodes 

Notes

Acknowledgments

This study was supported by Research Center for Food Hygiene and Safety, Shahid Sadoughi University of Medical Sciences,Yazd, Iran.

Complaince with ethical standards

Conflict of interest

The author declares that there is no conflict of interest.

References

  1. Adams MR, Moss MO (2008) Food microbiology. RSC, CambridgeGoogle Scholar
  2. Akhondzadeh Basti A, Haddadzadeh H, Tajik H, Hajimohammadi B, Shirali S, Hemati M, Ahmadiara E (2011) Effect of different temperature conditions on survival time of Linguatula serrata nymphs. Hum Vet Med Int J Bioflux Soc 3:76–82Google Scholar
  3. Akhondzadeh Basti A, Hajimohamadi B (2010) Principles of meat and abattoirs hygiene. University of Tehran Press, Tehran, pp 93–95Google Scholar
  4. Alborzi A, Derakhshandeh T (2008) A survey of infection of Linguatula serrata nymphs in slaughtered sheep at Yasuj abattoir. Sci Res Iran Vet J 4:101–109Google Scholar
  5. Alzohairy AM (2014) Letter to the editor. J Food Qual Hazard Control 1:35Google Scholar
  6. Bamorovat M, Borhani-Zarandi M, Mostafavi M, Kheirandish R, Sharifi I, Radfar MH (2014) The prevalence of Linguatula serrata nymphs in mesenteric and mediastinal lymph nodes in one-humped camels (Camelus dromedarius) slaughtered in Rafsanjan slaughterhouse, Iran. J Parasit Dis 38:374–377CrossRefPubMedGoogle Scholar
  7. Ekperigin HE, Nagaraja KV (1998) Microbial food borne pathogens. Salmonella. Vet Clin N Am Food Anim Pract 14:17–29CrossRefGoogle Scholar
  8. Giraffa G (2002) Enterococci from foods. FEMS Microbiol Rev 26:163–171CrossRefPubMedGoogle Scholar
  9. Haddadzadeh H, Athari S, Abedini R, Nabian S, HajiMohamadi B (2010) One-humped camel (Camelus dromedarius) infestation with Linguatula serrata in Tabriz, Iran. Iran J Arthropod Born Dis 4:54–59Google Scholar
  10. Hajimohammadi B, Akhondzadeh Basti A, Shirali S (2012) Impact of sodium chloride and heat on survival time of Linguatula serrata nymphs in vitro: an experimental study. J Health Res 1:54–61Google Scholar
  11. Hami M, Naddaf S, Mobedi I, Zare-Bidaki M, Athari S, Hajimohammadi B, Anaraki-Mohammadi G (2009) Prevalence of Linguatula serrata infection in domestic bovids slaughtered in Tabriz abattoir, Iran. Iran J Parasitol 4:25–31Google Scholar
  12. Haneklaus AN, Harris KB, Griffin DB, Edrington TS, Lucia LM, Savell JW (2012) Salmonella prevalence in bovine lymph nodes differs among feedyards. J Food Prot 75:1131–1133CrossRefPubMedGoogle Scholar
  13. Institute of Standards and Industrial Research of Iran (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella. ISIRI 1810Google Scholar
  14. Institute of Standards and Industrial Research of Iran (2005) Microbiology of food and animal feeding stuffs––detection and enumeration of presumptive Escherichia coli––most probable number technique. ISIRI 2946Google Scholar
  15. Institute of Standards and Industrial Research of Iran (2007) Microbiology of food and animal feeding stuffs––horizontal method for the enumeration of microorganisms––colony count technique at 30 c. ISIRI 5272Google Scholar
  16. Institute of Standards and Industrial Research of Iran (2008) Microbiology of foods and food stuffs––detection and enumeration of Enterococcus in food. ISIRI 2198Google Scholar
  17. International Organization for Standardization (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella spp. ISO 6579Google Scholar
  18. International Organization for Standardization (2005) Microbiology of food and animal feeding stuffs––horizontal method for the detection and enumeration of presumptive Escherichia coli––most probable number technique. ISO 7251Google Scholar
  19. International Organization for Standardization (2013) Microbiology of the food chain––horizontal method for the enumeration of microorganisms––part 1: colony count at 30 degrees C by the pour plate technique. ISO 4833-1Google Scholar
  20. Khalil GM, Schacher JF (1965) Linguatula serrata in relation to halzoun and the marrara syndrome. Am J Trop Med Hyg 14:736–746CrossRefPubMedGoogle Scholar
  21. Khalil G, Haddad C, Otrock ZK, Jaber F, Farra A (2012) Halzoun, an allergic pharyngitis syndrome in Lebanon: the trematode Dicrocoelium dendriticum as an additional cause. Acta Trop 125:115–118CrossRefPubMedGoogle Scholar
  22. Koehsler M, Walochnik J, Georgopoulos M, Pruente C, Boeckeler W, Auer H, Barisani-Asenbauer T (2011) Linguatula serrata tongue worm in human eye, Austria. Emerg Infect Dis 17:870–872CrossRefPubMedPubMedCentralGoogle Scholar
  23. Lazo R, Hidalgo E, Lazo J, Bermeo A, Llaguno M, Murillo J, Teixeira V (1999) Ocular linguatuliasis in ecuador: case report and morphometric study of the larva of Linguatula serrata. Am J Trop Med Hyg 60:405–409CrossRefPubMedGoogle Scholar
  24. Maleky F (2001) A case report of Linguatula serrata in human throat from Tehran, central Iran. Indian J Med Sci 55:439PubMedGoogle Scholar
  25. Meshgi B, Asgarian O (2003) Prevalence of Linguatula serrata infestation in stray dogs of Shahrekord, Iran. J Vet Med Ser B 50:466–467CrossRefGoogle Scholar
  26. Miclăuş V, Mihalca A, Negrea O, Oană L (2008) Histological evidence for inoculative action of immature Linguatula serrata in lymph nodes of intermediate host. Parasitol Res 102:1385–1387CrossRefPubMedGoogle Scholar
  27. Mir MS, Darzi MM, Hussain I, Wani SA (2009) Concurrent occurrence of visceral linguatulosis and paratuberculosis in alpine cross goats (Capra hircus). Vet Arh 79:301–314Google Scholar
  28. Nourollahi Fard SR, Kheirandish R, Norouzi Asl E, Fathi S (2010a) The prevalence of Linguatula serrata nymphs in goats slaughtered in Kerman slaughterhouse, Kerman, Iran. Vet Parasitol 171:176–178CrossRefPubMedGoogle Scholar
  29. Nourollahi Fard SR, Kheirandish R, Norouzi Asl E, Fathi S (2010b) The prevalence of Linguatula serrata nymphs in mesenteric lymph nodes in cattle. Am J Anim Vet Sci 5:155–158CrossRefGoogle Scholar
  30. Oryan A, Moghaddar N, Hanifepour MR (1993) Arthropods recovered from the visceral organs of camel with special reference to their incidence and pathogenesis in fars province of Iran. Indian J Anim Sci 63:290–293Google Scholar
  31. Oryan A, Sadjjadi S, Mehrabani D, Rezaei M (2008) The status of Linguatula serrata infection of stray dogs in Shiraz, Iran. Comp Clin Pathol 17:55–60CrossRefGoogle Scholar
  32. Oryan A, Khordadmehr M, Ranjbar VR (2011) Prevalence, biology, pathology, and public health importance of linguatulosis of camel in Iran. Trop Anim Health Prod 43:1225–1231CrossRefPubMedGoogle Scholar
  33. Rezaei F, Tavassoli M, Mahmoudian A (2011) Prevalence of Linguatula serrata infection among dogs (definitive host) and domestic ruminants (intermediate host) in the North West of Iran. Vet Med 56:561–567Google Scholar
  34. Rezaei H, Ashrafihelan J, Nematollahi A, Mostafavi E (2012) The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran. J Parasit Dis 36:200–202CrossRefPubMedPubMedCentralGoogle Scholar
  35. SadeghiDehkordi Z, Pajohi-Alamoti MR, Azami S, Bahonar AR (2013) Prevalence of Linguatula serrata in lymph nodes of small ruminants: case from Iran. Comp Clin Pathol 23:785–788Google Scholar
  36. Sajjadi S, Ardehali S, Shojaei A (1998) A case report of Linguatula serrata in human pharynx from Shiraz, southern Iran. Med J Islam Repub Iran 12:193–194Google Scholar
  37. Shekarforoush SS, Razavi S, Izadi M (2004) Prevalence of Linguatula serrata nymphs in sheep in Shiraz, Iran. Small Rumin Res 52:99–101CrossRefGoogle Scholar
  38. Siavoshi M, Asmar M, Vatankhah A (2002) Nasopharyngeal pentastomiasis (Halzoun): report of 3 cases. Iran J Med Sci 27:191–192Google Scholar
  39. Sohair IB, Eman MN (2009) Histopathological and bacteriological studies on livers affected with fascioliasis in cattle. Egypt J Comp Pathol Clin Pathol 22:19–45Google Scholar
  40. Svanevik CS, Levsen A, Lunestad BT (2013) The role of muscle-invading anisakid larvae on bacterial contamination of the flesh of post-harvest blue whiting (Micromesistius poutassou). Food Control 30:526–530CrossRefGoogle Scholar
  41. Svanevik CS, Lunestad BT, Levsen A (2014) Effect of Anisakis simplex larvae on the spoilage rate and shelf-life of fish mince products under laboratory conditions. Food Control 46:121–126CrossRefGoogle Scholar
  42. Tajik H, Tavassoli M, Dalir-Naghadeh B, Danehloipour M (2006) Mesenteric lymph nodes infection with Linguatula serrata nymphs in cattle. Iran J Vet Res 7:82–87Google Scholar
  43. Tajik H, Tavassoli M, Javadi S, Baghebani H (2008) The prevalence rate of Linguatula serrata nymphs in Iranian river buffaloes. Asian J Anim Vet Adv 3:174–178CrossRefGoogle Scholar
  44. Tavasoli M, Tajik H, Dalir-Naghadeh B, Lotfi H (2007) Study of Linguatula serrata infestation in mesenteric lymph nodes of goats in slaughterhouse of Urmia, Iran. Iran Vet J 2:85–89Google Scholar
  45. Tavassoli M, Tajik H, Dalir-Naghadeh B, Hariri F (2007) Prevalence of Linguatula serrata nymphs and gross changes of infected mesenteric lymph nodes in sheep in Urmia, Iran. Small Rumin Res 72:73–76CrossRefGoogle Scholar
  46. Yagi H, El Bahari S, Mohamed HA, Ahmed ERS, Mustafa B, Mahmoud M, Saad M, Sulaiman SM, El Hassan AM (1996) The marrara syndrome: a hypersensitivity reaction of the upper respiratory tract and buccopharyngeal mucosa to nymphs of Linguatula serrata. Acta Trop 62:127–134CrossRefPubMedGoogle Scholar
  47. Yakhchali M, Athari S, Hajimohammadi B, Raeisi M (2009) Prevalence of linguatula serrata in the ruminants slaugtered in Urmia slauhterhouse, Iran. Iran J Vet Res 64:329–332Google Scholar
  48. Yeghaneh Moghadam A, Talari SA, Dehghani R (2001) A case of human Linguatula serrata infestation in Kashan. J Kerman Univ Med Sci 8:175–178Google Scholar

Copyright information

© Indian Society for Parasitology 2017

Authors and Affiliations

  • Bahador Hajimohammadi
    • 1
    • 2
  • Gilda Eslami
    • 1
    • 3
  • Sepideh Khalatbari-limaki
    • 2
  • Mohammad Hasan Ehrampoush
    • 1
  • Ahmad Oryan
    • 4
  • Hengameh Zandi
    • 5
  • Hamid Reza Dehghan
    • 6
  1. 1.Research Center for Food Hygiene and SafetyShahid Sadoughi University of Medical SciencesYazdIran
  2. 2.Department of Food Hygiene and SafetyShahid Sadoughi University of Medical SciencesYazdIran
  3. 3.Department of Parasitology and MycologyShahid Sadoughi University of Medical SciencesYazdIran
  4. 4.Department of PathologyShiraz UniversityShirazIran
  5. 5.Department of Medical MicrobiologyShahid Sadoughi University of Medical SciencesYazdIran
  6. 6.Department of Health Technology AssessmentShahid Sadoughi University of Medical SciencesYazdIran

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