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Published in: Journal of Parasitic Diseases 3/2017

01-09-2017 | Original Article

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

Authors: Bahador Hajimohammadi, Gilda Eslami, Sepideh Khalatbari-limaki, Mohammad Hasan Ehrampoush, Ahmad Oryan, Hengameh Zandi, Hamid Reza Dehghan

Published in: Journal of Parasitic Diseases | Issue 3/2017

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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.
Literature
go back to reference Adams MR, Moss MO (2008) Food microbiology. RSC, Cambridge Adams MR, Moss MO (2008) Food microbiology. RSC, Cambridge
go back to reference 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 3:76–82 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 3:76–82
go back to reference Akhondzadeh Basti A, Hajimohamadi B (2010) Principles of meat and abattoirs hygiene. University of Tehran Press, Tehran, pp 93–95 Akhondzadeh Basti A, Hajimohamadi B (2010) Principles of meat and abattoirs hygiene. University of Tehran Press, Tehran, pp 93–95
go back to reference Alborzi A, Derakhshandeh T (2008) A survey of infection of Linguatula serrata nymphs in slaughtered sheep at Yasuj abattoir. Sci Res Iran Vet J 4:101–109 Alborzi A, Derakhshandeh T (2008) A survey of infection of Linguatula serrata nymphs in slaughtered sheep at Yasuj abattoir. Sci Res Iran Vet J 4:101–109
go back to reference Alzohairy AM (2014) Letter to the editor. J Food Qual Hazard Control 1:35 Alzohairy AM (2014) Letter to the editor. J Food Qual Hazard Control 1:35
go back to reference 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 38:374–377CrossRefPubMed 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 38:374–377CrossRefPubMed
go back to reference Ekperigin HE, Nagaraja KV (1998) Microbial food borne pathogens. Salmonella. Vet Clin N Am Food Anim Pract 14:17–29CrossRef Ekperigin HE, Nagaraja KV (1998) Microbial food borne pathogens. Salmonella. Vet Clin N Am Food Anim Pract 14:17–29CrossRef
go back to reference 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 4:54–59 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 4:54–59
go back to reference 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 1:54–61 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 1:54–61
go back to reference 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 4:25–31 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 4:25–31
go back to reference 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 75:1131–1133CrossRefPubMed 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 75:1131–1133CrossRefPubMed
go back to reference Institute of Standards and Industrial Research of Iran (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella. ISIRI 1810 Institute of Standards and Industrial Research of Iran (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella. ISIRI 1810
go back to reference 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 2946 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 2946
go back to reference 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 5272 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 5272
go back to reference Institute of Standards and Industrial Research of Iran (2008) Microbiology of foods and food stuffs––detection and enumeration of Enterococcus in food. ISIRI 2198 Institute of Standards and Industrial Research of Iran (2008) Microbiology of foods and food stuffs––detection and enumeration of Enterococcus in food. ISIRI 2198
go back to reference International Organization for Standardization (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella spp. ISO 6579 International Organization for Standardization (2002) Microbiology of food and animal feeding stuffs––horizontal method for the detection of Salmonella spp. ISO 6579
go back to reference 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 7251 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 7251
go back to reference 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 4833-1 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 4833-1
go back to reference Khalil GM, Schacher JF (1965) Linguatula serrata in relation to halzoun and the marrara syndrome. Am J Trop Med Hyg 14:736–746CrossRefPubMed Khalil GM, Schacher JF (1965) Linguatula serrata in relation to halzoun and the marrara syndrome. Am J Trop Med Hyg 14:736–746CrossRefPubMed
go back to reference 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 125:115–118CrossRefPubMed 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 125:115–118CrossRefPubMed
go back to reference 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 17:870–872CrossRefPubMedPubMedCentral 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 17:870–872CrossRefPubMedPubMedCentral
go back to reference 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 60:405–409CrossRefPubMed 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 60:405–409CrossRefPubMed
go back to reference Maleky F (2001) A case report of Linguatula serrata in human throat from Tehran, central Iran. Indian J Med Sci 55:439PubMed Maleky F (2001) A case report of Linguatula serrata in human throat from Tehran, central Iran. Indian J Med Sci 55:439PubMed
go back to reference Meshgi B, Asgarian O (2003) Prevalence of Linguatula serrata infestation in stray dogs of Shahrekord, Iran. J Vet Med Ser B 50:466–467CrossRef Meshgi B, Asgarian O (2003) Prevalence of Linguatula serrata infestation in stray dogs of Shahrekord, Iran. J Vet Med Ser B 50:466–467CrossRef
go back to reference 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 102:1385–1387CrossRefPubMed 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 102:1385–1387CrossRefPubMed
go back to reference Mir MS, Darzi MM, Hussain I, Wani SA (2009) Concurrent occurrence of visceral linguatulosis and paratuberculosis in alpine cross goats (Capra hircus). Vet Arh 79:301–314 Mir MS, Darzi MM, Hussain I, Wani SA (2009) Concurrent occurrence of visceral linguatulosis and paratuberculosis in alpine cross goats (Capra hircus). Vet Arh 79:301–314
go back to reference 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 171:176–178CrossRefPubMed 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 171:176–178CrossRefPubMed
go back to reference 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 5:155–158CrossRef 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 5:155–158CrossRef
go back to reference 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 63:290–293 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 63:290–293
go back to reference Oryan A, Sadjjadi S, Mehrabani D, Rezaei M (2008) The status of Linguatula serrata infection of stray dogs in Shiraz, Iran. Comp Clin Pathol 17:55–60CrossRef Oryan A, Sadjjadi S, Mehrabani D, Rezaei M (2008) The status of Linguatula serrata infection of stray dogs in Shiraz, Iran. Comp Clin Pathol 17:55–60CrossRef
go back to reference Oryan A, Khordadmehr M, Ranjbar VR (2011) Prevalence, biology, pathology, and public health importance of linguatulosis of camel in Iran. Trop Anim Health Prod 43:1225–1231CrossRefPubMed Oryan A, Khordadmehr M, Ranjbar VR (2011) Prevalence, biology, pathology, and public health importance of linguatulosis of camel in Iran. Trop Anim Health Prod 43:1225–1231CrossRefPubMed
go back to reference 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 56:561–567 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 56:561–567
go back to reference Rezaei H, Ashrafihelan J, Nematollahi A, Mostafavi E (2012) The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran. J Parasit Dis 36:200–202CrossRefPubMedPubMedCentral Rezaei H, Ashrafihelan J, Nematollahi A, Mostafavi E (2012) The prevalence of Linguatula serrata nymphs in goats slaughtered in Tabriz, Iran. J Parasit Dis 36:200–202CrossRefPubMedPubMedCentral
go back to reference 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 23:785–788 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 23:785–788
go back to reference 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 12:193–194 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 12:193–194
go back to reference Shekarforoush SS, Razavi S, Izadi M (2004) Prevalence of Linguatula serrata nymphs in sheep in Shiraz, Iran. Small Rumin Res 52:99–101CrossRef Shekarforoush SS, Razavi S, Izadi M (2004) Prevalence of Linguatula serrata nymphs in sheep in Shiraz, Iran. Small Rumin Res 52:99–101CrossRef
go back to reference Siavoshi M, Asmar M, Vatankhah A (2002) Nasopharyngeal pentastomiasis (Halzoun): report of 3 cases. Iran J Med Sci 27:191–192 Siavoshi M, Asmar M, Vatankhah A (2002) Nasopharyngeal pentastomiasis (Halzoun): report of 3 cases. Iran J Med Sci 27:191–192
go back to reference Sohair IB, Eman MN (2009) Histopathological and bacteriological studies on livers affected with fascioliasis in cattle. Egypt J Comp Pathol Clin Pathol 22:19–45 Sohair IB, Eman MN (2009) Histopathological and bacteriological studies on livers affected with fascioliasis in cattle. Egypt J Comp Pathol Clin Pathol 22:19–45
go back to reference 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 30:526–530CrossRef 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 30:526–530CrossRef
go back to reference 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 46:121–126CrossRef 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 46:121–126CrossRef
go back to reference Tajik H, Tavassoli M, Dalir-Naghadeh B, Danehloipour M (2006) Mesenteric lymph nodes infection with Linguatula serrata nymphs in cattle. Iran J Vet Res 7:82–87 Tajik H, Tavassoli M, Dalir-Naghadeh B, Danehloipour M (2006) Mesenteric lymph nodes infection with Linguatula serrata nymphs in cattle. Iran J Vet Res 7:82–87
go back to reference 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 3:174–178CrossRef 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 3:174–178CrossRef
go back to reference 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 2:85–89 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 2:85–89
go back to reference 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 72:73–76CrossRef 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 72:73–76CrossRef
go back to reference 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 62:127–134CrossRefPubMed 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 62:127–134CrossRefPubMed
go back to reference 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 64:329–332 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 64:329–332
go back to reference Yeghaneh Moghadam A, Talari SA, Dehghani R (2001) A case of human Linguatula serrata infestation in Kashan. J Kerman Univ Med Sci 8:175–178 Yeghaneh Moghadam A, Talari SA, Dehghani R (2001) A case of human Linguatula serrata infestation in Kashan. J Kerman Univ Med Sci 8:175–178
Metadata
Title
The role of Linguatula serrata nymph in transmission of enteric bacterial pathogens to internal organs in sheep
Authors
Bahador Hajimohammadi
Gilda Eslami
Sepideh Khalatbari-limaki
Mohammad Hasan Ehrampoush
Ahmad Oryan
Hengameh Zandi
Hamid Reza Dehghan
Publication date
01-09-2017
Publisher
Springer India
Published in
Journal of Parasitic Diseases / Issue 3/2017
Print ISSN: 0971-7196
Electronic ISSN: 0975-0703
DOI
https://doi.org/10.1007/s12639-017-0884-8

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