Skip to main content
NCBI home page
Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology logoLink to Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology
. 2013 Feb 15;38(4):374–377. doi: 10.1007/s12639-013-0258-9

The prevalence of Linguatula serrata nymphs in mesenteric and mediastinal lymph nodes in one-humped camels (Camelus dromedarius) slaughtered in Rafsanjan slaughterhouse, Iran

Mehdi Bamorovat 1, Mehdi Borhani Zarandi 2, Mahshid Mostafavi 1,✉, Reza Kheirandish 3, Iraj Sharifi 1, Mohammad Hossein Radfar 4
PMCID: PMC4185030  PMID: 25320486

Abstract

Linguatula serrata is a well-known zoonotic parasite belonging to the order of Pentastomida which infects both human and animals. Human can be infected by both the nymph stage, causing a disease condition called nasopharyngeal linguatulosis or halzoun syndrome and the egg, a condition called visceral linguatulosis. The aim of this study was to evaluate the prevalence of nymphal stages of L. serrata in mesenteric and mediastinal lymph nodes of one-humped camels slaughtered in Rafsanjan slaughterhouse, Kerman province, south-eastern Iran. For this purpose, mesenteric and mediastinal lymph nodes of 132 one-humped camels of different sex and age groups in different seasons were examined. Overall, 27 one-humped camels (20.5 %) were infected by L. serrata nymphs. The infection rate increased with age (P < 0.05). No significant difference by sex groups or seasons was observed (P > 0.05). The high prevalence of infection in one-humped camels is of major concern to public health, owing to the zoonotic nature of the parasite and the potential risk of infection to humans and other animals.

Keywords: Linguatula serrata, Lymph nodes, One-humped camels, Rafsanjan, Iran

Introduction

Linguatula serrata, is a tongue shaped parasite, lightly convex dorsally and flattened ventrally (Soulsby 1982). It is a cosmopolitan zoonotic parasite, belonging to the order of Pentastomida (Shekarforoush et al. 2004). Adults of L. serrata inhabit in the respiratory system (nasal sinuses and nasopharynx) of carnivorous especially dogs as definitive host (Alcala-vanto et al. 2007). It’s eggs containing fully developed larvae are discharged into the environment by nasal secretion of carnivores. Herbivores such as cattle, goats, camels and sheep as intermediate hosts digest the eggs. Parasite’s nymphal stages develop in various organs, particularly mesenteric and mediastinal lymph nodes of these animals (Berger and Marr 2006).

Humans can be infected by both adult stages, resulting in nasopharyngeal linguatulosis (halzoun syndrome) and the eggs causing a disease, called visceral linguatulosis. Ingestion of L. serrata nymphs with infected raw liver or lymph nodes of intermediate hosts can cause halzoun or marrara (maraca) syndrome in humans. Halzoun syndrome is often characterized by inflammation of the upper respiratory tract, swelling of the sub-maxillary and cervical lymph nodes and occasionally abscess formation in the eyes or ears (Yagi et al. 1996). The visceral form occurs by eating the eggs in contaminated water vegetables, or fruits (Yao et al. 2008; Tappe and Büttner 2009). This parasitic infection has also been reported in humans in Iran (Yeganeh Moghadam et al. 2001; Siavashi et al. 2002; Anaraki Mohammadi et al. 2008).

Several studies have been carried out regarding the prevalence rate of L. serrata infection in animals including dogs (Tavassoli et al. 2000; Meshgi and Asgarian 2003; Oryan et al. 2008), sheep (Esmail-Nia et al. 2000; Shekarforoush et al. 2004; Tavassoli et al. 2007; Ravindran et al. 2008; Nourollahi-Fard et al. 2011), goats (Razavi et al. 2004; Nourollahi-Fard et al. 2010b) and camels (Wahba et al. 1997; Tajik et al. 2007; Shakerian et al. 2008; Haddadzadeh et al. 2009).

The high prevalence of infection in ruminants is of concern owing to the zoonotic nature of the parasite and the potential risk of infection to humans and other animals.

So far no report of L. serrata infection has been carried out in camels of Rafsanjan, therefore the objective of this study was to determine the prevalence rate of L. serrata nymphs in mesenteric and mediastinal lymph nodes of one-humped camels slaughtered at Rafsanjan slaughterhouse.

Materials and methods

This study was conducted in Rafsanjan district. Rafsanjan is located in Kerman province, southeast of Iran. Kerman province has a moderate climate and the average annual rainfall is 135 mm, because it is located close to the Lut desert. Upon enquiry about the farming of the camels, most of the owners declared that they were raised in an open farming area.

Overall, 132 slaughtered camels including 61 males and 71 females were examined randomly for nymphal stages of L. serrata from March 2010 to March 2011 at Rafsanjan slaughterhouse.

The animals were classified in four age groups (<2, 2–4, 4–6 and >6 years old), and the age ranges were determined by using the eruption of permanent incisor teeth criteria as described elsewhere (Currasson 1947). Immediately after slaughtering, 4–6 samples from mesenteric and 2–3 samples from mediastinal lymph nodes, from each camel, were collected in plastic containers with the corresponding characteristic numbers and transferred to Medical School promptly for further examination.

Examination of the lymph nodes of the camels was performed in two steps. First, 50–100 g samples were sliced in small pieces and observed under stereomicroscope for observation of the nymphal stage. In the second step, the minced tissues were treated in 200 ml of digestion solution containing 5 g pepsin enzyme (7178, Merck) and 25 ml hydrochloric acid (374, Merck) in 1 L water and incubated at 37 °C for 24 h. Then, the suspensions were transferred to petri dishes and examined for L. serrata nymph (Shakerian et al. 2008).

Statistical analysis

Data were subjected to analysis using SPSS 17.0 software (SPSS Inc, Chicago, IL, USA). χ2-test was used to compare the relative frequency of infection among different groups by lymph nodes, age, sex and seasons. P ≤ 0.05 was considered as statistical difference.

Results

Twenty-seven out of 132 camels (20.5 %) were infected with L. serrata nymphs. The number of collected nymphs from each infected lymph node varied from 1 to 30. The infection rate of mesenteric and mediastinal lymph nodes were 26.5 and 14.1 %, respectively. The frequency of infection increased with age P < 0.05 (Table 1). However, there was no significant difference between sex and infection rate among the camels. The prevalence of L. serrata infection in different seasons is presented in Table 1, although no significant difference was observed (P > 0.05).

Table 1.

The prevalence of Linguatula serrata nymphs in camels slaughtered in Rafsanjan slaughter house by age, sex, seasons and lymph nodes, Iran

Parameter Infected no Non-infected no Total no
Age (years)
 <2 3 (2.3 %) 35 (26.5 %) 38 (28.8 %)
 2–4 8 (6.1 %) 37 (28 %) 45 (34 %)
 4–6 13 (9.8 %) 29 (22 %) 42 (31.8 %)
 >6 3 (2.3 %) 4 (3 %) 7 (5.4 %)
Sex
 Male 12 (9.1 %) 49 (37.1 %) 61 (46.2 %)
 Female 15 (11.4 %) 56 (42.4 %) 71 (53.8 %)
Seasons
 Spring 7 (5.4 %) 28 (21.2 %) 35 (26.5 %)
 Summer 6 (4.5 %) 23 (17.4 %) 29 (22 %)
 Autumn 8 (6.1 %) 29 (21.9 %) 37 (28 %)
 Winter 6 (4.5 %) 25 (19 %) 31 (23.5 %)
Lymph nodes
 Mesenteric or mediastinal 27 (20.5) 105 (79.5 %) 132 (100 %)
Total 27 (20.5) 105 (79.5 %) 132 (100 %)
Open in a new tab

Discussion

As intermediate hosts, camels, like other ruminants, play an important role in the life cycle of L. serrata. The prevalence rate of linguatulosis in dogs has been determined in different part of Iran such as Shiraz (76.2 %) by Oryan et al. (2008), Shahre-Kord (65.5 %) by Meshgi and Asgarian (2003) and Fars province (76.5 %) by Oryan et al. (1997). Close contact between dogs and the intermediate host plays an important role in transmission of L. serrata in this area. Many studies have been carried out on prevalence of L. serrata in various domestic ruminants in Iran and other parts of the world showing that L. serrata nymphs obtained from different visceral organs such as liver, lung and spleen (Tajik et al. 2008; Tavassoli et al. 2007; Nourollahi-Fard et al. 2010a; Razavi et al. 2004). But in most studies mesenteric and mediastinal lymph nodes were evaluated because they are the principal place of infection with parasite. Therefore, possibility of infection in mesenteric and mediastinal is higher than other viscera (Shakerian et al. 2008). Another study with slaughtered camels showed that mesenteric lymph nodes, the lungs and the liver were infected with L. serrata nymphs, (75, 29.7 and 30.4 %, respectively) of animals (Tajik et al. 2007). Shakerian et al. (2008) reported that mesenteric lymph nodes (21 %) and liver (4.5 %) were infected with the infective stage of these parasites in Najaf-Abad, Iran (2008). According to the life cycle of L. serrata, mesenteric lymph nodes, located in the way of portal circulation before the other organs, hence the infection rate of these nodes is higher than other organs. In this study, 26.5 and 14.1 % of the camels had L. serrata nymphs in mesenteric and mediastinal lymph nodes, respectively.

Several studies have been conducted to determine the prevalence of linguatulosis in ruminants in Iran and other countries. The prevalence rate was 44 % in cattle in Urmia slaughterhouse, Iran (Tajik et al. 2007), 29.9 % in goats in Shiraz, Iran (Razavi et al. 2004), 49.1 % in goats slaughtered in Kerman, Iran (Nourollahi-Fard et al. 2010b). Several studies regarding the prevalence of L. serrata nymphs in camels were carried out in Iran including Mashhad (75 and 18.3 % in two separate studies) (Tajik et al. 2007; Fard et al. 2012) and Najaf-Abad (35 and 21 %, in two separate studies) (Pourjafar et al. 2007; Shakerian et al. 2008) and 19 % in cattle of India (Ravindran et al. 2008).

The prevalence of the infection in camels may be influenced by many factors such as the geographic and climatic changes which affect the survival of the parasite eggs. Apparently, high prevalence rate of infection in Kerman province may be due to the suitable climatic conditions for the parasite to maintain the survival of it’s egg in vegetables, fruits, and water resources. The prevalence rate (20.5 %) of infection in lymph nodes should be considered as a risk factor for human being infection.

In several studies, seasonal variation of L. serrata infection in small ruminants of Iran was reported (Hamdast-joo 2001; Nematollahi et al. 2005). In our survey no significant difference between prevalence rates of infection in different seasons of the year was observed.

The results of our study showed a significant association of age and infection rate of camels (P < 0.05) that was consistent with other studies on sheep and camel in Iran (Shekarforoush et al. 2004; Shakerian et al. 2008). On the other hand no significant difference was observed in the infection rate in both sexes which was in agreement with other study (Shakerian et al. 2008).Due to the nature of such studies particularly in camels, the sample size seems to be enough as compared to the other studies (Haddadzadeh et al. 2010; Oryan et al. 2011).

Conclusion

Because of the veterinary and human medical importance of linguatulosis, further investigations in other herbivores, carnivores and also humans are recommended. This study showed a high risk of L. serrata for humans and other animal species. Adequate cooking of meat and viscera and drinking properly filtered water are crucial in preventing human infections.

Heightened public awareness of the danger of raw food and education of humans on different aspects of the epidemiology of the parasite together with preventing dogs or other canids ingesting infected materials should reduce the risk of infection and any such measures may also help to diminish other zoonoses.

References

  1. Alcala-Vanto Y, Alberti-Navarro A, Ibbara-Velarde F. Serin protease activity demonstrated in larval stage of the Pentastomid Linguatula serrata. Parasitol Res. 2007;100:1011–1014. doi: 10.1007/s00436-006-0374-x. [DOI] [PubMed] [Google Scholar]
  2. Anaraki Mohammadi G, Mobedi I, Ariaiepour M, Pourmohammadi Z, Zare Bidaki M. A case report of nasopharyngeal linguatuliasis in Tehran, Iran and characterization of the isolated Linguatula serrata. Iran J Parasitol. 2008;3:53–55. [Google Scholar]
  3. Berger SA, Marr JS. Human parasitic diseases source book. Sudbury: Jones & Bartlett Publishers; 2006. p. 294. [Google Scholar]
  4. Currasson G. Le chameau Estses maladies. Paris: Vigotfreres; 1947. pp. 188–237. [Google Scholar]
  5. Esmail-Nia K, Hadizadeh-Moalem S, Derakhshanfa A study on the prevalence of Linguatula serrata infestation in small ruminants of Mazandaran Province in babol abattoir. Pajouhesh Sazandegi. 2000;54:94–95. [Google Scholar]
  6. Fard SRN, Ghalekhani N, Kheirandish R, Fathi S, Asl EN. The prevalence of Linguatula serrata nymphs in camels slaughtered in Mashhad slaughterhouse, Northeast, Iran. Asian Pac J Trop Biomed. 2012;11:885–888. doi: 10.1016/S2221-1691(12)60247-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Haddadzadeh H, Shamsadin Athari S, Hajimohammadi B. The first record of Linguatula serrata infection of two-humped camel (Camelus bactrinus) in Iran. Iran J Parasitol. 2009;4:59–61. [Google Scholar]
  8. Haddadzadeh HR, Athari SS, Abedini R, Khazraii nia S, Khazraii nia P, Nabian S, Haji-Mohamadi B. One-humped camel (Camelus dromedarius) infestation with Linguatula serrata in Tabriz, Iran. Iran J Arthropod-Borne Dis. 2010;4(1):54–59. [PMC free article] [PubMed] [Google Scholar]
  9. Hamdast-joo M. Study of the prevalence of Linguatula serrata nymph in small ruminants in slaughterhouse of Shahryar, Iran. Karaj: School of Veterinary Medicine, Islamic Azad University, Karaj Branch; 2001. [Google Scholar]
  10. Meshgi B, Asgarian O. Prevalence of Linguatula serrata infestation in stray dogs of Shahrekord. Iran J Vet Med. 2003;50:466–467. doi: 10.1046/j.0931-1793.2003.00705.x. [DOI] [PubMed] [Google Scholar]
  11. Nematollahi A, Karimi H, Niyazpour F. The survey of infection rate and histopathological lesions due to nymph of linguatula serrata on slaughtered farm animals in East Azerbaijan slaughterhouses during different seasons of year. J Fac Vet Med Univ Tehran. 2005;60:161–165. [Google Scholar]
  12. Nourollahi-Fard SR, Kheirandish R, Nourouzi-Asl E, Fathi S. The prevalence of Linguatula serrata nymphs in mesenteric lymph nodes in cattle. Am J Anim Vet Sci. 2010;5(2):155–158. doi: 10.3844/ajavsp.2010.155.158. [DOI] [Google Scholar]
  13. Nourollahi-Fard SR, Kheirandish R, Nourouzi-Asl E, Fathi S. The prevalence of Linguatula serrata nymphs in goats slaughtered in Kerman slaughterouse, Kerman. Iran Vet Parasitol. 2010;171:176–178. doi: 10.1016/j.vetpar.2010.03.010. [DOI] [PubMed] [Google Scholar]
  14. Nourollahi-Fard SR, Kheirandish R, Nourouzi-Asl E, Fathi S. Mesenteric and mediastinal lymph node infection with Linguatula serrata nymphs in sheep slaughtered in Kerman slaughterhouse, Southeast Iran. Trop Anim Health Prod. 2011;43:1–3. doi: 10.1007/s11250-010-9670-7. [DOI] [PubMed] [Google Scholar]
  15. Oryan A, Sadjjadi SM, Rezaii M (1997) Prevalence of Linguatula serrata in stray dogs of Shiraz. In: Proceedings of the 2nd national congress of parasitic diseases. Tehran, p 176
  16. Oryan A, Sadjjadi SM, Mehrabani D, Rezaei M. The status of Linguatula serrata infection of stray dogs in Shiraz. Iran Comp Clin Pathol. 2008;17:55–60. doi: 10.1007/s00580-007-0707-x. [DOI] [Google Scholar]
  17. Oryan A, Khordadmehr M, Ranjbar VR. Prevalence, biology, pathology, and public health importance of linguatulosis of camel in Iran. Trop Anim Health Prod. 2011;43:1225–1231. doi: 10.1007/s11250-011-9830-4. [DOI] [PubMed] [Google Scholar]
  18. Pourjafar M, Azizi H, Darabi S, Khosravi M. The prevalence of nymphal stage of Linguatula serrata in camels (Camelus dromedarius) in Najaf-Abad. Iran J Camel Prac Res. 2007;14(2):171–173. [Google Scholar]
  19. Ravindran R, Lakshmanan B, Ravishankar C, Subramanian H. Prevalence of Linguatula serrata in domestic ruminants in South India, Southeast. Asian J Trop Med Public Health. 2008;39:808–812. [PubMed] [Google Scholar]
  20. Razavi SM, Shekarforoush SS, Izadi M. Prevalence of Linguatula serrata nymphs in goats in Shiraz, Iran. Small Rumin Res. 2004;54:213–217. doi: 10.1016/j.smallrumres.2003.11.013. [DOI] [Google Scholar]
  21. Shakerian A, Shekarforoush SS, Ghafari-Rad H. Prevalence of Linguatula serrata nymphs in Najaf-Abad. Iran Res Vet Sci. 2008;44:243–245. doi: 10.1016/j.rvsc.2007.04.015. [DOI] [PubMed] [Google Scholar]
  22. Shekarforoush SS, Razavi SM, Izadi M. Prevalence of Linguatula serrata nymphs in sheep in Shiraz. Iran Small Rumin Res. 2004;52:99–101. doi: 10.1016/S0921-4488(03)00224-4. [DOI] [Google Scholar]
  23. Siavashi MR, Assmar M, Vatankhah A. Nasopharyngeal Pentastomiasis (Halzoun): report of 3 Cases. Iran J Med Sci. 2002;27:191–192. [Google Scholar]
  24. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals, 7th edition. Philadelphia: Lea & Febiger; 1982. p. 809. [Google Scholar]
  25. Tajik H, Tavassoli M, Khani H, Javadi S. Prevalence of Linguatula serrata nymphs in slaughtered camels of Iran. J Camel Pract Res. 2007;14:69–71. [Google Scholar]
  26. Tajik H, Tavassoli M, Javadi S, Baghebani H. The prevalence rate of Linguatula serrata nymphs in Iranian River Buffaloes. Asian J Anim Vet Adv. 2008;3(3):174–178. doi: 10.3923/ajava.2008.174.178. [DOI] [Google Scholar]
  27. Tappe D, Büttner DW. Diagnosis of human visceral pentastomiasis. PLOS Negl Trop Dis. 2009;3:e320. doi: 10.1371/journal.pntd.0000320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Tavassoli M, Javadi S, Hadian M (2000) Canine linguatulosis in Urmia, West Azarbaidjan of Iran. In: Proceedings of the WSAVA/FECAVA Voorjaarsadgen congress, Amsterdam, The Netherlands, pp 528
  29. Tavassoli M, Tajic H, Dalir-Naghadeh B, Hariri F. Prevalence of Linguatula serrata nymphs and gross changes of infected mesenteric lymph nodes in sheep in Urmia. Iran Small Rumin Res. 2007;72:73–76. doi: 10.1016/j.smallrumres.2006.08.013. [DOI] [Google Scholar]
  30. Wahba AA, Shehab GJ, El-Refaii MAH. Some parasitological and pathological studies on two camel parasites, Dicrocoelium dendriticum (Rudolphi, 1819) and Linguatula serrata (Frohlich, 1789) in Egypt. Assiut Vet Med J. 1997;36:153–166. [Google Scholar]
  31. Yagi H, el Bahari S, Mohamed HA, el Ahmed RS, Mustafa B, Mahmoud M, Saad MB, Sulaiman SM, el Hassan AM. The Marrara syndrome a hypersensitivity reaction of the upper respiratory tract and buccopharyngeal mucosa to nymphs of Linguatula serrata. Acta Trop. 1996;62:127–134. doi: 10.1016/S0001-706X(96)00017-4. [DOI] [PubMed] [Google Scholar]
  32. Yao MH, Wu F, Tang LF. Human pentastomiasis in China: case report and literature review. J Parasitol. 2008;94:1295–1298. doi: 10.1645/GE-1597.1. [DOI] [PubMed] [Google Scholar]
  33. Yeganeh Moghadam A, Talari SA, Dehghani R. A case of human Linguatula serrata infestation in Kashan, Iran. J Kerman Univ Med Sci. 2001;8(3):175–178. [Google Scholar]

Articles from Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology are provided here courtesy of Springer

RESOURCES