J -Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

Case Report Nymphal Linguatulosis in Indian Crested (Histrix Indica) in Southwest of

*Mohammad Rajabloo 1, Seyed Mostafa Razavi 1, Hossein Shayegh 2, Amir Mootabi Alavi 1

1Department of Pathobiology, School of Veterinary Medicine, Shiraz University, Shiraz, Iran 2School of Veterinary Medicine, Shiraz University, Shiraz, Iran

(Received 7 Oct 2013; accepted 29 Mar 2014)

Abstract is one of the important zoonotic parasites. Carnivores serve as definitive host. The larvae ex- isted in mesenteric lymph nodes (MLNs), liver, lungs, etc of intermediate herbivores. The definitive host becomes infected by ingesting viscera containing the infective nymphal stage. Humans may be infected with Linguatula either by ingestion of nymphs resulting in a condition called nasopharyngeal linguatulosis or Halzoun syndrome or by in- gestion of infective eggs which develop in internal organs resulting in visceral linguatulosis. Indian crested porcu- pine ( indica) is a common in . Based on some tradition, consumption of Histrix meat and viscera is common in some parts of Iran. The present study reports the occurrence of Linguatula serrata nymph in H. indica as a new intermediate host from southwest of Iran.

Keywords: Nymphal linguatulosis, Linguatula serrate, Indian crested , Rodent host

Introduction

Linguatula serrata is one of the important fective eggs which develop in internal organs zoonotic parasites. Adults inhabit in respir- resulting in visceral linguatulosis (Shekar- atory system of canine (final hosts). Infective foroush et al. 2004). Halzoun syndrome may eggs containing larvae are discharged into the arise via consumption of raw or under- environment by nasopharyngeal secretions or cooked liver and lymph nodes. coughed up, swallowed, and passed out of The syndrome has been reported in many the host in the feces. When suitable inter- countries including Africa, South-East mediate host (herbivorous ), swallows and the Middle East (Beaver et al. 1984, these eggs, the larvae migrate to mesenteric Drabick 1987, El-Hassan et al. 1991). Some lymph nodes (MLNs), liver, lungs, etc. After researchers described clinical signs of the six to nine molting, the nymphs are infective syndrome including pharyngitis, salivation, for final host. Canine become infected by dysphagia and coughing. Visceral linguatulosis ingesting viscera containing the infective nym- generally remains asymptomatic (Khalil and phal stage. The parasite is tongue-shaped, light- Schacher 1965, Yagi et al. 1996). Clinical ly convex dorsally and flattened ventrally. signs associated with infections in interme- Males measure 1.8–2 cm, while females meas- diate hosts have not yet been described ure 8–13 cm in length (Soulsby 1982). carefully (Mehlhorn 2008). There are reports Humans may be infected with Linguatula of linguatulosis in other organs such as eye either by ingestion of nymphs resulting in a (Lazo et al. 1999). The prevalence of L. condition called nasopharyngeal linguatulosis serrata have been studied in various or Halzoun syndrome or by ingestion of in- in Iran, including dogs (Meshgi and Asgarian 131 *Corresponding author: Dr Mohammad Rajabloo, http://jad.tums.ac.ir E-mail: [email protected] Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

2003, Oryan et al. 2008, Rezaei et al. 2011), to allow nymphs to come out from tissue. sheep (Shekarforoush et al. 2004, Nourollahi The livers were sliced in 4–5 mm thick and Fard et al. 2011), goats (Razavi et al. 2004), observed carefully to find the encapsulated camels (Shakerian et al. 2008, Radfar et al. or free nymphs. The samples were examined 2010, Rajabloo et al. 2011, Oryan et al. 2011, for the presence of nymphs using a stere- Rezaei et al. 2012, Bamorovat et al. 2013) omicroscope. Recovered nymphs were fixed and cattle (Hami et al. 2009, Tajik et al. in ethanol 70%, slightly pressed between two 2011). There are also some reports of human flat glasses. They were stained with carmine linguatulosis in Iran (Sajjadi et al. 1998, and then mounted in Canada balsam® as Maleki 2001, Anaraki Mohammadi et al. permanent slides Measurements of morpho- 2008, Tabibian et al. 2012). logical features were made with a light mi- The Indian crested porcupine (Hystrix croscope using a calibrated ocular microm- indica) has been distributed in , Iran, eter. Samples (liver, MLNs, and mediastinal Palestine, Syria, , , southern lymphatic nodes) were studied separately. In and eastern states of the former Soviet Union the case of liver, no nymphal stage was and Indian subcontinent (Arsalan 2008). found. The results were also negative for Hystrix indica is nocturnal and spend day- mediastinal lymphatic nodes of both animals light hours in natural caves or excavated bur- but the MLNs were infected with 12 and 8 L. rows. Porcupines consumed storage organs serrata nymphs. Based on morphologic char- of at least twelve species of geophytes and acteristics, the parasite was identified as the hemicryptophytes and ate potatoes, peanuts, nymphal stage of L. serrata (Fig. 1). peppers, fallen fruit, and other agricultural The parasites were tongue-shaped, seg- crops (Alkon and Saltz 1988). mented and covered with several spines in The present study reports the occurrence linear arrangement. Total body length was of L. serrata nymph in H. indica from south- 52±3 mm, the body width was 1.2±1 mm in west of Iran. anterior and 0.25±0.02 mm in posterior ends. The hooklets surround elliptical mouth. Case Report

During a six month period, September 2012 to March 2013, the carcasses of two H. indica were transferred to Department of Pathobiology, School of Veterinary Medi- cine, Shiraz University, Shiraz, Iran. One of them was died in September 2012, when it was crossing the road in Bamu National Park Fig. 1. Nymphs of L. serrata recovered from (29° 40′ 20.52″ N, 52° 46′ 1.21″ E), Shiraz, mesenteric lymphatic nodes of H. indica, stained with Iran, and the other carcass was confiscated carmine (A×4, B×40) from unauthorized hunters. The animals were necropsized systematically. The body cavity Discussion was opened by a longitudinal incision from throat to vent. Mesenteric and mediastinal Canine are definitive hosts and the herbi- lymph nodes and liver were collected from vores such as sheep, goat, cattle and camel each animal, cut into small pieces and mas- act as intermediate host in life cycle of L. saged in tepid water and left for 30 minutes serrata. Cats (Esmaeilzadeh et al. 2008), fox 132 http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

(Gicik et al. 2009), dingo, Canis lupus dingo, Shiraz (Razavi et al. 2004) and in cattle, Chrysocyon brachyurus, Procyon cancrivorus 44% in Urmia and 0.25% in Tabriz (Hami et cancrivorus and wolf, Canis lupus lupus can al. 2009). It seems that the parasite is com- also be definitive hosts (Christoffersen and mon among herbivores and canine in Iran. De Assis 2013), L. serrata nymphs were found Halzoun syndrome was reported from Shiraz in European porcupine Hystrix (Hystrix) (Sajjadi et al. 1998), Tehran (Maleki 2001, cristata, degu, Octodon degus, common hare, Anaraki Mohammadi et al. 2008) and Isfahan Lepus (Eulagos) europaeus europaeus [as (Tabibian 2012). All of these reports showed Lepus europaeus] and common rabbit, the high rate of infection in both definitive Oryctolagus cuniculus cuniculus [as Lepus and intermediate hosts in various parts of cuniculus]. (Christoffersen and De Assis 2013). Iran and it is not unexpected to consider a It has been found commonly in cottontail canine-porcupine sylvatic cycle in this region. rabbits (Sylvilagus floridanus) in the USA The parasite has been reported from hu- (Moore and Moore 1947). Linguatula sp. is man beings in Iran (Sajjadi et al. 1998, maintained in Australia by a fox-rabbit cycle Maleki 2001, Anaraki Mohammadi et al. since foxes, not dogs, have been found in- 2008), Austria (Koehsler et al. 2011), Mo- fested (Pullar 1946). Our study revealed that rocco (Le Corroller and Pierre 1959) and H. indica can be regarded as another inter- Turkey (Yılmaz et al. 2011). These reports mediate host for this parasite and a sylvatic showed zoonotic importance of infection. cycle between porcupine and carnivores may Hystrix indica is a common rodent in Iran. exist in Fars Province. It fed from potatoes, peanuts, peppers, fallen The prevalence rate of nymphal stages fruit, and other agricultural crops and clas- was studied by many researchers in variety sified as an herbivore rodent (Alkon and of hosts. Shekarforoush et al. (2004) reported Saltz 1988, Arsalan 2008). Infection of MLNs a prevalence of 11.5% and 3% in the mes- suggests a similar migration and life cycle of enteric lymph nodes and liver of sheep, re- the parasite in this animal. With our knowledge spectively and Razavi et al. (2004) recorded there is no report about nymphal linguatulosis 29% infection in the mesenteric lymph in Indian crested porcupine species but it has nodes and 6% in the livers of goats in Shiraz been reported from lungs of European por- area, Fars Province, southern Iran. Preva- cupine Hystrix (Hystrix) cristata (Linnaeus lence rates of nymphal linguatulosis in one- 1758). humped camels were reported 12.9% in Yazd One part of the porcupine is always a (Oryan et al. 2011), 64% in Tehran (Rajabloo delicacy the liver, which is easily removed et al. 2011), 20.5% in Rafsanjan (Bamorovat by making a cut just under the neck into et al. 2013), 21.12% in Isfahan (Rezaei et al. which the hand is thrust, and the liver pulled 2012), 21.0%, 4.5% in MLNs and liver re- out. It may be fried with bacon, or baked spectively, in Najaf-Abad (Shakerian et al. slowly and carefully in the baker-pan with 2008). It has also been reported from two- slices of bacon (Kephart 2001). Many locals humped camel (Camelus bactrinus) in Ta- relish the porcupine's meat (Al Nees) as a briz, Iran (Haddadzadeh et al. 2009). The delicacy and for medicinal purposes. Per- Prevalence rates in sheep were 16.1% in haps this is responsible for the decline of H. Kerman (Razavi et al. 2004) and 11.5 % and indica population throughout (Amr et 3% in MLNs and liver, respectively, in al. 2014). Consumption of Histrix meat and Shiraz (Shekarforoush et al. 2004). In goat, viscera has been observed among native the prevalence rates were reported 29.9% people for medicinal purposes in south and and 6.4% in MLNs and liver, respectively in west of Iran (personal observation). 133 http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

Oryan et al. (2008) reported a prevalence Albert R, Petutsching B, Aubrecht G of 76.5% in stray dogs in Shiraz, southwest (eds) Reise durch die Natur Jordaniens. of Iran. The Prevalence of adult stage has Denisia 14. Linz: Biologiezentrum der also been reported 27.83% in North West Oberösterreichischen Landesmuseen, (Rezaei et al. 2011) and 62.2% in central pp. 437–464. part of Iran (Meshgi and Asgarian 2003). Arsalan A (2008) On the Indian crested por- Stray dogs and other wild canines can cupine, Histrix indica (Kerr 1792) in hunt porcupine and this animal can be a part Turkey (Mammalia: Rodentia). Pak J of their diets. Our study revealed that porcu- Biol Sci. 11(2): 315–317. pine can act as an intermediate host for syl- Bamorovat M, Borhani Zarandi M, Mostafavi vatic cycle of the parasite in this area. These M, Kheirandish R, Sharifi I, Radfar facts showed that the sylvatic cycle could MH (2013) The prevalence of Linguatula support the distribution of L. serrata. Further serrata nymphs in mesenteric and investigations are needed to be carried out to mediastinal lymph nodes in one- clarify the exact role of canine and other humped camels (Camelus dromedarius) wild in the life cycle of L. serrate. slaughtered in Rafsanjan slaughter- house, Iran. J Parasit Dis. DOI 10.1007/ s12639-013-0258-9. Conclusion Beaver PC, Jung ROC, Cup EW (1984) Crustacea, linguatulid, millipeds, centi- In conclusion, our results and high prev- peds, scorpions, spiders, ticks and mites. alence of linguatulosis in both definitive and In: Beaver, PC, Jung, ROC, Cup, EW intermediate host in Fars Province showed (Eds), Clinical Parasitology. 9th ed. Lea that sylvatic cycle should be considered as a and Febiger, Philadelphia, pp. 572–573. risk factor for human beings and other hosts. Christoffersen ML, De Assis JE (2013) A systematic monograph of the Recent Acknowledgements , with a compilation of their hosts. Zool Med Leiden. 87(1): The authors declare that there is no con- 1–206. flict of interests. Drabick JJ (1987) Pentastomiasis. Rev Infect Dis. 9: 1087–1094. El-Hassan AM, Eltoum IA, El-Asha BMA References (1991) The Marara syndrome: Isola- tion of Linguatula serrata nymph from Alkon PU, Saltz D (1988) Foraging time and a patient and the viscera of goats. the northern range limits of Indian crest- Trans R Soc Trop Med Hyg. 85: 309. ed porcupines (Hystrix indica, Kerr). J Esmaeilzadeh S, Mohammadian B, Rezaei A Biogeog. 15(3): 403–408. (2008) Linguatula serrata nymph in a Anaraki Mohammadi G, Mobedi I, Ariaiepour cat. Iranian J Vet Res. 9(4): 387–389. M, Pourmohammadi Z, Zare Bidaki M Gicik Y, Kara M, Sari B, Kilic K, Arslan M (2008) A case report of nasopharyngeal (2009) Intestinal parasites of red foxes Linguatuliasis in Tehran, Iran and char- (Vulpes vulpes) and their zoonotic im- acterization of the isolated Linguatula portance for human in Kars Province. serrata. Iran J Parasitol. 3(1): 53–55. Kafkas Univ Vet Fak Derg. 15: 135–140. Amr Z, Abu Baker M, Rifai L (2004) Haddadzadeh H, Athari SS, Hajimohammadi of Jordan. In: Waitzbauer W, B (2009) The first record of Linguatula 134 http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

serrata infection of Two-Humped camel southeast Iran. Trop Anim Health Prod. (Camelus bactrinus) in Iran. Iran J Pa- 43: 1–3. rasitol. 4: 59–61. Oryan A, Khordadmehr M, Ranjbar VR (2011) Hami H, Naddaf SR, Mobedi I, Zare-Bidaki Prevalence, biology, pathology, and pub- M, Athari SS, Hajimohammadi B, lic health importance of linguatulosis Anaraki-Mohammadi G (2009) Prev- of camel in Iran. Trop Anim Health alence of Linguatula serrata infection Prod. 43(6): 1225–1231. in domestic bovids slaughtered in Ta- Oryan A, Sadjjadi SM, Mehrabani D, Rezaei briz abattoir, Iran. Iran J Parasitol. 4(3): M (2008) The status of Linguatula 25–31. serrata infection of stray dogs in Shi- Kephart H (2001) Camp Cookery. Applewood raz, Iran. Comp Clin Path. 17: 55–60. Books, London. Pullar EM (1946) A survey of Victorian canine Khalil GM, Schacher JF (1965) Linguatula and vulpine parasites. V Athropoda serrata in relation to Halzoun and the Aust Vet J. 22: 112–118. Marrara syndrome. Am J Trop Med Radfar MH, Fathi S, Asgary Nezhad H, Hyg. 15: 736–746. Norouzi Asl E (2010) Prevalence of Lazo RF, Hidalgo Lazo EJE, Bermeo A, Linguatula serrata nymphs in one- Llanguno M, Murillo J, Teixeira VPA humped camel (Camelus dromedarius) (1999) Ocular linguatuliasis in Ecua- in southeast of Iran. Sci Parasitol. dor: case report and morphometric 11(4): 199–202. study of the larvae of Linguatula serrata. Rajabloo M, Youssefi MR, Majidi Rad M, Am J Trop Hyg. 60(3): 405–409. Kordafshari S, Fallah Omrani V, Le Corroller Y, Pierre JL (1959) On a case of Nazaralipour Sumali GR, Darvishi human linguatulosis in Morocco. Bull MM, Gerami Sadeghian A (2011) Soc Pathol Exot Filiales.52: 730–733. Prevalence of linguatula serrate Maleki F (2001) A case report of linguatula Nymphs in One-humped camel (Cam- serrata in human throat from Tehran, els dromedarus) in Tehran, Iran. central Iran. Ind J Med Sci. 55(8): Global Veterinaria. 6(5): 438–440. 439–441. Razavi SM, Shekarforoush SS, Izadi M (2004) Mehlhorn H (ed) (2008) Encyclopedia of Prevalence of Linguatula serrata nymph Parasitology. 3rd ed. Springer Publish- in goats in Shiraz, Iran. Small Rumin ing Co, New York. Res. 54: 213–217. Meshgi B, Asgarian O (2003) Prevalence of Rezaei F, Tavassoli M, Javdani M (2012) Linguatula serrata in Stray Prevalence and morphological charac- Dogs of Shahrekord, Iran. J Vet Med terizations of Linguatula serrata nymphs B Infect Dis Vet Public Health. 50: in camels in Isfahan Province, Iran. 466–467. Vet Res Forum. 3(1): 61–65. Moore ER, Moore GC (1947) The helminth Rezaei F, Tavassoli M, Mahmoudian A (2011) parasites of cottontail rabbits in Alabama, Prevalence of Linguatula serrata in- with notes on the arthropod Linguatula fection among dogs (definitive host) serrata. J . 28: 279–284. and domestic ruminants (intermediate Nourollahi Fard SR, Kheirandish R, Norouzi host) in the North West of Iran. Vet Asl E, Fathi S (2011) Mesenteric and Med (Praha). 56(11): 561–567. mediastinal lymph node infection with Sajjadi SM, Ardehali SM, Shojaei A (1998) Linguatula serrata nymphs in sheep A case report of Linguatula serrata in slaughtered in Kerman slaughterhouse, human pharynx from Shiraz, southern 135 http://jad.tums.ac.ir Published Online: July 16, 2014 J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in …

Iran. Med J Islam Repub Iran. 12: 193– Tajik H, Tavassoli M, Dalirnaghadeh B, 194. Danehloipour M (2011) Mesentric lymph Shakerian A, Shekarforoush SS, Ghafari Rad nodes infection with Linguatula serrata H (2008) Prevalence of Linguatula nymphs in cattle. Iran J Vet Res. 7(4): serrata nymphs in one-humped camel 82–85. (Camelus dromedarius) in Najaf-Abad, Yagi H, El-Bahari S, Mohamed HA, Sid- Iran. Res Vet Sci. 84: 243–245. Ahmed R, Mus-tafa B, Mahmoud M, Shekarforoush SS, Razavi SM, Izadi M (2004) Saad MBA, Ulaiman SM, Hassan AM Prevalence of Linguatula serrata nymph (1996) The Marrara syndrome: a hy- in sheep in Shiraz, Iran. Small Rumin persensitivity reaction of the upper res- Res. 52: 99–101. piratory tract and buccopharyngeal mu- Soulsby EJL (1982) Helminths cosa to nymphs of Linguatula serrata. and Protozoa of Domesticated Ani- Acta Trop. 62: 127–134. mals. 7th ed. Bailliere Tindall, London. Yılmaz H, Taş Cengiz Z, Çiçek M, Dülger Tabibian H, Yousefi Darani H,Bahadoran- AC (2011) A nasopharyngeal human Bagh-Badotani M, Farahmand Soderjani infestation caused by Linguatula serrata M, Enayatinia H (2012) A case report nymphs in Van Province: A Case Re- of Linguatula serrata infestation from port. Turkiye Parazitol Derg. 35: 47– rural area of Isfahan City, Iran. Adv 49. Biomed Res. 1: 42.

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