Nymphal Linguatulosis in Indian Crested Porcupines (Histrix Indica) in Southwest of Iran
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J Arthropod-Borne Dis, June 2015, 9(1): 131–136 M Rajabloo et al.: Nymphal Linguatulosis in … Case Report Nymphal Linguatulosis in Indian Crested Porcupines (Histrix Indica) in Southwest of Iran *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 Linguatula serrata 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 (Hystrix indica) is a common rodent in Middle East. 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 porcupine, 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 Asia mediate host (herbivorous animal), 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 animals 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 Iraq, Iran, eter. Samples (liver, MLNs, and mediastinal Palestine, Syria, Lebanon, Turkey, 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.