Parasitol Res DOI 10.1007/s00436-016-5074-6 ORIGINAL PAPER Prevalence and morphopathological characteristics of linguatulosis in one-humped camel (Camelus dromedarius) in Yazd, Iran G. Farjanikish1 & H. Shokrani 2 Received: 25 January 2016 /Accepted: 14 April 2016 # Springer-Verlag Berlin Heidelberg 2016 Abstract Linguatula serrata is a cosmopolitan zoonotic par- Keywords Linguatula serrata . Camel . Lymph nodes . asite. Its adult form inhabit the nasal and respiratory passages Liver . Yazd of canids as the definitive hosts while its immature stages localize in the mesenteric lymph nodes or in other organs of herbivorous intermediate hosts. We examined the liver, mes- Introduction enteric, and mediastinal lymph nodes of 272 camels slaughtered at the slaughterhouse of Yazd, Iran. Forty-one Linguatula (Porocephalida: Linguatulidae) is a worm-like en- out of 272 camels (15.1 %) were infected with nymphs of L. doparasite, belonging to a small phylum of parasites serrata. Twenty-four out of 166 males (14.45 %) and 17 out of Pentastomida which are commonly classified between anne- 106 females (16 %) were positive. The livers of five camels, lids and arthropods (Mehlhorn 2008). Linguatula serrata, which also had nymphs in their lymph nodes, were infected commonly known as tongue worm, inhabits the canine respi- with the larval stage of this parasite. The infection rate in- ratory system as final hosts (Berger and Marr 2006). If the creased with age and was highly significant, while sex did discharged eggs are swallowed by a suitable intermediate host not play a significant role in the prevalence of this parasitic (e.g., cattle, sheep, goat, camel, or buffalo), they will be infection. The infected lymph nodes were grossly enlarged, hatched in the alimentary canal, the larva penetrates the intes- edematous, and consisted of hemorrhagic and necrotic lesions. tine wall and migrates to mesenteric and mediastinal lymph Histopathologically, the architecture of the infected lymph nodes or other organs (Razavi et al. 2004). If the viscera of nodes was degraded, necrotic, and sectioned migrating stages infected herbivores are eaten by a definitive host, the larvae of L. serrata were clearly visible. In some lymph nodes, par- migrate to the respiratory tract and mature into adults. There asitic granulomatous lymphadenitis with necrosis and in some are many reports of L. serrata infection in different animals in cases, degenerated parasite in central area was observed. High Iran including small ruminants and camels (Shekarforoush prevalence of infection in camels suggests possibility of sim- et al. 2004; Tajik et al. 2007; Haddadzadeh et al. 2009; ilar high rate of infection in other animals of this region. In Oryan et al. 2011). Although adult parasites usually cause view of the consumption of raw or undercooked visceral or- catarrhal inflammation of the canine respiratory tract, larval gans of camel by humans of this region, the importance of or nymphal infection is usually asymptomatic in herbivores. careful inspection at slaughterhouse needs to be emphasized. Humans can be occasionally infected with both adult and nymphal stages of parasite. Infection often occurs after con- sumption of the raw or undercooked visceral tissues, known * G. Farjanikish as nasopharyngeal linguatulosis or Halzoun syndrome, or [email protected] rarely by accidental ingestion of infective eggs causing viscer- al linguatulosis. Pharyngitis, dysphagia, breathing blockage, 1 Department of Pathology, Faculty of Veterinary Medicine, Lorestan vomiting, coughing, and sneezing are some clinical signs of University, Khorram Abad, Iran the nasopharyngeal infection in humans (Mehlhorn 2008; 2 Department of Parasitology, Faculty of Veterinary Medicine, John and Petri 2006). Although L. serrata infection is cosmo- Lorestan University, Khorram Abad, Iran politan, it is mainly seen in tropical and subtropical areas. Parasitol Res Human cases have been reported from Iran, Africa, Southeast used for comparison of the prevalence of linguatulosis among Asia, and the Middle East (Beaver et al. 1984;Drabick,1987; male and female camels and different age groups. P values of El-Hassan et al. 1991; Anaraki Mohammadi et al. 2008; equal or less than 0.05 were considered statistically Tabibian et al. 2012). significant. One-humped camel (Camelus dromedarius)isanimpor- tant multipurpose popular local animal of Iran and more than 200,000 dromedary camels live in the arid and semiarid de- serts of eastern provinces of the country. Today, camel raisers Results try to submit the animals basically for the purpose of meat consumption. In some areas of Iran, people are used to con- Results of macroscopical investigation revealed the presence sume camel meat, which has good quality and is economically of L. serrata in 15.1 % (41/272) of the examined camels. The fair in comparison to beef and sheep (Mowlavi et al. 1997; infection rate increased with the age of animals (P < 0.01). Rahbari and Bazargani, 1995). Despite the general reputation L. serrata infection was found to occur more frequently in of hardiness and resilience, camels are, however, vulnerable to females (16 %), though not significant (Table 1). many infections including parasites (Bukachi et al. 2003; The lymph nodes of 41 camels (15.1 %) were infected with Wernery et al. 2004; Mohammed et al. 2007). Considering nymphs of L. serrata. The infection rate of mediastinal lymph the importance of this infection for the human health and nodes and livers was significantly lower than that of mesen- albeit eating undercooked meat in Iran, few studies have been teric lymph nodes. Mediastinal lymph nodes of six camels done to investigate the epidemiology of this parasite. (2.2 %) were infected with the larval stage of this parasite. Consumption of raw or undercooked meat is not unusual in Two camels had nymphs in their mediastinal lymph nodes, Iran; therefore, it is absolutely necessary to pay attention to the while no nymph were observed in their mesenteric lymph prevention of this disease and also decrease the infection rate nodes. Thirty-nine camels (14 %) had nymphs in their mesen- of intermediate host and domestic animals. The aim of this teric lymph nodes. The livers of five camels, which also had study was to determine the infection rate and nymphs in their mesenteric and mediastinal lymph nodes, morphopathological characteristics of linguatulosis in livers, were infected with the larval stage of the parasite. The num- mesenteric, and mediastinal lymph nodes of camels bers of L. serrata larvae localized in each infected mesenteric slaughtered at the slaughterhouse of Yazd, Iran. lymph node varied, ranging from one to nineteen parasites, while one to three and one to two larvae was localized in mediastinal lymph nodes and livers, respectively. Materials and methods Gross appearance of mesenteric lymph nodes consisted of hemorrhagic and necrotic lesions. The infected mesenteric and Lymph node and liver samples were collected randomly from mediastinal lymph nodes were grossly enlarged, and their slaughterhouse of Yazd between January and December 2014. cross-sectional areas were edematous, swollen, firm, granulat- Slaughtered camels were categorized in three age groups ed, and dark reddish in color. In some cases, histopathology (<5 years old, 5–10 years old and >10 years old). Their age revealed typical migration lesions, traumatic foci severe hem- was determined on the basis of cameleer information and orrhages, and necrosis (Fig. 1). Cell population of lymph using the eruption of permanent incisor teeth criteria as al- nodes decreased. Also infiltration of inflammatory cells in- ready described (Currasson 1947; Manefield and Tinson, cluding macrophages and eosinophils was observed (Fig. 2). 2000). Totally, 272 slaughtered camels (166 males and 106 In some of these lesions, sectioned migrating stages of L. females) were examined to identify the infection rate and serrata were clearly visible with fibrous connective tissue morphopathological characteristics of L. serrata nymphs. walls around the parasites (Fig. 3). In some lymph node, par- Tissue samples were separately collected from three mesen- asitic granulomatous lymphadenitis with necrosis or in some teric lymph nodes, a mediastinal lymph node and whitish pin- cases, degenerated parasite in central area and around these point spots on the liver. lesions fibrosis connective tissue was observed. Peripheral cell Morphologic appearance of lymph nodes were eval- structure of these granulomatous lesions contained multinu- uated initially, then appropriate samples were prepared cleated giant cells, macrophages, and eosinophils. In some of in 10 % buffered formalin, dehydrated in graded etha- these cases, the parasite in the necrotic area was degenerated, nol, cleared in xylene, and embedded in paraffin wax. and calcification covered some parts of the degraded parasite Histological sections (sections in 5 μmthickness)were and necrotic tissue (Fig. 4). The Linguatula nymphs in the stained routinely with hematoxylin–eosin stain (H&E) livers were encapsulated in a thick wall of fibrous connective and studied microscopically. tissue, and the mononuclear inflammatory cells lymphocytes; The statistical analysis was performed using SPSS software plasma cells, and macrophages were infiltrated in the connec- version 16 (SPSS, Inc, Chicago, IL). The chi-square test was tive tissue wall..