Microsoft Word - 7- Dr_Hadadzadeh RTL.doc Iranian J Arthropod-Borne Dis, 2010, 4(1): 54–59 R Haddadzadeh et al.: One-Humped Camel (Camelus … 54 Original Article One-Humped Camel (Camelus dromedarius) Infestation with Linguatula serrata in Tabriz, Iran *HR Haddadzadeh1, SS Athari2, R Abedini3, S Khazraii nia4, P Khazraii nia5, S Nabian1, B Haji-Mohamadi6 1Department of Parasitology, Faculty of Veterinary Medicine, University of Tehran, Iran 2Faculty of Veterinary Medicine, University of Urmia, Iran 3Faculty of Veterinary Medicine, University of Tabriz, Iran 4Biology Section , Faculty of Veterinary Medicine, University of Tehran, Iran 5Department of Clinical Science, Faculty of Veterinary Medicine, University of Tehran, Iran 6Department of Food Hygiene, Faculty of Veterinary Medicine, University of Tehran, Iran (Received 14 Oct 2009; accepted 7 Apr 2010) Abstract Background: Linguatula serrata is one of well known members of Pentastomida which infects both human and animals. The aim of this study was to evaluate the prevalence of L. serrata in mesenteric lymph nodes, livers and lungs of camels slaughtered in Tabriz area, Iran. Methods: Mesenteric lymph nodes (MLNs), livers and lungs of 140 one-humped camels slaughtered in Tabriz, north-west of Iran were investigated for nymphs of L. serrata from July 2007 to June 2008. The organs were examined macroscopically and then a tissue digestion method was also done for investigation of liver and lung of the camels that had infected MLN. The liver and lung samples were mostly taken from condemned and rejected part of organs. Results: The infection rate of L. serrata nymphs in MLNs, livers and lungs was 13.5%, 1.4% and 1.4% respectively. The number of isolated nymph in infected lymph nodes varied from 2 to 18 with a mean of 4.78. Only one nymph was isolated from each infected livers and lungs. The infection rate increased with age (P< 0.05). No significant difference in different sex groups and seasons was observed (P> 0.05). Conclusion: Considering this fact that consumption of undercooked camel liver was not common in the studied area, the zoonotic importance of this infection should be concluded. Keywords: Linguatula serrata, Infection, One humped camel, Tabriz, Iran Introduction Linguatula serrata Frohlich, 1789 is one of the most known members of Pentas- tomida, which infects both human and ani- mals. The Phylum Pentastomida consists of about 100 identified species of linguatulids, all of which are endoparasites of the respiratory tract and other organs/body cavities of tetrapod vertebrates, particularly reptiles. The evolution- ary affinities of this unusual group of organ- isms have continued to confound biologists be- cause of morphological similarities to both an- nelids and arthropods, and suggestive phy- logenetic relationships to Crustacea in the sub- class Branchiura (Raff 1998). Because pen- tastomes appear to have a generally stronger affinity to arthropods some authors regard this group of organisms as a taxonomic class (Pen- tastomida) in the Phylum Arthropoda (Bea- ver et al. 1984, Ravindran et al. 2008). Cur- rently some of authors regard pentastomida *Corresponding author: Dr Hamid Reza Haddadzadeh, Email: hhadad@ut.ac.ir Iranian J Arthropod-Borne Dis, 2010, 4(1): 54–59 R Haddadzadeh et al.: One-Humped Camel (Camelus … 55 as a taxonomic sub-phylum in the phylum Tardigrada (Myers et al. 2008). Regardless of its true taxonomic position within the inver- tebrate realm, there is no mistaking this highly peculiar parasite when recovered from a pa- rasitized host. It is a worldwide and a zoonotic para- site (Jubb et al. 1985, Noble Elmer et al. 1989, Shekarforoush et al. 2004). The adult female of the parasite is tongue-shaped and has a length between 100–130 mm and its width is about 10 mm, whereas its male has a length of 20 mm and its width is 3-4 mm. Eggs size are about 70–90 µm (Noble Elmer et al. 1989, Kaufmann 1996). Embryonated eggs are laid in the nasal passages and frontal sinuses of mammals specially canids and ex- pelled with nasal secretions. The embryo de- velops in the egg in the presence of water or plant humidity. If the eggs are swallowed by a suitable intermediate host such as cattle, goat, sheep, rabbit, mouse or man, it will be hatched in alimentary canal; thus the larva penetrates the intestine wall and migrates to mesenteric lymph nodes (MLNs) or other or- gans. After some molting steps, lasting 5-6 months, it reaches to its nymph stage with a protective capsule. The larva may have a length of 500 µm and the nymph may be between 4-6 mm (Razavi et al. 2004). The nymph is infectious for the carnivores who consume the raw meat of infected herbivores intermediate hosts (Noble Elmer et al. 1989, Oryan et al. 2008). The adult stages develop inside nasal tract. L. serrata infection in dogs has been reported in different parts of Iran (Meshgi and Asgarian 2003, Razmaraii et al. 2007, Oryan et al. 2008). Linguatula serrata infection is more common in tropical and subtropical areas of the world (Razavi et al. 2004). Human infec- tion often occurs through nostrils, throat and sinuses (Yeganeh-Moghadam et al. 2001). This infection is accompanied with some special symptoms such as coughing, sneezing, irritated and sore throat, vomiting and headache. This condition is called Halzoun syndrome or naso- pharyngeal linguatolosis (Lazo et al. 1999, Yeganeh-Moghadam et al. 2001, Razmaraii et al. 2007). Although man is accidental host of the nymph, the reports of human infection to this parasite is not uncommon (Symmers and Valteris 1950, Papadakis and Hourmouziadis 1958, Lazo et al. 1999, Yeganeh-Moghadam et al. 2001, Anaraki-Mohammadi et al. 2008). There are many reports of L. serrata infec- tion in different animals in Iran including small ruminants, dogs, cattle and camels (Shekar- foroush and Arzani 2001, Meshgi and Asgarian 2003, Razavi et al. 2004, Shekarforoush et al. 2004, Tavassoli et al. 2007a, Tavassoli et al. 2007b, Razmaraii et al. 2007, Oryan et al. 2008, Haddadzadeh et al. 2009). The aim of this study was to evaluate the prevalence of L. serrata in MLNs, livers and lungs of camels slaughtered in Tabriz, Iran. Materials and Methods From July 2007 till June 2008, among slaughtered one-humped camels (Camelus dro- medarius) in the Tabriz slaughterhouse and rural areas near to Tabriz, East Azerbaijan province of Iran, MLN, liver and lung of 140 camels were sampled. The approximate age of camels was determined on the basis of ca- meleer or butcher information. The liver and lung samples were mostly taken from con- demned and rejected part of organs. In the laboratory, each lymph node was cut longitudinally in a Petri dish containing normal saline and examined under stereomicro- scope, recording the numbers of nymphs per lymph node. The examination of livers and lungs of the camels that had infected MLN were done in two steps. First, the 50-100g samples (with a mean of 60g) were sliced in small pieces and observed precisely under stereomicroscope to find the nymphs. In the second step, the minced tissues were put in 200 ml of digestion solution containing 5g pepsin enzyme (7178, Iranian J Arthropod-Borne Dis, 2010, 4(1): 54–59 R Haddadzadeh et al.: One-Humped Camel (Camelus … 56 Merck) and 25 ml hydrochloric acid (374, Merck) in 1 liter water, incubating at 37° C for 24 h. After that, the suspensions were transferred to petri dishes and examined for L. serrata nymph (Shakerian et al. 2008). The data were analyzed using chi- squared and Fisher’s exact tests (SPSS 11.5, Standard version, Copyright SPSS Inc., 1982– 2002). The P value less than 0.05 was con- sidered as significant. Results The prevalence of L. serrata nymphs in MLNs, livers and lungs of 140 camels sla- ughtered in the Tabriz slaughterhouse and rural areas near to Tabriz is shown in Table 1. The infection rate of MLNs, livers and lungs was 13.5%, 1.4% and 1.4% respectively. There was no infected camel in <4 yr group. The in- fection rate increased with age (P= 0.009) (Table 1). No significant difference was ob- served between males and females (Table 1). The prevalence of L. serrata infection in dif- ferent seasons has been showed in Table 2, no significant difference was found. The num- ber of isolated nymph in infected lymph nodes varied from 2 to 18 with a mean of 4.78 (Fig. 1). From the infected livers and lungs, only one nymph was isolated. The results showed a higher infection rate of MLNs compared with that of livers and lungs (P= 0.0005). Table 1. The prevalence of Linguatula serrata nymphs in MLNs, livers and lungs of 140 slaughtered camels in Tabriz Age (Year) Sex No. of Camels camels with infected MLNs No. (%) camels with infected livers No. (%) camels with infected lungs No. (%) Male 13 0(0) 0 (0) 0 (0) Female 3 0(0) 0 (0) 0 (0) <4 Total 16 0(0) 0 (0) 0 (0) Male 15 2(13.3 ) 0 (0) 0 (0) Female 21 1(4.7 ) 0 (0) 0 (0) 4-8 Total 36 3(8.3 ) 0 (0) 0 (0) Male 29 4(13.7) 1 (3.4) 1 (3.4) Female 59 12 (20.3) 1 (1.6) 1 (1.6) >8 Total 88 16 (18.1) 2 (2.2) 2 (2.2) Male 57 6(10.5) 1 (1.7) 1 (1.7) Female 83 13 (15.6) 1 (1.2) 1 (1.2) Total Total 140 19 (13.5) 2 (1.4) 2 (1.4) Iranian J Arthropod-Borne Dis, 2010, 4(1): 54–59 R Haddadzadeh et al.: One-Humped Camel (Camelus … 57 Table 2. The seasonal variance of Linguatula serrata prevalence in MLNs, livers and lungs of 140 slaughtered camels in Tabriz Season No. of Camels camels with infected MLNs No. (%) camels with infected livers No. (%) camels with infected lungs No. (%) Total infected camels No. (%) Spring 27 4(14.8) 0 (0) 0 (0) 4 (14.8) Summer 21 3(14.2) 1 (4.7) 1 (4.7) 5 (23.8) Autumn 39 6(15.3) 0 (0) 0 (0) 6 (15.38) Winter 53 6(11.3) 1 (1.8) 1 (1.8) 8 (15) Total 140 19 (13.5) 2 (1.4) 2 (1.4) 23 (16.4) Fig. 1. A Linguatula serrata nymph under stereomicroscope (×35) Discussion Without any specific clinical symptoms, L. serrata infection in ruminants leads to the reduction of animal products and hidden economic loss, as well as public health risks (Nematollahi et al. 2005). This study was done in East Azerbai- jan Province, north-west of Iran. The slaugh- tered camels were mostly from the same area. Previously, Oryan et al. (1993) reported L. serrata infection in 12.5% of examined cam- els in Shiraz, Iran. Shakerian et al. (2008) reported the infection rate of MLNs and livers of the camels slaughtered at a slaugh- terhouse in Najaf-Abad, central part of Iran, as 21% and 4.5% respectively and the maxi- mum and minimum numbers of parasites was reported as 30 and 1 in MLNs and 10 and 1 in livers. This rate of infection is about 2 times higher than our result. It should be mentioned that Najaf-abad is located in Isfahan plain in Iranian J Arthropod-Borne Dis, 2010, 4(1): 54–59 R Haddadzadeh et al.: One-Humped Camel (Camelus … 58 central arid region of Iran with a different climate compare with East Azerbaijan prov- ince with cold winters and heavy snowfall and subfreezing temperatures during Decem- ber and January. It seems that the difference in climate can be the cause of the different rate of infection. On the other hands, in our study because of economic limitations, the amount of liver and lung samples was too low (with a mean of 60g) and the samples were mostly taken from condemned and rejected parts of organs. In different studies have been done on seasonal variation of L. serrata infection in small ruminant of Iran, the results were not the same (Hamdast-joo 2001, Nematollahi et al. 2005). In our survey no significant differ- ence between prevalence rates of infection in different seasons of the year was observed. The results of our study showed a sig- nificant correlation of age and infection rate of camels slaughtered in the Tabriz slaugh- terhouse and rural areas near to Tabriz that was compatible with other studies had been done on sheep and camel in Iran (Shekar- foroush et al. 2004, Shakerian et al. 2008). In our study, no camel in the <4 yr group was infected. Also in our studies no significant dif- ference was observed in the infection rate in both males and females that were compatible with other study (Shakerian et al. 2008). Linguatula serrata, infests first MLNs, and then migrates to other organs such as the liver and lung (Shekarforoush et al. 2004, Razavi et al. 2004, Shakerian et al. 2008). In this study, the prevalence of L. serrata nymph in liver and lung were lower than MLNs, which is in accordance with the findings of other in- vestigation (Oryan et al. 1993, Shekarforoush et al. 2004, Tajik et al. 2006, Shakerian et al. 2008). Considering this facts that consumption of undercooked camel liver is common in the studied area, the zoonotic importance of this infection should be concluded. Acknowledgments We acknowledge financial support of Center of Excellence for Veterinary Research on Iranian Indigenous Domestic Animals, of University of Tehran. 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