One-Humped Camel (Camelus dromedarius) Infestation with Linguatula serrata in Tabriz, Iran.

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.

Introduction

Linguatula serrata Frohlich, 1789 is one of the most known members of Pentastomida, which infects both human and animals. 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 evolutionary affinities of this unusual group of organisms have continued to confound biologists because of morphological similarities to both annelids and arthropods, and suggestive phylogenetic relationships to Crustacea in the subclass Branchiura (Raff 1998). Because pentastomes appear to have a generally stronger affinity to arthropods some authors regard this group of organisms as a taxonomic class (Pentastomida) in the Phylum Arthropoda (Beaver et al. 1984, Ravindran et al. 2008). Currently some of authors regard pentastomida as a taxonomic sub-phylum in the phylum Tardigrada (Myers et al. 2008). Regardless of its true taxonomic position within the invertebrate realm, there is no mistaking this highly peculiar parasite when recovered from a parasitized host.

It is a worldwide and a zoonotic parasite (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 expelled with nasal secretions. The embryo develops 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 organs. 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 infection 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 nasopharyngeal 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 infection in different animals in Iran including small ruminants, dogs, cattle and camels (Shekarforoush 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 dromedarius) 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 cameleer or butcher information. The liver and lung samples were mostly taken from condemned and rejected part of organs.

In the laboratory, each lymph node was cut longitudinally in a Petri dish containing normal saline and examined under stereomicroscope, 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, 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 considered as significant.

Results

The prevalence of L. serrata nymphs in MLNs, livers and lungs of 140 camels slaughtered 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 infection rate increased with age (P= 0.009) (Table 1). No significant difference was observed between males and females (Table 1). The prevalence of L. serrata infection in different seasons has been showed in Table 2, no significant difference was found. The number 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 MLNsNo. (%)	camels with infected liversNo. (%)	camels with infected lungsNo. (%)
<4	Male	13	0 (0)	0 (0)	0 (0)
	Female	3	0 (0)	0 (0)	0 (0)
	Total	16	0 (0)	0 (0)	0 (0)
4–8	Male	15	2 (13.3)	0 (0)	0 (0)
	Female	21	1 (4.7)	0 (0)	0 (0)
	Total	36	3 (8.3)	0 (0)	0 (0)
>8	Male	29	4 (13.7)	1 (3.4)	1 (3.4)
	Female	59	12 (20.3)	1 (1.6)	1 (1.6)
	Total	88	16 (18.1)	2 (2.2)	2 (2.2)
Total	Male	57	6 (10.5)	1 (1.7)	1 (1.7)
	Female	83	13 (15.6)	1 (1.2)	1 (1.2)
	Total	140	19 (13.5)	2 (1.4)	2 (1.4)

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 MLNsNo. (%)	camels with infected liversNo. (%)	camels with infected lungsNo. (%)	Total infected camelsNo. (%)
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 Azerbaijan Province, north-west of Iran. The slaughtered camels were mostly from the same area. Previously, Oryan et al. (1993) reported L. serrata infection in 12.5% of examined camels in Shiraz, Iran. Shakerian et al. (2008) reported the infection rate of MLNs and livers of the camels slaughtered at a slaughterhouse in Najaf-Abad, central part of Iran, as 21% and 4.5% respectively and the maximum 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 central arid region of Iran with a different climate compare with East Azerbaijan province with cold winters and heavy snowfall and subfreezing temperatures during December 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 difference between prevalence rates of infection in different seasons of the year was observed.

The results of our study showed a significant correlation of age and infection rate of camels slaughtered in the Tabriz slaughterhouse and rural areas near to Tabriz that was compatible with other studies had been done on sheep and camel in Iran (Shekarforoush 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 difference 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 investigation (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.