# Frequency of *Taenia hydatigena* cysts in slaughtered sheep in Sulaymaniyah province/Iraq

A. A. MOHAMMED<fnref n="1" />*, M. A. KADIR<fnref n="2" />

## SUMMARY

Taenia hydatigena is a common economically important parasite in Iraq. Its larval stage is called Cysticercus tenuicollis. This study aimed to investigate the effects of host sex, age and breed on the frequency rate of T. hydatigena cysts in sheep. The survey conducted from January 2017 to December 2017 and inspection performed from 19,897 sheep slaughtered at Modern Sulaimani Slaughterhouse of Sulaymaniyah province. C. tenuicollis was found in 4,495 (22.6%) sheep and the highest rate of infection was found in omentum (37%). April recorded the highest rate of infection (26.1%) and there were significant differences between months of year. Ages and sexes had not significant effect on the rate of infection, but significant difference was found in imported sheep including Awassi breed in Syria, Turkey and Iran (23.7%) compared to local one involving Karadi and Hamdani breeds (19.6%). It was concluded that the high frequency of this metacestode infestation might reveal the endemicity of the disease in the study area and this may constitute economic and health problems in the meat industry. It is recommended to the veterinary authority to apply a suitable preventive and control measures to get over this issue.

**Keywords:** cyst; frequency; sheep; slaughterhouse; survey

## RÉSUMÉ

### Fréquence des kystes de Taenia hydatigena chez les ovins abattus dans la province de Sulaymaniyah/Iraq

Taenia hydatigena est un parasite courant et économiquement important en Irak. Son stade larvaire est appelé Cysticercus tenuicollis. Cette étude avait pour but d'étudier les effets du sexe, de l'âge et de la race de l'hôte sur le taux de fréquence de kystes de T. hydatigena chez les moutons. L'enquête menée de janvier 2017 à décembre 2017 a portésur de 19 897 moutons abattus au Modern Abattoir Sulaimani de la province de Sulaymaniyah. C. tenuicollis était trouvé chez 4 495 moutons (22,6 %) et le taux d'infection le plus élevé a été trouvé dans l' omentum (37 %). Le mois d'avril a enregistré le taux d'infection le plus élevé (26,1 %) et il y eu des différences significatives entre les mois de l'année. Âges et sexes n'ont pas eu d'effet significatif sur le taux d'infection. Une différence significative a été trouvée chez des moutons importés de race Awassi, de en Syrie, Turquie et Iran (23,7 %) par rapport aux races locales Karadi et Hamdani (19.6%). Il a été conclu que la fréquence élevée de ce métacestode pourrait révéler l'endémicité de la maladie dans la zone d'étude.

**Mots-clés :** kyste ; fréquence ; mouton ; abattoir ; Iraq

## Introduction

Taenia hydatigena is a universal and boundless parasite of canids that can taint an extensive variety of warm blooded animals with its larval stage which is generally alluded to as C. tenuicollis [14]. Cysticerci are typically found on the omentum, mesentery, peritoneum, and less regularly, on the pleura and pericardium. The migrating larvae can be discovered for the most part in the liver parenchyma inside 7-10 days and may cause hepatitis cysticercosa in youthful animals [4]. Most diseases are perpetual and asymptomatic and are not generally distinguished until slaughter [6]. In overwhelming contaminations, the migrating larvae could create serious annihilation of the liver parenchyma with eosinophilic invasion and extreme irritation that could be lethal [15]. Notwithstanding constituting an animal wellness issue, the parasitosis is a wellspring of financial misfortune for the meat business [14].

In recent years, it is becoming increasingly clear that greater priority should be given to C. tenuicollis because of its economic impact due to condemnation of offal's containing these larvae, particularly in resource poor countries [20]. Loss in quantity or quality of meat or offal will have

financial implications, with reduced payment for carcass contamination or diseases or infected tissues.

Diagnosis of ovine cysticercosis in animals depends on the finding the gross cysts during meat examination or necropsy technique, while different strategies, for example, serological, biochemical and hematological tests can be valuable for diagnosis of live animals [3].

There are many risk factors associated with developing of Cysticercus tenuicollis infection in the study area. Enormous animal industry is managed mainly by villagers with poor management and in combination with existing a large number of stray dogs make a risk of spreading the disease. In addition, street slaughtering of animals with improper disposal of offal accelerates the dissemination of the disease [9, 19]. According to Kouam et al. [11], research directed towards the risk factors that lead to development of a given disease or pathogen are of the utmost importance, since this has the aims of helping to formulate control strategies. Therefore, the purpose of current study was to document the frequency of *T. hydatigena* cysts according to sexes, ages, and breeds in slaughtered sheep of Sulaymaniyah province /Iraq.

<footnote n="1">¹Department of Microbiology, College of Veterinary Medicine, Sulaimani University, 00964 New Sulaimani, Street 11, Zone 207, Sulaymaniyah City, Kurdistan Region, Iraq.</footnote>

<footnote n="2">²Department of Microbiology, College of Medicine, Kirkuk University, Kirkuk City, Iraq</footnote>

<footnote>*Corresponding Author: aram.mohammed@univsul.edu.iq</footnote>
# Materials and Methods

## STUDY AREA

The survey was done in Sulaymaniyah province, Kurdistan Region, north-east of Iraq. Its lies between (35° 04 sec.) and (36° 30 sec.) latitude and (44° 50 sec.) and (46° 16 sec.) longitude. The altitude of Sulaymaniyah province is 400 m above sea-level, and 2,500 m in the northern and north-eastern of the province. So in general, as long as we go north and north-east wards, its ground becomes higher. The maximum absolute temperature is 46 °C recorded in summer, while the minimum temperature is -5 °C recorded in winter. Rainfall occurs only in the cold half of the year, which is from October up to May.

Sheep population in Sulaymaniyah province is approximately 1.2 million according to survey done by General Directorate of Veterinary in Sulaymaniyah city. The survey was conducted from the beginning of January 2017 to the end of December 2017 by collecting data on events associated with *C. tenuicollis* in sheep slaughtered at Modern Sulaimani slaughterhouse. The inspection was carried out during four seasons and the data was collected by regularly visiting the slaughterhouse once per week.

## PRE AND POST MORTEM EXAMINATION

A total of 19,897 sheep were selected and identified by origin, sex and age during ante mortem inspection in the lairage of Sulaimani slaughterhouse from January 2017 to the end of December 2017. Identification number was given for each animal to examine after evisceration. The examined sheep were 16,697 males and 3,200 females and originated from local and imported breeds. Most of the sheep were originated from neighboring countries especially Syria, Iran and Turkey. Out of 19,897 sheep inspected 5,466 (27.5%) and 14,431 (72.5%) were local (Karadi and Hamdani) and imported (Awassi) breeds, respectively. The origin of sheep was determined from the questioning of the animal owners

or slaughterhouse personnel as described by Sissay et al. [18], and identified based on brands and ear clippings [5]. A total of 6,533 young sheep and 13,364 adult sheep were examined in the study. The age grouping was based on eruption patterns and seasons. Sheep with no erupted permanent incisor teeth were classified as young, while those with one pair or more permanent incisors' teeth were classified as adults [16].

During postmortem examination visceral organs and tissues in abdominal, thoracic and pelvic cavities were inspected for the presence of *C. tenuicollis* by applying the routine meat inspection procedures [7]. The number and location of cysts were recorded. *C. tenuicollis* cysts were initially identified according to their feature such as a long-necked single scolex, virtually translucent cyst fluid and rostellar hook morphology [12].

## STATISTICAL ANALYSIS

The frequency of *C. tenuicollis* is presented as the percentage of infected sheep. The variation between infection rates of specific organs, age, sexes, and breeds of animals were evaluated by Chi-square (X²) test using MS Excel (2010). The sizes of cysts were expressed as mean ± standard deviation (SD). Values of P < 0.05 were considered statistically significant.

## Results

The percentage of slaughtered sheep infected with *C. tenuicollis* in the Modern Sulaimani Slaughterhouse was shown in (Table I), the result showed that (4,495) sheep were infected out of a total of (19,897) examined and the percentage of infection was (22.6%).

The highest percentage of infection was found in April (26.1%), while the lowest percentages were seen in August and September 19% and 19.5%, respectively, as shown in (Table I), there were significant differences between months of the year (P < 0.05).

<table><thead><tr><th>Month (2017)</th><th>No. examined</th><th>No. infected</th><th>(%) of infection</th></tr></thead><tbody><tr><td>January</td><td>1,657</td><td>390</td><td>23.5</td></tr><tr><td>February</td><td>1,667</td><td>397</td><td>23.8</td></tr><tr><td>March</td><td>1,637</td><td>364</td><td>22.2</td></tr><tr><td>April</td><td>1,690</td><td>441</td><td>26.0</td></tr><tr><td>May</td><td>1,635</td><td>395</td><td>24.1</td></tr><tr><td>June</td><td>1,706</td><td>375</td><td>21.9</td></tr><tr><td>July</td><td>1,640</td><td>353</td><td>21.5</td></tr><tr><td>August</td><td>1,720</td><td>327</td><td>19.0</td></tr><tr><td>September</td><td>1,595</td><td>310</td><td>19.4</td></tr><tr><td>October</td><td>1,571</td><td>338</td><td>21.5</td></tr><tr><td>November</td><td>1,700</td><td>415</td><td>24.1</td></tr><tr><td>December</td><td>1,679</td><td>390</td><td>23.2</td></tr><tr><td>Total</td><td>19,897</td><td>4,495</td><td>22.5</td></tr></tbody></table>

P-value of X² = 0.003

P < 0.05

<caption>TABLE I: Frequency of *C. tenuicollis* in slaughtered sheep according to month</caption>
There were no significant differences between animal sexes and ages (P > 0.05). Both males and females showed relatively the same rate of infection, 22.7% and 21.8% respectively. The rate of infection in young (aged less than 1 year) and adult (aged above 1 year) sheep were 21.8% and 22.9% respectively. Local breeds recorded the least rate of infection (19.6%), which was significantly (P < 0.05) less than imported sheep (23.7%), as shown in (Table II).

C. tenuicollis was found in different body organs (omentum, mesentery, liver, diaphragm, gall bladder,

urinary bladder, uterus and kidneys). The more prominent predilection site was recorded in omentum, and mesentery, while uterus and kidney had the lowest rate of infection as shown in (Table III; Figure 1). The numbers and sizes of cysts in infected organs were shown in (Table IV). The highest numbers of cysts were found in uterus (15) and liver (11), while the least numbers (5) were seen in kidneys, urinary bladder, and gall bladder. It was found that the average size of the examined cysts were 5 ± 1.3 and 4.1 ± 1.9 in mesentery and omentum, respectively, while it recorded the smallest size in kidney with average of 2.3 ± 0.3.

<table><thead><tr><th>Sex</th><th>No. examined</th><th>No. (%) of infection</th><th>P-value of X<sup>2</sup></th></tr></thead><tbody><tr><td>Male</td><td>16,697</td><td>3,797 (22.7)</td><td></td></tr><tr><td>Female</td><td>3,200</td><td>698 (21.8)</td><td>0.359</td></tr><tr><td>Total</td><td>19,897</td><td>4,495 (22.5)</td><td></td></tr><tr><th colspan="4">Age</th></tr><tr><td>Young (&lt; 1year)</td><td>6,533</td><td>1,427 (21.8)</td><td></td></tr><tr><td>Adult (&gt; 1year)</td><td>13,364</td><td>3,068 (22.9)</td><td>0.161</td></tr><tr><td>Total</td><td>19,897</td><td>4,495 (22.5)</td><td></td></tr><tr><th colspan="4">Breed</th></tr><tr><td>Indigenous breed</td><td>5,466</td><td>1,075 (19.6)</td><td></td></tr><tr><td>Imported breed</td><td>14,431</td><td>3,420 (23.6)</td><td>*1.17E-06</td></tr><tr><td>Total</td><td>19,897</td><td>4,495 (22.5)</td><td></td></tr></tbody></table>

<table><caption>TABLE II: Frequency of C. tenuicollis in slaughtered sheep in relationship to sex, age and breed</caption><thead><tr><th>Organ</th><th>No. of infected organ</th><th>(%) of infected organ</th></tr></thead><tbody><tr><td>Omentum</td><td>1,662</td><td>36.9</td></tr><tr><td>Mesentery</td><td>1,534</td><td>34.1</td></tr><tr><td>Liver</td><td>844</td><td>18.7</td></tr><tr><td>Diaphragm</td><td>303</td><td>6.7</td></tr><tr><td>Gall bladder</td><td>76</td><td>1.6</td></tr><tr><td>Urinary bladder</td><td>40</td><td>0.8</td></tr><tr><td>Uterus</td><td>25</td><td>0.5</td></tr><tr><td>Kidney</td><td>11</td><td>0.2</td></tr></tbody></table>

<table><caption>Table III: Frequency of C. tenuicollis in slaughtered sheep in relationship to infected organ</caption><thead><tr><th>Organ<br>(n = 5)</th><th>Total no. of cysts</th><th>Average</th><th>Size of cyst in cm (mean ± SD)<br>Shortest - longest</th></tr></thead><tbody><tr><td>Omentum</td><td>8</td><td>1.6</td><td>4.1 ± 1.9<br>1.9 - 6.2</td></tr><tr><td>Mesentery</td><td>8</td><td>1.6</td><td>5 ± 1.3<br>2.9 - 7</td></tr><tr><td>Liver</td><td>11</td><td>2.2</td><td>3.4 ± 0.8<br>1.9 - 4.9</td></tr><tr><td>Diaphragm</td><td>6</td><td>1.2</td><td>3.5 ± 0.6<br>2.8 - 4.5</td></tr><tr><td>Gall bladder</td><td>5</td><td>1</td><td>3.4 ± 0.5<br>2.8 - 4.1</td></tr><tr><td>Urinary bladder</td><td>5</td><td>1</td><td>3.4 ± 0.4<br>2.9 - 4.1</td></tr><tr><td>Uterus</td><td>15</td><td>3</td><td>3.0 ± 1.9<br>1.0 - 7.7</td></tr><tr><td>Kidney</td><td>5</td><td>1</td><td>2.3 ± 0.3<br>1.8 - 2.7</td></tr></tbody></table>

<caption>Table IV: Numbers and sizes of C. tenuicollis per organ in slaughtered sheep</caption>

<footnote>*P < 0.05</footnote>
<figure><img src="image_1.png" /><figcaption>FIGURE 1: *C. tenuicollis* suspended in the omentum (A), mesentery (B), liver(C), diaphragm (D), gall bladder (E), urinary bladder (F), uterus (G) and kidney (H) of infected sheep</figcaption></figure>

Discussion

In this study the overall rate of *C. tenuicollis* infection in sheep slaughtered at Modern Sulamani abattoir in Sulaymaniyah province was 22.6%. This result was higher than that recorded by each of Ghaffar [8] in Duhok province (0.7%) and Al-Bakri [1] in Mosul province (2%) of Iraq. In contrast, the result of the present study was much lower than registered by Isra'a and Al-Azizi [10] in Basrah province (40.5%). Also the result of the present study was higher than that recorded in some countries: 2.2% in India by Singh et al. [17]; 14.6% in Italy by Scala et al. [14]. On the other hand, the result of the study was lower than those recorded from nearby and some other countries including Turkey by Senlik [16] with infection rate of 24.1%; in Iran by Oryan et al. [13] with 28.4%; 36.2% in Ethiopia by Wondimu et al. [20]; 29.4% in Greek by Christodoulopoulos et al. [6].

It is clear that our findings were somewhat higher than in some regions of Iraq and many countries. Such higher rates could be due to geographical, environmental, meteorological factors such as climate, soil properties, and relative humidity, season, and rainfall level which are crucial to the life cycle of the helminthes. Other factors play subsidiary but important roles like the degree of pasture contamination, animal management, feeding habits and grazing pattern [20]. Furthermore, dog's divagation and illegal slaughtering, shepherd dogs on grazing land as well as in paddock play the greatest role in the infection dynamic between ruminant's intermediate hosts and dog final host [16]. According to religion and culture of most families, dog is not allowed to be reared as a pet and valuable animal in the country, so all of them live freely as stray dogs in a poor hygienic condition and live with infested worm for life without treatment. This may cause continues shedding of parasite eggs into the environment and contaminate wide area of grazing pasture. On the other hand, there is a poor authority plan and regulation in the country to control and eradicate parasitic diseases.

The months of the year had significant effect on the rate of infection. It was observed that the highest percentage of infection was found in April (26.1%) which is relatively wet and humid month in the Sulaymaniyah region, in contrast the lowest percentages were seen in hot and dry months of the region including August (19%) and September (19.5%). This result was in agreement with that found by Attindehou and Salifou [2] in Benin, who indicated that *C. tenuicollis* infection was more prevalent in wet months than dry one. This is in accordance with parasite biology. In addition to that the higher infection during the rainy months might be due to the availability of the adequate humidity necessary for the development of the eggs [18].

A significant difference in the rate of infection was found between imported and local sheep, while there was no difference between ages and sexes. The frequency rate of infection in imported breed of sheep (23.7%) was higher than indigenous breed of sheep (19.6%). This difference may be linked to the divergence in genetic structure of these animals. Another reason for variation in intensity between breeds may arise from the differences in grazing behavior, which would influence the intake of infective eggs of *T. hydatigena*. In addition to that fact, the indigenous breed was subjected to infection continuously for long periods which leads to obtaining acquired immunity against infection [16]. In our knowledge there was no any other report studying the influence of host breed on the frequency of *C. tenuicollis* infection in sheep. Therefore, it was not possible for us to discuss and compare our findings with the others.

Based on predilection site, the infestation rate of *C. tenuicollis* in different organs of sheep showed, although, the mesentery, liver, diaphragm, gall bladder, urinary bladder, uterus were also affected, the cysts had a tendency to be located more in the omentum (37%). This is due to the fact that omentum covers larger surface area in the peritoneal cavity. The observation of Senlik [16]; Wondimu et al. [20]; Braae et al. [5] were concords our findings.

Acknowledgement

The findings described in this paper are a part of PhD thesis of the corresponding author. The work was financially supported by Sulaimani University, Sulaymaniyah, Iraq.

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