Journal of Helmlnthology (1976) 50, 65—73

The epidemiology of Echinococcus infection in Kuwait O. HASSOUNAH and K. BEHBEHANI Department of Zoology, Faculty of Science, University of Kuwait, Kuwait

ABSTRACT Infection of dogs with E. granulosus is recorded for the first time in the State of Kuwait and observations on 204 dogs from different suburbs showed an infection rate of 23.039%. Cattle, sheep, goats and camels killed for public consumption in the period 6th April to 6th May, 1975, in a slaughter house were inspected and the rate of infection with E. granulosus cysts was recorded. The possible methods of transmission from animals and dogs to man is discussed.

INFECTION IN KUWAIT Dogs infected with Echinococcus granulosus are the main source of human infection by the cyst of this parasite. Therefore the prevalence of infection in dogs in an area is the most reliable indicator of the danger to the human population. In addition to providing information concerning the degree of risk to the human population, the accurate determination of infection in dogs also reveals important epidemiological information concerning transmission of the parasite in the area under study and is one of the most sensitive methods for measuring the progress of a control programme. E. granulosus infection in dogs in the neighbourhood of the State of Kuwait has been investigated by various authors: Gireev (1964) in Dagestan, U.S.S.R.; Hoghoughi (1967) in Iran; Babero et al. (1963) and Kelly and Izzi (1959) in Iraq. The larval stage infection in ruminants has been recorded in the same area by various authors: Imari (1962) and Babero et al (1962) in Iraq; Yari (1962), Khalili (1962) and Mobedi et al. (1970) in Iran; Dailey and Sweatman (1965) in Syria and Frayha (1970) in Lebanon. Infection in man is from swallowing Echinococcus ova. El-Gazzar and McCreadie (1962) first reported on 51 cases from Kuwait, in which the sites of hydatid disease were: liver, 23; spleen, 3; lung, 7; bone, 2; muscles, 6; breast, 1; peritoneum, 6; ovary, 1; kidney, 1; intraorbital, 1. In addition, Tannir and Fahmy (1967) reported on three cases of pelvic hydatid cysts, Atawneh (1969) a case of hydatid cyst in the aorta and Booz (1968, 1972) on 12 cases of hydatid disease of bone. This study describes an investigation into the prevalence of E. granulosus in dogs in Kuwait and the infection of domestic animals with hydatid cyst at the Kuwait slaughterhouse. The study started in October 1974 and has covered most areas of the State of Kuwait with human settlements and areas where stray dogs have been observed, but cannot yet provide the overall prevalence in the State. 65

O. HASSOUNAH and K. BEHBEHANI

MATERIALS AND METHODS Examination of dogs Stray dogs were shot and then subjected to dissection, either in thefieldor at the Kuwait Veterinary Hospital. Unwanted dogs brought by the owners to the hospital were injected intramuscularly with 3 cm3 of Combelen (Bayer) anaesthetic and the animal was then put to sleep by making it inhale Halothane (/C/). For sampling, the abdomen of the animal was opened and the appropriate portion of the intestine collected. The portion of the intestine subject to examination was about 2 ft., beginning at the pylorus and ending distally. Tight, double, adjacent ligatures were made on either side of the required segment to secure the contents. Samples thus obtained were kept separately in polythene bags and labelled appropriately. As soon as possible the specimens were collected into a metalcovered container and cooled in a — 70°C deepfreeze until they were examined. The dogs' carcasses were afterwards incinerated. Frozen specimens were picked up after a sufficient number of specimens had been collected. They were individually thawed and slit open in a dissecting dish containing water. The mucosa was scraped with a scalpel and both mucosal scrapings and intestinal contents were washed through an 80 mesh-per-inch brass sieve. The material retained on the sieve was washed into a glass container and examined in a strong light against a black background by using a hand lens for magnification. Suspected Echinococcus and detached proglottids were removed with disposable pasteur pipettes and examined microscopically, then washed with 70% alcohol initially and stored in 70% alcohol in a securely capped bottle with a label indicating the number of specimen, the type of infection and the date of examination. Examination of slaughtered domestic animals The Governmental Central Slaughter House (G.C.S.H.) was inspected twice daily, once in the morning and once in the afternoon, and all slaughtered animals were examined for cysts. Most of the animals coming to the G.C.S.H. were imported: cattle from Somalia, sheep from Australia, Saudi Arabia, Syria and Iraq and camels from Iraq and Somalia. Sections were made from infected organs and examined microscopically for confirmation of the type of infection. RESULTS During the dog survey which was conducted from the 10th October, 1974, to the 10th February, 1975, in different suburbs and districts of the State of Kuwait, E. granulosus was found in 47 out of 204 dogs examined. The samples covered nearly all the suburbs and areas inhabited in the State of Kuwait. There were 38 suburbs and dogs were collected from 27; no dogs were found in the remaining suburbs or from Failakka Island (Figs. 1 and 2). Infection was distributed over 13 suburbs oi the 27. From 47 infected dogs, 27 were males and 20 females with an overall rate of infection of 23 %. Of the 204 dogs examined, 124 were infected with cestodes other than E. granulosus (60-78 % of the total) and of these 40 dogs were infected with nematodes (19-6% of the total). The species of cestodes and nematodes will be described separately. 66

Epidemiology of Echinococcus in Kuwait

THE

ARABIAN 100500

PENINSULA

TO 200 300KM.

FIG. 1 The position of the State of Kuwait in relation to surrounding countries in the Arabian Peninsula. The area surveyed for Echinococcus infection is shown in figure 2.

The majority of dogs examined were mongrels, known as the desert breed and three were terriers; 15 were hunting dogs belonging to a different genus (Lycaon pictus). Only one of the terriers was stray and the other two were brought by the owners to the Veterinary Hospital. All the dogs brought by owners to the Veterinary Hospital were negative. Of the 15 hunting dogs examined six were found to be infected. No puppies examined were infected with E. granulosus.

The degree of infection varied from three to several thousand worms. The average length of an entire worm was between 4-6 mm and had three to five segments. In some districts very few dogs could be collected. For statistical significance the sample was based upon dividing the State of Kuwait into two major towns, Kuwait and Al-Ahmadi. Collections were made in these towns and in their suburbs (Table 1). The infection rate was highest in Kuwait city and its suburbs (24-24%) followed by Al-Ahmadi town and its suburbs (17-94%). 67

O. HASSOUNAH and K. BEHBEHANI

10.0%

KUWAIT \

100% FIG. 2 Showing the rate of infection among dogs in Kuwait City, ( = ) and Al-Ahmadi town, (|||||) and their suburbs Key to districts: 1. Kuwait City 2. Al-Jahra 3. Al-Doha 4. Abraq Khitan 5. Al-Sulibikhat 6. Al-Gewan 7. Al-Salmyah 8. Al-Shwaikh Ind. Area 9. Al-Sulaibiya lO.Al-Rass 11. Al-Rumythyah 12. Al-Bnade Al-Qar 13.Abdulla Al-Salem 14. Al-Sour Area 15. Al-Surra 16. Al-Jidadyia 17. Al-Khaldiya 18. Hawalli 19. Al-Shwaikh 20. Al-Ahmadi 21. Salwa 22. Al-Fintas 23. Al-Shuaiba 24. Al-Fahahil 25. Al-Wafra 26. Al-Funitces 27. Al-Mesylah 28. Failaka Island 68

Epidemiology of Ech'mococcus in Kuwait

Of the 924 cattle observed, 369 were infected, of which 159 were infected only in the liver, 56 only in the lungs and 154 in both the lungs and livers. The rate of infection in the native cattle was 32*5% among 43 individuals examined. 881 cattle from Somalia had an infection rate of 40-2%. Most of the sheep that came into tbe slaugher-house (approx. 90%) had been imported from Australia. A small number of sheep were also imported from Iraq, Saudi Arabia and Syria. From 9 922 Australian sheep, only 22 were infected (0-2%) while, of 724 Iraqi sheep, 84 were infected (11*2%). The rate of infection among Saudi Arabian sheep (10-4%) was close to those from Iraq. The number of slaughtered sheep from Syria was too few to give a dependable profile of the infection rate. All slaughtered goats were native; only one of a total of 20 was found to be infected. Somalia and Iraq were the only sources from which camels were imported (37 from Somalia and 31 from Iraq). A higher infection rate appeared in camels imported from Iraq (35-4% lrom Iraq, 10-8% from Somalia). The infected organs in most animals were lung or/and liver. A few were infected in the spleen, heart or peritoneum (Table 2).

TABLE 1 Showing the rate of infection among dogs in Kuwait City and Al-Ahmadi town and their different suburbs T3

S

Locality

Kuwait City and suburbs: Al-Jahra Al-Doha Abraq Khitan Al-Sulibikhat Al-Gewan Al-Salmyah Al-Shwaikh Ind. area Al-Sulaibiya Al-Rass Al-Rumythyah Al-Bnade Al-Qar Abdulla Al-Salem Al-Sour Area Al-Surra Kuwait City Al-Jidadyia Al-Khaldiya Hawalli Al-Shwaikh

Locality

05

40

24-24

24 20 16 13 9 4

13 5 4 4 0 2

7

3

7

0 1 0

54-16 25 25 30-76 0 50 42-80 0 14-20 0

7

10 6

5 5

4 4 4 2 1 1

0 0

0 0

2 1 0 0 0

40 25 0 0 0 0 0

0 0

Al-Ahmadi Town and suburbs: Salwa Al-Fintas Al-Shuaiba Al-Fahahil Al-Ahmadi Al-Wafra Al-Funitees Al-Mesylah Failaka Island

%

i

2-8

39

7

17-94

16 9 9 7 6 4 3 1 —

5 3 0 3 0 0 0 1 —

31-25 33-30 0 42-80 0 0' 0 100 —

69

355 40-20

881

Somalia

24

75 15 1

19 10-40 2 5000

182

Syria

4

1

5

3 31

37

%

Camels

11 35-40

4 10-80

No. No. Liver Lung exam- infecined ted

Site

22

Sheep

22 00-20 84 11-60

9922

Saudi Arabia

200

10

724

300

13

No. No. Liver Lung exam- infecined ted

Site

Iraq

Australia

14 32-50

43

No. No. exam- infecined ted

Native

Country of origin of animals

Cattle

4



20

1 0005

No. No. Liver Lung exam- infecined ted

Site

Goats

Liver Lung

Site

The rate of hydatid cyst infection of domestic animals slaughtered at the Governmental Central Slaughter House of Kuwait between 6th April and 6th May, 1975

TABLE 2

5

S ™

s

Epidemiology of Echinococcus in Kuwait

DISCUSSION The prevalence of E. granulosus in dogs varies considerably throughout the world. In the Middle East an infection rate of 50-58-5% has been recorded in Dagestan (Gireev, 1964), 34-4% in Shiraz, Iran (Hoghoughi, 1967), 38-4% in Iraq (Babero et a!., 1963) and 85% in Baghdad (Kelly and Izzi, 1959). The infection rate of dogs in Kuwait is, therefore, close to the average for the region and can form an important source of infection to man. Infection of Echinococcus larval stages in ruminant has been recorded in countries surrounding or near the State of Kuwait, such as Iraq, Iran, Syria and Lebanon. In Iraq, Imari (1962) undertook two surveys on echinococcosis in ruminants. In thefirst,which was carried out in 1954, he found that 40 % of 182 sheep and 20 % of 25 cattle were infected with hydatid cysts; aboutfiveyears later, he found hydatid cysts in 42% of 2 120 sheep, 12% of 65 lambs, 40% of 300 goats, 50% of 52 buffaloes and 75% of 68 camels. The most recent survey was carried out by Babero et al. (1963) who found that 29-5% of 2048 sheep, 13-9% of 172 cows, 35-6% of 87 buffaloes, 49-1 % of 55 camels and 26-6% of goats were infected. In Iran, Mobedi et al. (1970) found that 64% of camels slaughtered in Teheran had hydatid cysts. Mobedi et al. (1971) also reported that of 1 040236 sheep and goats slaughtered during four years in different parts of Iran, 68 672 (6-6%) were infected with hydatid cysts. The highest rate of infection (14%) was found among sheep and goats on the northern slopes of the Alborz Mountains, in the Zagros Mountains and in the north of State of Khorassan. Yari (1962) reported that 1-5% of 36 329 sheep and goats and 10% of 5 552 cattle examined in Teheran slaughter-house were infected and Khalili (1962) found an infection rate of 4-3% among 64231 sheep and goats examined in Ahwaz. The rate of infection among 64231 cattle and 161 buffaloes in the same areas was 14% and 57% respectively. Dailey and Sweatman (1965) reported an infection rate of 100% among 31 camels examined in Syria. Frayha (1970) reported an infection rate amongst animals from Lebanon as 33-6 % in swine, 37-8% in cattle, 23-1 % in sheep and goats, 60 % in donkeys and 100% in camels. On comparison, the rate of infection in Lebanon, Syria, Iraq and Iran is more or less the same as that found in the State of Kuwait. A variety of factors relative to home environment, socioeconomic and educational background might assist in transmission of hydatid parasite. One could generally classify people in the State of Kuwait into two groups—the majority (88-04%) who live in towns and supposedly have a higher standard of hygiene than the minority (11-96%) living in the outskirts and countryside. The latter group consists mainly of the Bedouins who live in the desert either in permanent shanties or in portable tents for their travels following their flocks. The shanties are of wooden construction, made from old packing cases and covered with waterproof bituminous felt. A typical shanty consists of four to five room units including a central courtyard with a separate "diwaniyah" (sitting room) and an animal enclosure, the whole separated from adjacent dwellings by at least 10 metres. The Bedouins are nomadic stock-rearing tribesmen, keeping sheep herds. It is clear from the nomadic life of the Bedouins that they travel from place to place in search of food and water for theirflocks.They and their animals—sheep, camels, goats and dogs—use the same source of water for drinking and other purposes. The rate of infection among dogs as shown in this study was found to be very high in Bedouin areas, similar to the high infection rates among this community reported by 71

O. HASSOUNAH and K. BEHBEHANI

Gazzar and McCreadie (1962) and by Booz (1972). In the areas where Bedouins live, one can observe a close contact between children and infected dogs, as well as children playing in places contaminated with dog faeces. The high rates of household or occupational contact with livestock and dogs, and frequent practise of feeding dogs the raw viscera of home slaughtered sheep or goats, create excellent conditions for the maintenance of the parasite. During the survey, it was observed that dead sheep or goats as well as the internal organs of slaughtered animals were thrown near the Bedouins' camp and the dogs were eating from the carcasses and offal. On one occasion it was seen that a number of dogs were eating the organs of a slaughtered sheep which was found to be infected with Echinococcus cysts. The relatively high rate of infection found in Kuwait town and its suburbs may also be due to the traditional slaughtering of sheep on special Islamic occasions such as Al-Adha Eid. Infected viscera are usually thrown away and stray dogs can get access to them. It was also observed that the offal from the slaughter-house was dumped outside Kuwait town (Al-Mahraga area) in the morning and burnt in the late evening each day. In the meantime stray dogs had access to discarded infected organs. The data collected from the slaughter-house shows that most of the slaughtered sheep had been imported from Australia (approx. 90 %). A great difference in the infection rate was clearly evident when Australian imported sheep were compared to those imported from Iraq, Saudi Arabia and Syria. This may be due to the extensive work done in Australia towards eradication of the disease (Le Riche and Jorgensen, 1971). To avoid the risk of infection to human beings with this dangerous parasite, a control programme for eradication of the infected sources should be established. For this purpose, the dogs must be prevented from eating the raw viscera of infected sheep, cattle or other intermediate hosts and the stray dogs must be eliminated. The offal of the slaughtered animals must not leave the slaughterhouse and should be incinerated in the slaughterhouse or deeply buried in the ground so that the dogs will not have access to it. The Bedouin and the public should be informed of the danger of the disease and methods of prevention. Since the completion of this work, a confined place has been constructed in G.C.S.H. to store the infected organs. These organs, after being processed through series of different methods in order to eliminate the viable hydatid cysts, are used as poultry food. As a way of minimizing the danger of infection carried by dogs, the authorities in Kuwait have now established "stray dog" shooting campaigns.

ACKNOWLEDGEMENTS The authors would like to express their full gratitude and acknowledgement to H. E. The Minister of Public Health, Dr Abdul-Rahman Al-Awadi for the assistance and facilities he has given during the execution of the work. Our thanks are also due to Dr Aly Zein El-Abidin, Head of Quarantine and epidemiology section Vet. Department and Dr R. K. Alshaer, Head of Technical units slaughterhouses section for their cooperation. We would also like to acknowledge the Department of Zoology, Faculty of Science, University of Kuwait, for providing facilities. 72

Epidemiology of Echinococcus in Kuwait

REFERENCES ATAWNEH, A. (1969) Hydatid cyst embolus at the bifurcation of the aorta. The Journal of Kuwait Medical Association, 3, 223-226. BABERO, B. B., AL-DABAGH, M.A., AL-SAFFAR, A. S., and ALI, F. M. (1963) The zoonosis of animal parasites in Iraq. VIII: Hydatid disease. Annals of Tropical Medicine and Parasitology, 57, 499-510. BOOZ, M. K. (1968) Hydatid disease of bone in Kuwait with special reference to differential diagnosis. The Journal of Kuwait Medical Association, 2, 27-33. BOOZ, M. K. (1972) The management of hydatid disease of bone and joint. Journal of Bone and Joint Surgery, 54B, 698-709. DAILEY, M. D., and SWEATMAN, G. K. (1965) The taxonomy of Echinococcus granulosus in donkey and dromedary in Lebanon and Syria. Annals of Tropical Medicine and Parasitology, 59,463-477. FRAYHA, G. (1970) Studies on hydatid disease in Lebanon. Lebanese Medical Journal, 23, 135-150. FUCHS, W., GATTINGER, T. E., and HOLZER, H. F. (1968) Explanatory Text to the Synoptic Geologic Map of Kuwait. The Geological Survey of Austria: Vienna. GAZZAR, A., and McCREADIE, D. W. A. (1962) Hydatid disease in Kuwait. British Medical Journal, (July), 232-234. GIREEV, G. I. (1964) Epidemiology of hydatid echinococcosis in Dagestan (in Russian, English summary). Medskaya Parazit, 33, 352. HOGHOUGHI, N. and JALAYER, T. (1967) The prevalence of Echinococcus granulosus in dogs in Shiraz, Iran. Annals of Tropical Medicine and Parasitology, 61, 437-438. IMARI, A. J. (1962) Pulmonary hydatid disease in Iraq. American Journal of Tropical Medicine and Hygiene, 11, 481-490. KELLY, T. D., and IZZI, N. (1959) Pulmonary hydatid disease in Iraq, with a review of history and life history of parasite. Journal of the Faculty of Medicine, Baghdad, 1, 115-140. KHALILI, Kh. (1962) Quoted from Alani and Maghami, 1964. The Archives Institute ofRazi, 16, 76-81. LE RICHE, P. D., and J0RGENSEN, R. J. (1971) Echinococcosis (hydatidosis) and its control. Food and Agriculture Organization of the United Nations. N.E.A.H.I. Handbook No. 6. MOBEDI, I., MAD ADI, H., and ARFAA, F. (1970) Camel Camelus dromidarius as intermediate host of Echinococcus granulosus in Iran. The Journal of Parasitology, 56, 1255. MOBEDI, I., ARFAA, F., and FARAHMANDIAN, I. (1971) Studies on Echinococcosis in Iran. Acta Medica Iranica, 14, 221-229. TANNIR, A. D., and FAHMY, K. (1967) Pelvic hydatid cysts. The Journal of Obstetrics and Gynaecology British Commonwealth, 74, 592-595. YARI, M. (1962) Study on hydatid cyst and its infection rate among animals slaughtered in slaughter-houses in Teheran. Thesis for Veterinarian Medical degree from School of Veterinary Medicine, Teheran University. (No. 318). Accepted 19 February 1976

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The epidemiology of Echinococcus infection in Kuwait.

Journal of Helmlnthology (1976) 50, 65—73 The epidemiology of Echinococcus infection in Kuwait O. HASSOUNAH and K. BEHBEHANI Department of Zoology, F...
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