Sot.Sci.Med. Vol. 29,No. 8,pp.999-1001,1989 Printed in Great Britain. All rights reserved
Copyright C 1989Pergamon Press plc
FRANK W. KIEL and M. YOUSUF KHAN King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia Abstract-This paper describes the history of brucellosis and the current public health picture in the Kingdom of Saudi Arabia. Health protection is made more difficult by several factors: (a) the local custom of drinking raw and warm milk of sheep, goats, and camels, (b) the animal reservoir of infection in the country complicated by importation of live animals both for sacrifice during Haj periods and to increase commercial flocks, and (c) by uncontrolled movements of humans and stock across political borders. Key words--Saudi
Arabia, brucellosis, animal reservoir
cities, so that customers could have fresh milk. When animals were infected, the raw milk became an optimal source of the bacteria [l]. The Mediterranean Fever Commission (1904-07) in Malta found goats to be infected, with mastitis a significant manifestation. It was concluded that raw goat milk was the source of human disease. Prohibiting goat milk and cheese in military establishments caused the disease to diminish remarkably among the soldiers and sailors of Malta in a few years .
Brucellosis is a bacterial disease affecting animals and humans, with acute and chronic forms. It is characterized by fever, generalized malaise and lassitude, with localized joint, genital and cerebral manifestations. A major epidemiologic concern throughout Saudi Arabia, brucellosis is particularly prevalent in the rural Nejd region around Riyadh and the rural Eastern Province around Dammam. In the more urbanized western area of the Hejaz around Jeddah, where raw milk is drunk less frequently, there is a lower incidence of the disease. Urbanization and medical care are advancing swiftly, but the population has a nomadic background which perpetuates the drinking of raw milk, the suspected source of the disease.
Malta Fever is still the most common name in Saudi Arabia for this disease, although ‘brucellosis’ is preferred by veterinarians and physicians. British reports of ‘protracted and remittent fevers’ occurring in Malta were made in the eighteenth and nineteenth centuries, probably referring to brucellosis. It was confused with typhoid and malaria. David Bruce, born in 1855, a Lieutenant in the British Army Medical Service, was assigned to Malta about 1885. He encountered there a local disease, characterized by pains in the tibia, called ‘Malta fever.’ (It was also known as ‘Rock of Gibraltar fever’, ‘country fever of Constantinople’, ‘new fever of Crete’, Cyprus fever’.) Bruce, with his wife as assistant, established a laboratory and a monkey colony. He discovered an organism in the spleen, and reproduced the disease in monkeys (188687). Clinical features were described and the organism was cultivated from the spleen in 1889. He named it Micrococcus melitensis. (‘Melita’ was the Roman name for Malta, because of the honey produced there.) It was renamed Brucella melitensis in 1920. It was the Maltese practice for goats to be driven morning and evening to the doors of houses in Valletta and Sliema, Mdina and Rabat, and other
The potential for a brucellosis epidemic is exemplified by the occurrence in the spring of 1983 of 29 cases of brucellosis (B. melitensis) in Houston, among Mexican immigrants, aged 2-81 yr. They reported eating goat cheese (‘queso blanco’) before the onset of their symptoms. It had been purchased from neighbourhood weekend vendors who sold the product from vehicles. The cheese was reportedly produced in Linares, Mexico and was unpasteurized. After the news releases, the vendors disappeared . In the United States, in the period 1965-78, there were 3316 brucellosis cases, 4% attributed to raw dairy products from Mexico, predominantly fresh cheese from unpasteurized goat milk. Other countries with > 1000 cases of brucellosis per year are Argentina, Greece, Iran, Italy (especially due to pecorino cheese made from unpasteurized sheep milk in central Italy), Mexico, Peru, Spain . ARAMCO (Arabian American Oil Company) has reported that brucellosis in Saudi Arabia is increasing. From 1956 to 1982, there were 39 sporadic cases. In just 2 yr, 1983-84, there were 48 new cases . Young males had an increase because of their travels in pasture areas where unpasteurized milk and cheese were available. Older women had an increase because they frequently cared for the animals, as opposed to the younger women who had a child-bearing role. The nomadic life style may be disappearing, but persons with that heritage retain a fondness for camel, goat and sheep milk, including ‘laban’ (buttermilk). The milk is considered best while still warm,
KIELand M. YOUSUF KHAN
fresh and unpasteurized, because boiling is reputed to remove its ‘goodness’. It is generally obtained from animals maintained by the family, although it can be purchased or be received as a gift. The infectiousness of the disease is illustrated by nine cases among the expatriate staff of the hospital in 4 yr-an obstetrician, two nurses and six bacteriology laboratory technicians. One nurse had B. abortus, suggesting that the disease had been acquired when she was on vacation in Thailand, where that strain is more common. Infection control was tightened in the Bacteriology Section after the fifth and sixth laboratory-acquired cases, with Brucella work being performed within a safety hood and visitors to the section being curtailed. CLINICAL FEATURES AND THEIR GEOGRAPHIC ASPECTS
In humans, acute brucellosis presents with fever, chills, sweating and malaise, with more discrete manifestations in the brain, joints or genitalia. At King Fahad Hospital, it appears to be a common cause of fever of unknown origin, acute and subacute arthritis, epididymitis, meningitis and low back pain particularly in the sacroiliac area . Spontaneous abortion, though reportedly not a complication in women because of the human placenta’s lack of erythritol, occurred in 18 of 26 first/second trimester patients with brucellosis. Early treatment may prevent that complication . The disease may be suspected in any geographic area in a patient with typical findings and a history of exposure, but the diagnosis can be proved only in a laboratory. In much of the world, brucellosis titers of 1: 160 or 1:320 would be considered appropriate for diagnosis. In Saudi Arabia, however, where past and continuing exposure is frequent, the predictive value of 1: 160 and 1:320 is low. This observation reflects the fact that farmers and veterinarians who work in brucellosis regions may have persistently high brucellosis antibody levels. Therefore, a higher threshold of I:640 has been found to correlate better with culture-positive disease [q. B. melitensis accounts for 92% of cases, with B. abortus 8%. B. suis, the organism found in hogs, is not expected and not found. ANIMAL
During the Haj period, Saudi Arabia imports sheep and goats for sacrifice from Africa, India and Australia, significant numbers infected with brucellosis. Those not slaughtered may be sold, and enter the local livestock pool and mix with local breeds, thereby increasing the potential for spread of the disease among animals. The incidence of brucellosis in domestic livestock in Saudi Arabia was determined in a study covering the period 1977-82. Of 14,000 serum samples, 305 were positive by plate agglutination procedure. Incidence was highest at sheep and goat breeding farms (11.6%). Imported livestock sacrificed at Mecca during Haj in 1977 had an incidence of 2.6% while 1.5% of the local livestock sacrificed was infected. Rates in imported sheep, goats, cattle and camels
among Ha; Arabia. 1977
Country Domestic W) Sheep Goats Cattle Camels Source:
0.5 0.8 3.6 2.8
Imported (%I I.1 4.8 7.5 3.5
1.3 4.8 7.2 0
were all reported higher than in domestic animals (see Table 1). Countries of origin for the imported animals showed varying rates (see Table 1). Animals on desert ranges have a low incidence (O.S%), attributable to factors hostile to organismsdesiccation, sunlight and the mobility of animals. It is not uncommon to see camels, sheep and goats in backyard enclosures and also roaming freely in small towns and villages. Backyard operations had a low incidence (0.4%), but the confinement in close proximity to people makes them a dangerous source of infection. Commercial dairies had the lowest incidence (0.2%) [S]. It will be noted in Table 1 that no Australian imports were infected. According to an Australian exhibitor at the Saudi Agriculture Exhibit in Riyadh, 10-14 April 1988, brucellosis was eliminated in cattle in Australia by 1986, with destruction of positive herds and the shooting of isolated animals. A few pockets of the disease in sheep may remain. This is significant, since the Melbourne Islamic abattoir alone exports sheep, goats and cattle to Muslim countries valued at $Aus.SO million. Camels have been incriminated as a source of infection. As with sheep and goats, the milk is considered best if fresh and warm. Brucellosis has been reported in camels elsewhere: Sudan4.9%, India-1.8% and 5.2%, Nigeria-l %, Kenya-12%. It is also reported to occur in wild animals, such as fox, polecat, moose, buffalo, hedgehog and reindeer. Bacteria have been identified in parasites, such as bedbugs and ticks . The Pathology Department of King Fahad Hospital in 1987 began the project ‘Investigation of family animals of patients diagnosed as having brucellosis’. Sixteen interviews were conducted, but the source of the infection could not be pinpointed. A history of ingestion of raw milk was often obtained, but the milk was sometimes a combination of sheep and goat milk, sometimes a gift from visiting or distant relatives, or a purchase from a passing shepherd. Sick animals at home might be identified as having poor appetite. Two field studies, one involving milk and blood from 10 sheep, and the other involving a camel, were done. Cultures and serology were negative. There is concern that if an infected animal is discovered, it will not be treated or destroyed, but rather will be quickly sold. PREVENTION
The increasing incidence of brucellosis is attributed to recent changes in the system of animal production and marketing. The dairy industry has been formed with pregnant heifers from the U.S.A., Holland, West
Brucellosis in Saudi Arabia CONCLUSION
Table 2. Recent stock importations to Saudi Arabia
Sheep Goats Camels Cattle Buffalo Source:
2,465.127 718,269 17,290 76,984 IS60
I.375941 12,094 176,389 12,101
Germany and France. Intensive sheep and goat production has been established and subsidized by the government. The local desire for meat has increased considerably, and the importation of animals has occurred, including from countries where brucellosis is prevalent (see Table 2). There are no controls on movement of animals across political boundaries, so that Saudi herds may range into Iraq or Jordan. There is no testing to confirm brucellosis-free certificates. Imported semen is used, which may be from infected bulls. There is no overall government programme for slaughter or compensation [lo]. This is in contrast to Texas where brucellosis is both a health problem and an economic problem. Cattle cannot be sold without a ‘brucellosis-free’ certificate. Considerable effort to assure brucellosis-free herds has occurred. The 1980-85 Texas Report showed certified brucellosisfree herds there increased from 46 to 1450. Calf vaccinations increased from 557,888 to 1,353,337. Quarantined herds declined from 2413 to 1528 [I I]. A programme for control of the disease in the Najdi sheep flock at Haradh was implemented in 1981. At the first test, 14.2% were reactors; 2nd test-1.5%; 3rd test-O.3%. Of eight shepherds, six had Malta fever. Positive reactor sheep were slaughtered and buried after each test. After the third test, all negative sheep were vaccinated with killed B. mefitensis 53H38 vaccine. One year later, abortion and infertility were gone, and the lambing percentage had increased from 0.8 to 1.3 per ewe . Commercial camel milk production started in Saudi Arabia in 1987, and there are now two camel dairies, located not far from Riyadh at Al-Kharj. They produce 1100 1 of camel milk per day. All milking is done by hand, since mechanical milking has not been successful because of the irregular teat size and the loud machine noise. A good milk camel may give 25 1 per day. The milk is pasteurized and sold to stores.
Brucellosis appears to be increasing in prevalence in Saudi Arabia in the central and eastern regions. The disease is acquired by the ingestion of raw milk and milk products obtained from sheep, goats and camels, a custom fostered by the nomadic heritage and dietary customs of the people. Animal brucellosis has been confirmed, but a national policy to eradicate the animal disease has not been undertaken, although attempts have been made to identify the problem in imported infected animals. Increased awareness of brucellosis as a cause of human disease has been accomplished, leading to quicker diagnosis and earlier treatment to ease the individual patient’s distress. REFERENCES
Christie A. B. infectious Diseases: Epidemiology and Clinical Practice, pp. 824-843. Churchill Livingtone, Edinburgh, 1980. Strong R. P. Stitt’s Diagnosis, Prevention and Treatment of Tropical Diseases, pp. 739-740. Blakiston, Philadelphia, Pa., 1944. Centers for Disease Control. Brucellosis-Texas. Morbid. Mortal. Wkly Rev. 32, 548-553,
Arrighi H. M. Brucellosis surveillance in Saudi Arabia’s Eastern Province. Ann. Saudi Med. 6, S5-SlO, 1986. Khan M. Y. Brucellosis: observations on 100 patients. Ann Saudi Med. 6, SlP-S23, 1986. Khan M. Y. and Kiel F. W. Outcome of B. melitensis infection in pregnancy. 28rh International Conference on AntimicrobiaL Agents and Chemotherapy, Am. Sot. Microbial., Los Angeles, Calif., 1988. 7. Kiel F. W. and Khan M. Y. Analysis of 506 consecutive positive serologic tests for brucellosis in Saudi Arabia. J. clin. Microbial. 25. 1384-1387,
8. Radwan A. I., Asma; J. A., Freichs W. M., Bekairi S. 1. and Al-Mukayel A. A. Incidence of brucellosis in domestic livestock in Saudi Arabia. Trop. Anim. Hlth Prod. 15, 139-143, 1983. 9. Al-Kandari S., Al-Enezi A. and Christie A. B. Brucellosis, a continuing problem. Postgrad. Doctor Middle East 10, 412-417, 1987. 10. Hafez S. M. The impact of uncontrolled animal importation and marketing on the prevalence of brucellosis in Saudi Arabia. Ann. Saudi Med. 6, S15-S18, 1986. 11. Brucellosis progress Report. Five Year Summary. The Comfort News 7, 12 December, 1985. 12. Radwan A. I., Bekairi S. I., AI-Mukayel A. A. and Abu Agla 0. S. Control of ovine brucellosis in Najdi sheep in Saudi Arabia. Trop. Anim. Hlth Prod. 16. 213-218. 1984.