An epidemiological profile of brucellosis in Tabuk Province, Saudi Arabia

K.E. Elbeltagy1

1Department of Public Health and Preventive Medicine, Primary Health Care Administration, General Directorate of Health Affairs, Tabuk Province, Saudi Arabia; and Department of Public Health and Preventive Medicine, Faculty of Medicine, University of Tanta, Tanta, Egypt.

مُرْتَسَم (بروفيل) وبائي لداء البروسيلات في محافظة تبوك، بالمملكة العربية السعودية

كامل السيد محمد البلتاجي

الخلاصـة: أجريت دراسة استعادية لجميع حالات داء البروسيلات البالغ عددها 137 حالة، والتي حدثت في محافظة تبوك بالمملكة العربية السعودية في عام 1997. وقد اعتبر عيار تراصّ البروسيلات الذي يبلغ 1/80 فأكثر، أو ارتفاع عيار التراص مع سبق ظهور علامات وأعراض نموذجية، بيِّنة على الإصابة بالعدوى. وقد بلغ معدل الحدوث 34 في كل 000 100، ومتوسط العمر 33.8 ± 13.9 سنة (المجال 3 – 72 عاماً) والنسبة بين المصابين والمصابات 1.8 : 1. وكانت 63.5% من الحالات من سكان الريف، بينما كان 58.4% من المصابين ممن يربون الحيوانات في بيوتهم أو في أماكن أخرى، و27% ممن يخالطون الحيوانات أثناء العمل أو يعملون في المزارع، أو من كليهما، و88.3% ممن أبلغوا عن شرب لبن نيء. وتمثلت أوسع العوامل المعدية شيوعاً في البروسيلة المالطية Brucella melitensis والبروسيلة المجهضة B. abortus، والبروسيلة الخنزيرية B. suis. واكتشفت الإصابة بتضخم الطحال في 25.5% وضخامة الكبد في 22.6% من الحالات.

ABSTRACT All 137 brucellosis cases occurring in Tabuk Province, Saudi Arabia in 1997 were studied retrospectively. Brucella agglutination titre of ³ 1/80, or rising titre plus history of typical signs and symptoms were considered evidence of infection. The incidence rate was 34/100 000, mean age 33.8 ± 13.9 years (range: 3–72 years) and male:female ratio 1.8:1. There were 63.5% of cases rurally resident, 58.4% kept animals at home or elsewhere, 27.0% worked with animals and/or on farms, and 88.3% reported a history of raw milk ingestion. The most common infecting agents were Brucella melitensis, B abortus and B. suis. Splenomegaly and hepatomegaly were detected in 25.5% and 22.6% of cases respectively.

RESUME Tous les 137 cas de brucellose qui se sont produits dans la province de Tabouk (Arabie saoudite) en 1997 ont fait l’objet d’une étude rétrospective. Un titre d’agglutination de Brucella ³ 1/80, ou l’élévation du titre plus des signes et des symptômes typiques dans le passé étaient considérés comme preuve de l’infection. Le taux d’incidence s’élevait à 34/100 000, l’âge moyen était de 33,8 ± 13,9 ans (âge compris entre 3 et 72 ans) et le rapport hommes/femmes était de 1,8:1. Il y avait 63,5 % de cas résidant en zone rurale, 58,4 % gardaient des animaux à la maison ou dans d’autres endroits, 27,0 % travaillaient avec des animaux et/ou dans des fermes, et 88,3 % signalaient une habitude de consommation de lait cru. Les agents infectieux les plus courants étaient Brucella melitensis, B. abortus et B. suis. Une splénomégalie et une hépatomégalie avaient été dépistées chez 25,5 % et 22,6 % des cas respectivement.

Introduction

Brucellosis is a zoonotic disease of worldwide distribution. Although eradicated from many Western countries, it represents a major public health problem in Mediterranean Africa and Europe, in central Asia, and in Central and South America [1–6]. The global incidence of brucellosis is probably underestimated because of misdiagnosis and underreporting [7,8]. In Saudi Arabia, the disease is a major diagnostic concern and has been frequently reported among humans and animals [9,10].

In 1997, there was an unexpectedly sharp increase in the number of patients with brucellosis in the Province of Tabuk (north-western Saudi Arabia), a region of seven administrative districts: Hakl, Albedaa, Dubaa, Alwageh, Omlog, Tymaa and Tabuk (the capital), and a population of approximately 400 000 inhabitants. We retrospectively examined the epidemiological characteristics of all reported cases of brucellosis in the Province for 1997.

Methods

Human brucellosis is a reportable disease in Tabuk Province. Ministry of Health regulations require cases of communicable diseases such as brucellosis to be reported regularly (weekly). All hospitals (including military hospitals), primary health care centres, private polyclinics and physicians in the Province provide information to the Preventive Medicine Department of the General Directorate of Health Affairs in Tabuk, for forwarding to the Ministry of Health. Active surveillance is used to obtain incomplete information on reported cases and to detect unreported cases.

Clinical and epidemiological information on human brucellosis cases reported during 1997 were obtained. Personal identifiers for patients were excluded from the database to assure confidentiality. Descriptive, epidemiological and clinical data for each patient were obtained, including: age, sex, nationality, area of residence, marital status, education, occupation, date of onset, date of diagnosis, serological tests, titres, Brucella species, symptoms and signs, history of association with animals and/or farms, and history of raw milk ingestion.

A clinical case of brucellosis was defined as any patient with febrile illness characterized by acute or insidious onset and at least two of the following symptoms: night sweats, prolonged fatigue, anorexia, weight loss, or headache; or one of the afore-mentioned symptoms plus positive response by culture or serology. Culture was considered positive if Brucella spp. were isolated from a clinical specimen. Serology was considered positive if there was a fourfold rise in titre between acute and convalescent serum specimens, or a single titre of ³ 1/80 by agglutination titre or single titre of ³ 1/4 by complement fixation test.

Incidence calculations were based on population data from census reports. Due to the insidious nature of brucellosis, the illness onset data were imprecise. We therefore analysed the data by date of diagnosis. Data were analysed using STATA, version 3.0. Frequency distributions were tabulated and relevant statistical tests used.

Results

Of the 137 patients’ information sets reviewed and confirmed, 55.5% were reported from Ministry of Health hospitals and primary health care centres, 32.1% from private polyclinics, doctors and hospitals, and 12.4% from the military hospital. The incidence rate was 34/100 000. Figure 1 shows the sharp increase in the number of cases in 1997 compared to the previous 5 years in the province. The mean age was 33.8 ± 13.9 years (range: 3–72 years), with the highest frequency of cases in those aged 30–39 years (32.1%). Males were significantly more affected than females — 64.2% versus 35.8%, a male to female ratio of 1.8:1 (Table 1). The great majority of cases (86.1%) occurred in Saudi nationals and 65.7% of all affected cases were married. There was a seasonal variation of brucellosis throughout 1997, with two peaks — one in May and the other in September (Figure 2).

Figure 1 Brucellosis cases in Tabuk (1993–97)

Table 1 Demographic data of new brucellosis cases, Tabuk Province, Saudi Arabia, 1997

Socioeconomic data showed that 54.0% of cases had received no formal education; 27.0% worked with animals/on farms; 63.5% were resident in rural areas; and 78.8% were from the Tabuk area (Table 2). More than half of all cases 80 (58.4%) kept animals either at home or on a separate farm, and 121 (88.3%) reported a positive history of raw milk ingestion, either from their own animals and farms, or as a gift from their neighbours or relatives. The most frequent agglutination titre was 1/320 (in 56.9% of cases). The most common Brucella species isolated was B. melitensis, in 44.5% of cases, followed by 40.9% of cases of mixed infection of B. abortus and B. melitensis (Table 3). The predominant clinical manifestations were symptoms of fever, joint/back pain, lethargy, sweating and headache (Table 4). Splenomegaly and hepatomegaly were reported in 25.5% and 22.6% of cases respectively.

Figure 2 Brucellosis cases in Tabuk by month 1997

Table 3 Distribution of new brucellosis cases by brucella agglutination titre and Brucella spp., Tabuk Province, Saudi Arabia, 1997

Table 4 Comparison of clinical features of brucellosis in studies conducted in Saudi Arabia

Discussion

Brucellosis is a disease with a profound public health and economic impact. Endemicity of human brucellosis in the Middle East in general and in Saudi Arabia has been reported in several previous studies. These studies have shown a close relationship between endemicity of animal infection, inappropriate eating habits and low standards of hygiene [11,12].

The present study revealed an incidence of 34/100 000 (Figure 1) in 1997, a significant increase in the number of reported cases compared to previous years. This increased incidence could have two possible explanations. First, heavier than usual precipitation during the 1996–97 rainy season resulted in the growth of grasses in the province’s desert areas. Because precipitation in neighbouring provinces was not as great as in Tabuk, shepherds and their flocks (particularly sheep, goats, camels and cattle) were attracted from nearby regions to the grassed Tabuk desert. Some of these animals were infected. Subsequently, the infection was transmitted to local healthy animals. A second reason may be due to the cessation of the national programme for the vaccination of animals against brucellosis. However, the rate obtained in our study is lower than those reported in studies previously conducted in other parts of the country. [1,4,5,9,13]. El-Sekait [14], in a study carried out in northern Saudi Arabia, reported an incidence of 1.6% (1600/100 000), compared to the present study’s 34/100 000. The difference between the two rates may be related to the difference in areas examined. The El-Sekait study included the other four of the country’s northern provinces (Hail, Qurriyyat, Northern Frontier and Al-Jouf).

Seasonal variation of cases is explained according to the geographical nature, as well as customs and traditions in Tabuk. Grass growth in the spring, due to the rainy season, results in more animals being attracted to the area, and thus, an increase in milk and meat production, with a consequent increase in untreated milk and raw animal liver consumption and of new cases of disease peaking in the month of May. In summer, large numbers of urban Saudis habitually return to their original families in the desert and rural areas to spend the vacation. On their return to the towns and cities (August/September) they traditionally bring large quantities of untreated milk to distribute as gifts to their neighbours, relatives and friends, leading to an increase in consumption of untreated milk by more consumers, and a September peak in new brucellosis cases.

The finding of this study that the most affected group was those aged 30–39 years, (mean age 33.8 ± 13.9 years) is consistent with many other studies [1,4,5,9,14]. The study also showed a higher rate of infection among males than females, a finding also consistent with many earlier studies [4,5,9,15,16], although some studies have reported an equal frequency between sexes [1,14,17,18,19]. Infection was most common among Saudis who consumed the greatest quantities of untreated milk and raw liver and spleen. The study also found patients were more likely to be from lower socioeconomic strata, a finding which accords with the results of several previous studies [5,14,15,17]. The Tabuk area was more severely affected due to its greater population concentration and consumption of milk and animals.

Consumption of untreated milk (from goats, sheep, camels or cattle) represented the most common source of infection in this study. The most frequent Brucella species isolated was B. melitensis (44.5%), due to the preponderance of goats and sheep in Tabuk, a finding consistent with many other studies [14,15,20,21]. The relatively increased frequency of infection by B. abortus, either alone or with B. melitensis, may be due to the trend to increased consumption of untreated, infected camel’s milk, and the habit of eating raw or insufficiently cooked cow’s liver and spleen.

The comparatively higher percentage of brucellosis cases reported from general hospitals and primary health care centres is explained by their wide distribution and high patient volume. The variation in the frequency of symptoms and signs between this study and other studies is probably due to the difference in the methods of selection and in the activity and stages of disease. Patients in this study were reported from among those presenting with disease at health care facilities, whereas those of other studies were detected during field surveys [1,4,14,15,20–25].

Brucellosis is increasing in the north-western region of Saudi Arabia. Coordinated, comprehensive and organized efforts between the ministries of health, agriculture, municipal and rural affairs are required to prevent and control the disease.

Acknowledgements

I would like to thank Mr Abdullah E. Aljohany and Mr Abdullah S. Albalawi for their great assistance and support in conducting this study.

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