Systematic review of brucellosis in the Middle East: disease frequency in ruminants and humans and risk factors for human infection.

A systematic review of studies providing frequency estimates of brucellosis in humans and ruminants and risk factors for Brucella spp. seropositivity in humans in the Middle East was conducted to collate current knowledge of brucellosis in this region. Eight databases were searched for peer-reviewed original Arabic, English, French and Persian journal articles; the search was conducted on June 2014. Two reviewers evaluated articles for inclusion based on pre-defined criteria. Of 451 research articles, only 87 articles passed the screening process and provided bacteriological and serological evidence for brucellosis in all Middle Eastern countries. Brucella melitensis and B. abortus have been identified in most countries in the Middle East, supporting the notion of widespread presence of Brucella spp. especially B. melitensis across the region. Of the 87 articles, 49 were used to provide evidence of the presence of Brucella spp. but only 11 provided new knowledge on the frequency of brucellosis in humans and ruminants or on human risk factors for seropositivity and were deemed of sufficient quality. Small ruminant populations in the region show seroprevalence values that are among the highest worldwide. Human cases are likely to arise from subpopulations occupationally exposed to ruminants or from the consumption of unpasteurized dairy products. The Middle East is in need of well-designed observational studies that could generate reliable frequency estimates needed to assess the burden of disease and to inform disease control policies.

Cross-sectional study of brucellosis in Jordan: Prevalence, risk factors and spatial distribution in small ruminants and cattle.

Brucellosis is considered endemic in many Middle Eastern countries including Jordan. To determine the frequency, risk factors and spatial distribution of ruminant brucellosis in Jordan, a nationwide cross-sectional study was conducted. Small ruminant flocks (n=333) and cattle herds (n=204) were randomly selected, and their disease status was ascertained by testing individual serum samples using the Rose Bengal Test and a competitive ELISA (sheep and goats) and milk samples using an indirect ELISA (cattle). Information on putative risk factors was collected using standardized questionnaires. A logistic model with a binomial outcome was built to identify risk factors for being seropositive. The estimated true seroprevalence values were 18.1% (95% CI: 11-25.3) (cattle-only herds), 22.2% (95% CI: 16.5-28.8) (sheep flocks), 45.4% (95% CI: 30.3-61.6) (goat herds), 70.4% (95% CI: 55.5-84.9) (mixed sheep-goat flocks), 34.3% (95% CI: 28.4, 40.4) (all small ruminant flocks) and 38.5% (95% CI: 24.3-51.8) (mixed herds of cattle and small ruminants). Only 1.5% of small ruminant flocks were vaccinated. The seroprevalence was higher in northern areas, where livestock density is also higher. The logistic model fitted the data well and had a very high predictive ability. In the small ruminant model, five variables were significantly associated with a higher odds of seropositivity: lending/borrowing rams (OR=8.9, 95% CI: 3.0-26.1), feeding aborted material to dogs (OR=8.0, 95% CI: 3.5-18.1) the presence of goats (OR=6.9, 95% CI: 3.1-15.4), introducing new animals to the flock (OR=5.8, 95% CI: 2.5-13.6), and a large flock size (OR=2.2, 95% CI: 1.0-4.6). Conversely, separating newly introduced animals (OR=0.16, 95% CI: 0.05-0.47), separating animals that had aborted (OR=0.19, 95% CI: 0.08-0.46) and using disinfectants to clean pens (OR=0.37, 95% CI: 0.16-0.83) were significantly associated with a lower odds of being seropositive. The main risk factor for cattle herds being seropositive was the introduction of new animals (OR=11.7, 95% CI: 2.8-49.4); while separation of newly introduced animals (OR=0.09, 95% CI: 0.03-0.29), herd disinfection (OR=0.04, 95% CI: 0.01-0.15) and having calving pens (OR=0.14, 95% CI: 0.05-0.43) significantly reduced the odds of infection. Brucellosis is endemic at high levels across Jordan, and the current vaccination programme, which is limited to small ruminants, has very low coverage. A revised brucellosis control programme is required in Jordan. Given the high baseline prevalence, it should be based on vaccination accompanied by measures to promote hygiene and husbandry practices that minimize the risk of introduction and maintenance of Brucella spp., and thereby the risk of human infection.

Risk factors for human brucellosis in northern Jordan.

Little is known about the risk factors of human brucellosis in Jordan. A case-control study was conducted involving 56 Jordanians who had been treated for brucellosis and at least 3 matched controls for each case (n = 247). Matching was for sex, age, locality (the same village) and socioeconomic standard. Univariate and multivariate logistic regression analyses were used. In all, 17 risk factors were examined related to: contact with various livestock, milk and milk product consumption, drinking-water treatment and disease awareness. Most variables were associated with brucellosis in the univariate analysis but the final logistic model included only 4: milking sheep and goats (OR 3.5), consumption of raw feta cheese made from sheep and goat milk (OR 2.8) and consumption of cows' milk (OR 0.4) and boiled feta cheese (OR 0.4). Small ruminant farmers need to be trained in safer milking practices and feta cheese making procedures.

Risk factors for human brucellosis in northern Jordan

Little is known about the risk factors of human brucellosis in Jordan. A case-control study was conducted involving 56 Jordanians who had been treated for brucellosis and at least 3 matched controls for each case [n = 247]. Matching was for sex, age, locality [the same village] and socioeconomic standard. Univariate and multivariate logistic regression analyses were used. In all, 17 risk factors were examined related to: contact with various livestock/ milk and milk product consumption, drinking-water treatment and disease awareness. Most variables were associated with brucellosis in the univariate analysis but the final logistic model included only 4: milking sheep and goats [OR 3.5], consumption of raw feta cheese made from sheep and goat milk [OR 2.8] and consumption of cows' milk [OR 0.4] and boiled feta cheese [OR 0.4]. Small ruminant farmers need to be trained in safer milking practices and feta cheese making procedures

Seroprevalence of Brucella species among women with miscarriage in Jordan.

Results differ as to whether Brucella infection during pregnancy increases a woman's risk of miscarriage. We determined the seroprevalence of BrucelIa spp. among a sample of women with miscarriage and women with no history of miscarriage in Jordan during January-July 2003. Serum samples were collected from 445 women with miscarriage and a similar number of women with no history of miscarriage, matched on age, socioeconomic status and residence. Sera were tested using the Rose Bengal plate test and complement fixation test. The true seroprevalence among women with miscarriage was 1.8% (95% CI: 0.6-3.0), while the true seroprevalence among women with no history of miscarriage was 1.0% (95% CI: 0.08-1.9). There was no significant difference between seroprevalences of Brucella spp. among women with miscarriage and those with no history of miscarriage (P= 0.6).

Seroprevalence of Brucella species among women with miscarriage in Jordan

Results differ as to whether Brucello infection during pregnancy increases a woman's risk of miscarriage. We determined the seroprevalence of Brucella spp. among a sample of women with miscarriage and women with no history of miscarriage in Jordan during January-July 2003. Serum samples were collected from 445 women with miscarriage and a similar number of women with no history of miscarriage, matched on age, socioeconomic status and residence. Sera were tested using the Rose Bengal plate test and complement fixation test. The true seroprevalence among women with miscarriage was 1.8% [95% Cl: 0.6-3.0], while the true seroprevalence among women with no history of miscarriage was 1.0% [95% CI: 0.08-1.9], There was no significant difference between seroprevalences of Brucello spp. among women with miscarriage and those with no history of miscarriage [P= 0.6]

Prevalence and burden of gastrointestinal helminthes among local chickens, in northern Jordan.

We conducted a cross-sectional study from December 2004 to February 2005 and from June 2005 to August 2005. The study aimed to determine the prevalence of gastrointestinal and tracheal helminthes among local chickens in northern Jordan. A total of 208 male and female local scavenging chickens were selected randomly. We examined the trachea and gastrointestinal tract of each bird for the presence of helminthes. We recovered three nematode and eight cestode species. No trematodes were found. One hundred and fifty-two birds (73.1%) (95% CI: 67, 79) were infected. The prevalences of different species were as follows: Ascaridia galli female 28%, male 43%; Capillaria obsignata 0.5%; Heterakis gallinarum 33%; Amoebotaenia cuneata 4.3%; Choanotaenia infundibulum female 23%, male 13%; Davainea proglottina 1.4%; Hymenolepsis cantaniana 11%; Hymenolepsis carioca female 35%, male 24%; Raillietina cesticillius female 5%, male 11%; Raillietina echinobothrida 16%; and Raillietina tetragona 18%. The prevalences of A. galli and R. cesticillus were higher in male than female hosts while those of C. infundibulum and H. carioca were higher in females. The median worm burden was 7 (range 0-168) worms per chicken.

Estimating the economic effects of cystic echinococcosis. Part 3: Jordan, a developing country with lower-middle income.

The economic costs of cystic echinococcosis (CE) in Jordan, a developing country of lower-middle income, were investigated. Initial cost-estimates for livestock were based on the published prevalences of Echinococcus granulosus infection in sheep and goats and the values of livestock-related products together with likely production losses. Likewise, the annual numbers of human cases of CE were estimated using published surgical incidences in man. The costs of surgery were estimated from hospital records and by costing out the procedures each patient received whilst undergoing treatment. After comparing the quality of life of patients treated for CE with that of case-matched controls, it appeared that the treated patients had some long-term morbidity caused either by the disease or the resulting treatment. A simple spreadsheet model was built up, to sum the individual cost items. Each cost item and each of the data related to prevalence and incidence was assigned a mathematical distribution and varied randomly, using Monte-Carlo techniques, throughout its range, over 10 000 simulations. The results of the study indicate that the most likely range of annual economic losses attributable to CE in Jordan (encompassing 95% confidence limits) is from U.S.$2 602 215-6533 661, with a median of U.S.$3 874 070.

Seasonal variations in the abundance of Gasterophilus spp. larvae in donkeys in northern Jordan.

One hundred and five donkeys were examined over a 12-month period for the presence of Gasterophilus spp. larvae in their stomachs. G. intestinalis and G. nasalis were found, but there was a distinct seasonal variation in their abundance. The numbers of second-stage larvae (L2) peaked during the early winter and early summer, but they were absent or at low levels during the early spring and early autumn. This suggests that there are two periods of adult fly activity (late autumn and late spring) for both G. nasalis and G. intestinalis. Third-stage larvae (L3) were found throughout the year, but the lowest levels were seen in the late summer and autumn. The parasites also had an aggregated distribution, which may be due to host selection by the fly. The numbers of larvae did not vary significantly with age, which may be due to a lack of acquired protective immunity or to tolerance after repeated exposure.

Age and seasonal variations in the prevalence of Oestrus ovis larvae among sheep in northern Jordan.

During the period March 1996-July 1997, 417 heads of Awassi sheep slaughtered at the Irbid Abattoir (northern Jordan) were examined for the three larval instars (L1, L2 and L3) of Oestrus ovis. Of the 417 heads, 242 (58%) were infested with O. ovis larvae. Larval numbers were highly aggregated. The lowest number of larvae and the lower quartile were both zero, whilst the median was two and the upper quartile was 12. The highest number of larvae recovered from one head was 151. All three larval instars were observed in each month of the year. July and October had the highest proportions of L1, 75 and 78%, respectively, among infected animals (adjusted for age). The number of larvae increased with age. Infestation with live larvae was associated with inflammatory responses in the upper respiratory tract and with catarrhal or purulent discharge. The percentage of infested sheep and the mean monthly total number of larvae/sheep peaked in the warmer part of the year. Most larvae were L1 except during the spring when L2 and L3 predominated. Distribution analysis demonstrates that the numbers of larvae recovered in the sheep population followed a negative-binomial distribution. Furthermore, the negative-binomial constant k for each month correlated with the monthly prevalence.

Risk factors associated with human cystic echinococcosis in Jordan: results of a case-control study.

The parasites causing cystic echinococcosis (CE) are transmitted to man and domestic animals either directly or indirectly from dogs. High levels of human infection have been frequently described in sheep-rearing areas of the world, where the infection cycles between dogs and sheep through the use of working dogs and the feeding of sheep offal to dogs. A case-control study was undertaken in northern Jordan to examine the epidemiological characteristics of echinococcosis in a Muslim community. Forty-four indigenous Jordanians who had been treated for CE between 1990 and 1996 were contacted and three controls for each case, matched for sex and age, were selected from the Jordanian population. The most important single factor associated with treatment for CE was the main source of domestic water; 42 (95%) of the cases but only 81 (61%) of the controls reported that they used a public, piped, water supply as their principal source of household water [odds ratio (OR) = 13.22; 95% confidence interval (CI) = 2.91-83.7]. The keeping of dogs or close association with dogs or farm animals was not associated with any increased risk of CE. However, individuals who grew their own vegetables had a significantly decreased risk of acquiring CE (OR = 0.30; CI = 0.08-0.98). There was evidence of widespread ignorance of the disease and how it is transmitted.

Prevalence of hydatidosis among donkeys in northern Jordan.

One hundred and thirty donkeys (Equus asinus), aged between 5 months and 14 years of age, from the Irbid Governorate in northern Jordan were necropsied between November 1997-May 1999. Of these animals, 16.9% had hydatid cysts in either their lungs and/or livers. No donkeys of 3 years of age or less were infected, where as 33.3% (22 of 66) aged 4 years or greater were infected. Intensity of infection increased with age in a linear fashion. The prevalence also increased with age approaching an asymptotic prevalence of 1 in the oldest animals. This implied there was minimal regulation of the parasite population by intermediate host immunity. The numbers of cysts in the donkeys were increasing at a rate of 0.48 cysts per year from 0.054 infections. The frequency distribution was highly aggregated, consistent with a negative binomial distribution indicating infection of donkeys was not random.

Prevalence of Surra among camels and horses in Jordan.

The prevalence of Trypanosoma evansi infection among camels and horses in Jordan was studied using thick blood smears and inoculation techniques with mice and rats. A total of 437 camels and 83 horses from four climatic zones were surveyed. In addition, 40 donkeys, 32 cattle and 35 goats in contact with infected camels and horses were also tested in the same way. Clinical disease was evident in 8.2% of the camels (36 out of 437) and in 9.6% of the horses (8 out of 83). Infection was limited only to the Sweama area on the Dead Sea (within the warm desert-climatic zone), with prevalence of 30.5% and 33.3%, respectively, for camels and horses. Donkeys, cattle and goats examined were all free from T. evansi. Clinically affected camels were positive by both, thick blood smear and mouse and rat inoculations. Rat and mouse inoculations revealed (X2 = 3.2, df = 1, exact p = 0.07) greater number of positive cases in horses than those revealed by thick blood smears. T. evansi-infected camels and horses showed all the clinical signs known for Surra. In addition, it was observed that 100% of infected camels stared at the sun.

Modelling the prevalence of Echinococcus and Taenia species in small ruminants of different ages in northern Jordan.

A base-line survey of Echinococcus granulosus, Taenia hydatigena and T ovis were undertaken in order to investigate the transmission dynamics of these parasites in northern Jordan. Intensity of E. granulosus infection, in sheep, increased with age in a linear fashion whilst the asymptotic prevalence was one. This implied that E. granulosus is in an endemic steady state with no evidence of protective immunity in the intermediate host. The mean number of cysts increased by 1.66 per year with approximately 0.320 infections per year, each infection consisting of 598 eggs to produce 5.2 cysts. The basic reproduction ratio (R0) was estimated to be 1.5-1.8. A similar pattern was suggested with E. granulosus in goats but the infection pressure appeared to be lower with only 0.128 cysts per year. Although infection in goats appeared to be endemic there was some evidence of departure from the model which might indicate that the model needs adjusting for this species. In the case of T. hydatigena the host age-intensity helminth distribution indicated that this parasite was hyperendemic in both sheep and goats, implying regulation by intermediate host immunity. Consequently, R0 was determined from asymptotic prevalence curves for T hydatigena and was calculated to be 4.0 and 3.1 in sheep and goats, respectively. The lower R0 in goats, together with the higher asymptotic age-intensity and age-prevalences, indicates that goats acquire immunity more slowly to T hydatigena in comparison to sheep. Taenia ovis was not detected in any animals.

Seroprevalence of brucellosis among high risk people in northern Jordan.

BACKGROUND: Brucellosis is considered the most important zoonosis in Jordan with high prevalence among man and livestock. METHODS: This study was carried out on high risk people in 1992 in order to assess the seroprevalence of brucellosis in northern Jordan. The sera of 1236 individuals (636 at high risk and 600 controls) were evaluated using the Rose Bengal plate agglutination test (RBPT) and enzyme-linked immunosorbent assay (ELISA-IgG) tests. RESULTS: A significantly (P < 0.05) higher seroprevalence of brucellosis among high risk people (8.2 percent) compared to the control sample (0.5 percent) was found. The overall seroprevalence was significantly higher among sheep farmers and meat handlers than in other occupations tested. The seroprevalence increased with age and years at work, but was not influenced by sex or locality. The results indicated a higher seroprevalence among veterinarians in northern Jordan, compared to central Jordan but the difference was not significant. Seroprevalence was present only among veterinarians working in clinics especially in the working age group (34-43 years). CONCLUSION: The results of this study emphasized the importance of contact infections, namely contact with infected animals and their products, as a method of transmission of brucellosis compared to ingestion of contaminated animal products.

Use of dried poultry litter in the diet of pregnant and lactating Awassi ewes.

Two groups of 45 Awassi ewes, were fed a control diet (group C) or a diet containing 0.30 poultry litter from laying birds (group PL). The experiment began when the rams were put with the ewes and continued through pregnancy and lactation. Mean weight changes of ewes of both groups were small and not significantly different. The numbers of ewes that lambed and the numbers of lambs weaned, as proportions of the number of ewes mated, were 0.91 and 0.73 respectively for group C, and 0.93 and 0.70 for group PL. The mean weaning weight of lambs of group C (20.6 kg) was just significantly greater than the value for group PL (18.4 kg) but the estimated mean daily milk yields, 0.716 and 0.626 kg respectively, did not differ significantly. Differences in breeding and lactation performance, between ewes given the control and those given the poultry litter diet, were small for all the data obtained. Also, there was no disease problem related to the use of poultry litter; and the food products milk and cheese, from ewes given poultry litter, were just as acceptable as those from ewes given the control diet.

Some observations on hydatidosis in Jordan.

A total of 2.8% (5 of 176) sera from schoolchildren and university students were seropositive for hydatidosis (Echinococcus granulosus), by the ELISA IgE test. The prevalence of seropositivity was 4.5% among females of all age groups (5-24 years) and among males of the age group 18-24 years. Males of the age group (5-17 years) were seronegative. The ratio of seropositivity between schoolboys and schoolgirls was 1:4. Sera collected from 1085 university students, aged 18-24 years, and from 1656 outpatients from northern and central Jordan, and the Jordan River valley, when tested by the IHA test, revealed the presence of anti-hydatid agglutinating antibodies in 5.16% (56 of 1085) and in 3.6% (60 of 1656) respectively, with a male to female infection ratio of 1:3 in the university students and 1:1.1 in the outpatients. Intensity, prevalence and cyst fertility of E. granulosus increased in sheep with age. The results of this study indicate that hydatidosis is in an endemic steady state in Jordan with estimated economic losses of JD 3.0 (= US $4.4) per infected sheep.

Ophthalmomyiasis externa caused by Oestrus ovis L. in the Ajloun area of northern Jordan.

During the years 1990-1991 17 cases of ophthalmomyiasis externa due to the sheep nasal botfly, Oestrus ovis, were reported from the Ajloun area in northern Jordan. Symptoms included mild to severe conjunctivitis, cellulitis, lacrimation and conjunctival hyperaemia. All cases were among males, and they occurred either from April to July or from September to November.