Abstract
A cross-sectional sero survey of 199 apparently healthy persons from various occupations was carried out in Tanga, Tanzania in November 2004 to investigate exposure to Rift Valley fever (RVF) virus. Sera were tested for the presence of antibodies to RVF virus by the inhibition enzyme-linked immunosorbent assay (ELISA) for detecting immunoglobulin G (IgG). All reactive sera were further tested by the capture ELISA test and specific RVF immunoglobulin M (IgM) assay. Eight (4.0%) tested positive for IgG and none of the samples tested positive for IgM. Among the occupational groups examined, the seroprevalence was 7.3%, 1.5%, and 9.5% in the abattoir workers, livestock keepers, and others categories, respectively. Seropositivity was higher in men (5.3%) than women (1.5 %) and increased markedly in men aged between 20 to 40 years, with no significant differences among the age groups and sexes. The results indicate that a small proportion of people in Tanga municipality were exposed to RVF virus infection prior to 2007 disease outbreak in Tanzania. These findings need to be taken into consideration when future disease control programs are implemented.
Introduction
Previous history of RVF outbreaks in Tanzania, which were confined to mainly livestock and mostly affecting northern parts of Tanzania, were recorded in 1956, 1978–79, and 1997–98 (Kondela et al. 1985, Woods et al. 2002). The recent reemergence (early 2007) of the disease among humans and livestocks, covering nine different geographical regions, and the fact that RVF virus replicates in a wide range of competent mosquito vectors (Turell et al. 2008) have raised concern that the virus might spread further into nonendemic (Tanga, Coast, Mtwara, Ruvuma, Rukwa, Kigoma, Shinyanga) regions of Tanzania. These threats emphasize the need for capable surveillance tools and a sound disease control strategy in place. Unpublished, hospital-based reports from this recent outbreak in Tanzania indicate that RVF claimed 144 deaths and the corresponding case fatality rate was 46.6% (WHO 2007).
RVF is known to be endemic in most of the sub-Saharan countries and in some regions in Tanzania (FAO 2002, FAO/OAU/IBAR/UNDP 2001). Between epidemic waves, RVF virus circulates at very low incidence without noticeable clinical manifestation, in both humans and animals (FAO 2003). Much less is known of the prevalence in man and the effect on human health in this region of the world. Such information is important to envisage when designing appropriate strategies that would help reduce its prevalence and effects. This inadequacy of data, consistent with sera bank collected in 2004, prompted the initiation of this study with a view of establishing past exposure to RVF virus before the 2007 outbreak. The objectives of the present study were to estimate the RVF antibody prevalence in apparent healthy, various occupational risk groups of inhabitants in Tanga Municipality, Tanzania. The overall purpose was to collect baseline data to enhance understanding of the epidemiology of the disease.
Materials and Methods
Study area and population
This cross-sectional field study was conducted in Tanga Municipality, Tanga Region, one of the eight regional districts. The area is located between latitude 4° 21′ and 6° 14′ S, and longitude 36° 11′ and 38° 26′ E, in northeast Tanzania. It has a human population of around 242,640 inhabitants growing at 2.9% per annum (URT 2002). Most rural inhabitants are subsistence farmers, and Tanga town, the regional center, provides many jobs in industry and trade. Tanga Municipality has a hot and humid tropical climate with two rainy seasons: an intense one observed during months of March, April, and May, and a mild one occurring in November and December. The mean annual rainfall varies from 500 to 1400 mm/y. The relative humidity of the day ranges from 60% to 90% for most of the year. Monthly mean temperatures range typically from 15°C between June and August to 35°C between December and March, and the area receive between 2300 to 3100 hours of sunshine a year. Subjects for the study were selected according to the willingness of the individual to be included in the study frame for testing.
Data collection
A pretested individual questionnaire comprising closed-ended questions was administered to obtain demographic (age, gender, location) and occupational data (categorized as “abattoir workers”; “livestock keepers”; “non–livestock keepers”; “veterinary/livestock farmers,” and “others”). The others category comprises people from the general community outside the traditional occupational risk groups (i.e., business people, housewives, students, soldiers, etc.). Other information collected included contact with livestock at home, type of activities engaged with, as well as awareness regarding zoonoses including RVF.
Ethical consideration
In this study, ethical issues were addressed through the following way: confidentiality of laboratory information was maintained and volunteering persons were explained the reason for taking blood samples and further asked for oral/written consent. The ethical approval was obtained from the Human Ethics Committee of the National Institute for Medical Research (NIMR), Dar-es–Salaam, Tanzania.
Laboratory analysis of sera samples
During the year 2004, we collected a total of 199 human (ages between 14 and 84 years) serum samples from urban and periurban areas surrounding Tanga town. The radius was about 30 km of the town center. Serum samples from each individual were then stored at −20°C until further use. Serodiagnosis of RVF was performed using Rift Valley fever Inhibition enzyme-linked immunosorbent assay (ELISA) kit (batch No. 2007/10) obtained from National Institute for Communicable Disease Sandringham, South Africa. Results or cutoff values were expressed as percent inhibition (PI) values using the equation: [(100 − (mean net optical density (OD) of test sample/mean net OD of negative control) × 100]. For ease of interpretation and comparison with other studies, test sera were classified as seropositive if the PI was ≥38.6%. RVF immunoglobulin G (IgG)-positive (past exposure to virus/infection before or during November 2004) samples were subjected to capture ELISA to evaluate the level of anti-RVF immunoglobulin M (IgM) antibodies (which reflect recent infection at least 1 month prior to November 2004) using test kit batch No. 2007/06. Results were expressed as percent positivity (PP) values of optical densities (Paweska et al. 2005), relative to those of a strong positive control serum. Threshold PP values ≥7.1% were considered to be positive and less than these values were considered to be negative.
Statistical analysis
Questionnaire and laboratory data were handled and analyzed using Epi-info (version 6.04) (CDC, Atlanta, GA). The differences in RVF antibody prevalences were compared across the investigated variables using the Mantel-Haenszel chi-square test. A value of p < 0.05 was considered significant. Biostatistical analysis was performed using Epi-info (version 6.04) (CDC).
Results
Two thirds of the sampled people were men and one third were women (Table 1). The majority of the sampled people were between 20 and 50 years old. The overall prevalence of anti RVF virus IgG antibody was 4.02%, and none had IgM antibodies. The seroprevalence of anti-RVF virus immunoglobulin (IgG) antibody was higher in men than in women; however, no significant statistical difference was present (p = 0.34). Seroprevalence increased markedly in men aged between 20 and 40 years (data not shown), and antibodies were not detected in the young population (up to 20 years). Among the occupational groups examined, the seroprevalence was 7.3%, 1.5%, and 9.5% in the abattoir workers, livestock keepers, and others categories, respectively (Table 1), although no statistical difference was found among various occupational groups (p = 0.086). None of the study participants perceived RVF to be a zoonotic disease.
Discussion
There is a paucity of virological and epidemiological investigations pertaining to RVF seroprevalence status in general population and various occupational groups in Tanzania. Overall, 60% of the investigated sera were from people who had contact with cattle, either through cattle-keeping at home or through their occupation like abattoir and veterinary staff, and for 40% of people who had no close contact with cattle, like crop farmers and others. This last group might still have contact with cattle products, like raw meat and milk when preparing or consuming food. Interestingly, the detected seropositive status of the general population before 2007 outbreaks support the endemicity of this disease in Tanzania (Kondela et al. 1985, FAO/OAU/IBAR/UNDP 2001, Woods et al. 2002).
The low reactor rate for women in this study could probably be due to the small number of women (n = 67) studied compared to men (n = 132). Recent RVF outbreak in Tanzania showed that the ratio of male:female mortalities to be1.6:1, and patient aged 16–60 years died more than other age group (MoHSS 2007). The higher proportionate infection rate in men than women agrees with the findings of other workers (Nabeth et al. 2001). Traditionally, the majorities of abattoir and cattle-keeping activities in Tanzania are predominantly carried out by men. This may in part explain the high prevalence rate detected in men and in abattoir workers.
The overall detected prevalence of infection in the present study was lower than many other previous reports in Africa, which reported prevalence of 14.8% (Olaleye et al. 1996) in Nigeria, 24.4% (Nabeth et al. 2001) in Mauritania, and 22.3% in Senegal (Wilson et al. 1994). On the other hand, our prevalence rate was higher than reports made in other places (e.g., 2% reported in pregnant women in Mozambique [Niklasson et al. 1987]). The variability in the prevalence of RVF antibodies between reports could be attributed to difference in sampling techniques, investigator technical know-how, climate-agro-ecological factors, as well as diagnostic methods used.
Tanga Municipality is characterized by hot, humid, and wet climate variables. This climate is thought to permit many and high densities of mosquitoes of veterinary and medical importance (James 1979) and may similarly promote high densities of other biting mosquito species that are potential vectors of RVF virus (i.e., Aedes and Culex [Turell et al. 2007, 2008]). Laboratory-based vector competence and field isolation studies carried out in selected African mosquitoes revealed and suggested Culex zombaensis, Culex poicilipes, Culex pipiens, and Aedes caspius to be possible potential vectors for RVF virus transmission (Turell et al. 2007, 2008, Diallo et al. 2005, Meegan et al. 1980). Aedes and Culex species are known to be prevalent in Tanga; however, the role played by these mosquitoes warrants further investigation (Mboera et al. 2000, Magesa and Kamugisha 2006). As found in other studies, (Wilson et al. 1994, Elfadil et al. 2006, Turell et al. 2007, 2008), presence or exposure to a wide range of mosquito vectors (i.e., Aedes spp.) was associated with the increased likelihood human seroconversion to RVF virus. This would be consistent with RVF virus being transmitted by mosquitoes vectors as well with contact with infected animal parts (tissue, blood, urine, uterine fluid, etc.) during slaughtering (Chevalier et al. 2004, Gerdes 2004) or when assisting the delivery of newborn animals and mechanically by contaminated needles during mass vaccination (FAO 2002).
The finding that none of the participants were aware of RVF as a zoonotic disease is striking, and this is a reflection of the poor knowledge of zoonoses by livestock keepers, veterinary field staff, and staff in the health facilities. Limited knowledge level recorded in this study may be due to the general lack of data on RVF and inadequate communication between veterinary and human health care professionals. This low awareness is likely to expose people to increased risk of contracting RVF, as they might not take proper precaution (i.e., use insecticide-treated bed nets or use protective clothing when dealing with abortion cases and during on-farm activities like slaughtering cattle). For instance, a majority of the abattoir staff were found to have no protective clothing during the current study period. Likewise, the habit of consuming raw milk, raw blood, or raw or undercooked meat, however, is still common practice in some communities in Tanzania (Shirima et al. 2003).This shows that the emergency preparedness for RVF epidemic is low. Consistent with low knowledge on RVF, possibly due to the interepizootic nature of the disease occurrence, the role of vectors and RVF virus transmission in Tanzania is not clearly understood. Further research is required. Consistent with research initiatives, targeted information and education of the population (vet, health staff, community) to increase awareness could help increase early case detection and limit further spread of infection.
Conclusions
From findings of this study, it is concluded that there is a clear evidence of human exposure to RVF virus before 2007 epidemics, with all studied occupational groups being equally at risk of contracting RVF virus.
Considering the paucity of epidemiological reports on RVF in the northeast of Tanzania and the absence of any data concerning factors related to either prevention or the spread of the disease, our results could make a useful contribution toward the prevention of human RVF epidemic in Tanzania.
Footnotes
Acknowledgments
Special thanks go to all individuals who volunteered to donate blood in this study. Health officers in Tanga are thanked for their help during the study period. VIC colleagues are thanked for technical assistance.
Disclosure Statement
This study was self-financed by one of the authors (L.S.).
