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Abstract
Background
Brucellosis is a neglected tropical zoonosis allegedly reemerging in Middle Eastern
countries. Infected ruminants are the primary source of human infection; consequently,
estimates of the frequency of ruminant brucellosis are useful elements for building
effective control strategies. Unfortunately, these estimates are lacking in most Middle
East countries including Egypt. Our objectives are to estimate the frequency of ruminant
brucellosis and to describe its spatial distribution in Kafr El Sheikh Governorate,
Nile Delta, Egypt.
Methodology/Principal Findings
We conducted a cross-sectional study in which 791 sheep, 383 goats, 188 cattle milk
tanks and 173 buffalo milk tanks were randomly selected in 40 villages and tested
for the presence of antibodies against
Brucella spp. The seroprevalence among different species was estimated and visualized using
choropleth maps. A spatial scanning method was used to identify areas with significantly
higher proportions of seropositive flocks and milk tanks. We estimated that 12.2%
of sheep and 11.3% of goats in the study area were seropositive against
Brucella spp. and that 12.2% and 12% of cattle and buffalo milk tanks had antibodies against
Brucella spp. The southern part of the governorate had the highest seroprevalence with significant
spatial clustering of seropositive flocks in the proximity of its capital and around
the main animal markets.
Conclusions/ Significance
Our study revealed that brucellosis is endemic at high levels in all ruminant species
in the study area and questions the efficacy of the control measures in place. The
high intensity of infection transmission among ruminants combined with high livestock
and human density and widespread marketing of unpasteurized milk and dairy products
may explain why Egypt has one of the highest rates of human brucellosis worldwide.
An effective integrated human-animal brucellosis control strategy is urgently needed.
If resources are not sufficient for nationwide implementation, high-risk areas could
be prioritized.
Author Summary
Brucellosis is a zoonosis of mammals caused by bacteria of the genus
Brucella. It is responsible for a vast global burden imposed on human health through disability
and on animal productivity. In humans brucellosis causes a range of flu-like symptoms
and chronic debilitating illness. In livestock brucellosis causes economic losses
as a result of abortion, infertility and decreased milk production. The main routes
for human infection are consumption of contaminated dairy products and contact with
infected ruminants. The control of brucellosis in humans depends on its control in
ruminants, for which accurate estimates of the frequency of infection are very useful,
especially in areas with no previous frequency estimates. We studied the seroprevalence
of brucellosis and its geographic distribution among domestic ruminants in one governorate
of the Nile Delta region, Egypt. In the study area, the seroprevalence of ruminant
brucellosis is very high and has probably increased considerably since the early 1990s.
The disease is widespread but more concentrated around major animal markets. These
findings question the efficacy of the control strategy in place and highlight the
high infection risk for the animal and human populations of the area and the urgent
need for an improved control strategy.
In countries of the Near East region, brucellosis was reported in almost all domestic animals, particularly cattle, sheep and goats. Brucellosis in camels has been reported in Saudi Arabia, Kuwait, Oman, Iraq, Iran, Sudan, Egypt, Libya and Somalia. It has been reported even in racing camels in the United Arab Emirates. In Egypt, brucellosis has been reported also in buffaloes, equines and swine. Brucella melitensis biovar 3 is the most commonly isolated species from animals in Egypt, Jordan, Israel, Tunisia and Turkey. B. melitensis biovar 2 was reported in Turkey and Saudi Arabia, and B. melitensis biovar 1 in Libya, Oman and Israel. B. abortus biovar 1 was reported in Egypt, biovar 2 in Iran, biovar 3 in Iran and Turkey, and biovar 6 in Sudan. The countries with the highest incidence of human brucellosis are Saudi Arabia, Iran, Palestinian Authority, Syria, Jordan and Oman. Bahrain is reported to have zero incidence. Most human cases are caused by B. melitensis, particularly biovar 3. However, B. abortus has been responsible for an increasing number of cases in recent years, e.g. in Yemen, where B. abortus was identified in 45 cases and B. melitensis in 7 cases out of 330 cultures performed in 1995. Concerning control of brucellosis in animals, there is a controversy on the choice of policy. In some countries, the test and slaughter policy together with the vaccination of young females is adopted, in others, particularly with regard to sheep and goats; mass vaccination has been recently started. The most commonly used vaccines are B. abortus S19 and B. melitensis Rev.1 vaccines. B. abortus RB51 vaccine is used in some countries on small scale. Vaccination is limited to cattle and small ruminants. Copyright 2002 Elsevier Science B.V.
The economic aspects of controlling zoonoses are rapidly gaining attention in light of challenges, both well-known and new. Wildlife reservoirs of classical and emerging zoonoses (e.g., bovine tuberculosis) persist in many countries and substantially slow control efforts for livestock ( 1 ). The fast-growing demand for milk and meat in urban centers in resource-limited countries is leading to the intensification of livestock production systems, especially in periurban areas of these countries. However, because efficient zoonosis surveillance and food safety are lacking, the risk for zoonosis transmission is increasing, particularly in rapidly growing urban centers of resource-limited countries ( 2 , 3 ). Many countries in postcommunist transition face a sharp increase in zoonotic diseases resulting from the breakdown of government-run disease surveillance and control and weak private health and veterinary services ( 4 ). Industrialized countries have responded rapidly to recent zoonosis outbreaks and contained them well ( 5 ), but many resource-limited and transitioning countries have not been able to respond adequately because they lack human and financial resources and have not sufficiently adapted public health surveillance. In industrialized countries, an important part of successful zoonosis control has been compensating farmers for culled livestock. However, many resource-limited countries would not be able to conduct such programs. Most zoonoses are maintained in the animal reservoir but can cross over to humans as a result of different risk factors and behavioral traits. For example, brucellosis is transmitted to humans from direct contact with livestock or ingestion of unpasteurized milk or milk products; however, brucellosis is not transmitted from humans to livestock. Hence, elimination of zoonoses such as rabies, echinococcosis, and brucellosis is possible only by interventions that vigorously target animal reservoirs. Control of most zoonoses usually requires interventions outside the public health sector. When one considers health from a point of view independent of species, including humans, domestic animals, and wildlife, zoonoses are part of a broader ecologic concept of health systems ( 6 – 8 ). To attempt control, and possibly elimination, of zoonoses, benefits to public health and society need to be demonstrated, particularly in countries with scarce resources. We present examples from our work on brucellosis and rabies and demonstrate the circumstances for which zoonosis control would save money for resource-limited countries and likely reduce the occurrence of zoonoses worldwide. Avian influenza is discussed as an additional example. Diseases Brucellosis In Mongolia and central Asian countries after democratic reform and the shift from dependence on the former Soviet Union in 1990, human brucellosis reemerged as a major, but preventable, disease ( 9 ). After consultations with experts, the World Health Organization (WHO) raised the question whether mass vaccinations of animals saved money for the public health sector. We used an animal-to-human transmission model to estimate the economic benefit, cost-effectiveness, and distribution of benefit (to society and the public health and agricultural sectors) of mass brucellosis vaccination of cattle and small ruminants ( 10 ). The intervention consisted of a planned 10-year annual livestock mass vaccination campaign using Brucella melitensis Rev-1 for small ruminants and Brucella abortus S19 for cattle. In a scenario of achieving 52% reduction of brucellosis transmission between animals, 51,856 human brucellosis cases could be averted, which would add up to a gain of 49,027 human disability-adjusted life years (DALYs; see Appendix). The human death rate from brucellosis is considered to be 100,000 deaths for the United States alone ( 20 ). To implement disease prevention and control measures, early identification of emerging patterns of disease is necessary and uses economic methods to determine which mix of measures is most cost-effective. Resource-limited countries in Africa are almost devoid of surveillance capacity and efficient early warning systems, which would be crucial. Surveillance of cross-border diseases cannot be restricted to countries that have the funds. High-income countries would ultimately benefit by providing funding for surveillance and control to low-income countries. Comprehensive economic assessment of this issue are, however, lacking so far. Awareness, Knowledge, and Information Many countries, especially those with resource constraints and those in sub-Saharan Africa, lack information on the distribution of zoonotic diseases. Risks for zoonoses are considered negligible compared with those for diseases of higher consequence because the societal consequences of zoonoses are not recognized by the individual sectors. For example, outbreaks of Rift Valley fever in persons in Mauritania were mistakenly identified as yellow fever. The correct diagnosis was made only after public health services contacted livestock services, which informed them of abortions in cattle ( 21 ). In resource-limited and transitioning countries, many zoonoses are not controlled effectively because adequate policies and funding are lacking. However, transmission of zoonoses to humans can already be greatly reduced by health information and behavior. Authorities in Kyrgyz, for example, have started an information campaign to reduce brucellosis transmission to small-ruminant herders by encouraging them to wear gloves for lambing and to boil milk before consuming. Interventions in livestock should always be accompanied by mass information, education, and communication programs. Financing Substantial evidence documents that the combined effects of human disease caused by zoonoses, as part of the neglected infectious diseases, are in the same range as the classical diseases of poverty such as HIV/AIDS, tuberculosis, and malaria ( 22 , 23 ). On the other hand, the public health component justifies including zoonoses such as bovine tuberculoses in current global programs and initiatives on tuberculosis control ( 22 , 23 ). Recognition of these facts should result in affected countries applying for funds from the Global Fund to Fight AIDS, Tuberculosis and Malaria ( 24 ). Surveillance and control of cross-border zoonotic diseases such as highly pathogenic avian influenza cannot be restricted to wealthy countries. According to Vallat, “One country not able to carry out early detection and rapid response to animal disease outbreaks can represent a threat to all the others” ( 25 ). To approach these threats, new partnerships (e.g., between resource-limited and industrial countries, public and private sectors, and animal and public health) and permanent dialogue are needed. “It is evident that the interest of the rich countries is to support the others in order to protect themselves” ( 25 ). Zoonosis control in general should thus be seen from a global perspective and lead to a call for a global subsidiary approach for control. International bodies like the World Organization for Animal Health, the Food and Agriculture Organization, and WHO should foster establishment of global standards for zoonosis surveillance and control. Fostering of global standards is also part of the WHO International Health Regulations that will come into force in mid-2007 and will require all countries to do a better job of surveillance for diseases that can spread between countries (www.int/gb/edwha/pdf_files/WHA58-REC1/english/Resolutions.pdf). These efforts should lead to a global fund for the control of zoonoses or become a component of an extended Global Fund to Fight AIDS, Tuberculosis and Malaria. Such a joint facility would allow coherent and integrated control approaches, particularly in the countries with the most serious resources constraints, which in turn would benefit the whole world. Conclusion Zoonoses are among the most important animal and public health problems that affect the well-being of societies worldwide, yet they are too often forgotten or neglected. Because most zoonoses go unrecorded, they call for a rethinking of research and control efforts and the economic consequences. The example of brucellosis demonstrates that interventions in livestock against zoonoses, which would never be cost-effective when uniquely assessed from a public health sector point of view, may become cost-saving when considered from a societal perspective. Creating a new global finance facility for the control of zoonoses, similar to or linked with the Global Fund to Fight AIDS, Tuberculosis and Malaria, is timely, is of global interest, and represents a further contribution to successful attainment of the Millennium Development Goals.
To measure the incidence of typhoid fever and other febrile illnesses in Bilbeis District, Egypt, we conducted a household survey to determine patterns of health seeking among persons with fever. Then we established surveillance for 4 months among a representative sample of health providers who saw febrile patients. Health providers collected epidemiologic information and blood (for culture and serologic testing) from eligible patients. After adjusting for the provider sampling scheme, test sensitivity, and seasonality, we estimated that the incidence of typhoid fever was 13/100,000 persons per year and the incidence of brucellosis was 18/100,000 persons per year in the district. This surveillance tool could have wide applications for surveillance for febrile illness in developing countries.
Conceived and designed the experiments: YMH AR JG. Performed the experiments: YMH
AM SO. Analyzed the data: YMH AR JG. Contributed reagents/materials/analysis tools:
YMH AM SO. Wrote the paper: YMH AR JG.
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