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1.  Causes of death in the Taabo health and demographic surveillance system, Côte d'Ivoire, from 2009 to 2011 
Global Health Action  2015;8:10.3402/gha.v8.27271.
Current vital statistics from governmental institutions in Côte d'Ivoire are incomplete. This problem is particularly notable for remote rural areas that have limited access to the health system.
To record all deaths from 2009 to 2011 and to identify the leading causes of death in the Taabo health and demographic surveillance system (HDSS) in south-central Côte d'Ivoire.
Deaths recorded in the first 3 years of operation of the Taabo HDSS were investigated by verbal autopsy (VA), using the InterVA-4 model. InterVA-4 is based on the World Health Organization 2012 VA tool in terms of input indicators and categories of causes of death.
Overall, 948 deaths were recorded, of which 236 (24.9%) had incomplete VA data. Among the 712 deaths analyzed, communicable diseases represented the leading causes (58.9%), with most deaths attributed to malaria (n=129), acute respiratory tract infections (n=110), HIV/AIDS (n=80), and pulmonary tuberculosis (n=46). Non-communicable diseases accounted for 18.9% of the deaths and included mainly acute abdomen (n=38), unspecified cardiac diseases (n=15), and digestive neoplasms (n=13). Maternal and neonatal conditions accounted for 8.3% of deaths, primarily pneumonia (n=19) and birth asphyxia (n=16) in newborns. Among the 3.8% of deaths linked to trauma and injury, the main causes were assault (n=6), accidental drowning (n=4), contact with venomous plants/animals (n=4), and traffic-related accidents (n=4). No clear causes were determined in 10.0% of the analyzed deaths.
Communicable diseases remain the predominant cause of death in rural Côte d'Ivoire. Based on these findings, measures are now being implemented in the Taabo HDSS. It will be interesting to monitor patterns of mortality and causes of death in the face of rapid demographic and epidemiological transitions in this part of West Africa.
PMCID: PMC4426287  PMID: 25959772
mortality; cause of death; verbal autopsy; InterVA-4; health and demographic surveillance system; Côte d'Ivoire
2.  Source Tracking Mycobacterium ulcerans Infections in the Ashanti Region, Ghana 
PLoS Neglected Tropical Diseases  2015;9(1):e0003437.
Although several studies have associated Mycobacterium ulcerans (MU) infection, Buruli ulcer (BU), with slow moving water bodies, there is still no definite mode of transmission. Ecological and transmission studies suggest Variable Number Tandem Repeat (VNTR) typing as a useful tool to differentiate MU strains from other Mycolactone Producing Mycobacteria (MPM). Deciphering the genetic relatedness of clinical and environmental isolates is seminal to determining reservoirs, vectors and transmission routes. In this study, we attempted to source-track MU infections to specific water bodies by matching VNTR profiles of MU in human samples to those in the environment. Environmental samples were collected from 10 water bodies in four BU endemic communities in the Ashanti region, Ghana. Four VNTR loci in MU Agy99 genome, were used to genotype environmental MU ecovars, and those from 14 confirmed BU patients within the same study area. Length polymorphism was confirmed with sequencing. MU was present in the 3 different types of water bodies, but significantly higher in biofilm samples. Four MU genotypes, designated W, X, Y and Z, were typed in both human and environmental samples. Other reported genotypes were only found in water bodies. Animal trapping identified 1 mouse with lesion characteristic of BU, which was confirmed as MU infection. Our findings suggest that patients may have been infected from community associated water bodies. Further, we present evidence that small mammals within endemic communities could be susceptible to MU infections. M. ulcerans transmission could involve several routes where humans have contact with risk environments, which may be further compounded by water bodies acting as vehicles for disseminating strains.
Author Summary
Buruli ulcer is a skin disease, which is endemic in over thirty countries, mostly in West Africa, with affected populations being largely rural. The causative organism, Mycobacterium ulcerans (MU), is an environmental mycobacterium and although transmission is unclear, frequent exposure to these MU-contaminated environments have been suggested as risk factors. We conducted this study on the premise that if patients are infected from MU-contaminated water bodies, then the genotype of MU strains in these patients should be identical to those in their community associated water bodies and wetlands. Using Variable Number Tandem Repeat (VNTR) as a genetic tool, we determined the genotypes of MU from both water bodies and patient samples. Comparison and overlap of these genotypes, within each community, suggest that patients were possibly infected from at least one water body. Additionally, we present evidence that small mammals within endemic communities could be susceptible to MU infections and may be acting as reservoirs. Our findings suggest that future ecological and molecular studies in the hope of elucidating a definite transmission route, should focus on source-tracking MU infections to community associated risk environments while employing a OneHealth approach in the process.
PMCID: PMC4303273  PMID: 25612300
3.  Diversity and prevalence of gastrointestinal parasites in seven non-human primates of the Taï National Park, Côte d’Ivoire 
Parasite  2015;22:1.
Parasites and infectious diseases are well-known threats to primate populations. The main objective of this study was to provide baseline data on fecal parasites in the cercopithecid monkeys inhabiting Côte d’Ivoire’s Taï National Park. Seven of eight cercopithecid species present in the park were sampled: Cercopithecus diana, Cercopithecus campbelli, Cercopithecus petaurista, Procolobus badius, Procolobus verus, Colobus polykomos, and Cercocebus atys. We collected 3142 monkey stool samples between November 2009 and December 2010. Stool samples were processed by direct wet mount examination, formalin-ethyl acetate concentration, and MIF (merthiolate, iodine, formalin) concentration methods. Slides were examined under microscope and parasite identification was based on the morphology of cysts, eggs, and adult worms. A total of 23 species of parasites was recovered including 9 protozoa (Entamoeba coli, Entamoeba histolytica/dispar, Entamoeba hartmanni, Endolimax nana, Iodamoeba butschlii, Chilomastix mesnili, Giardia sp., Balantidium coli, and Blastocystis sp.), 13 nematodes (Oesophagostomum sp., Ancylostoma sp., Anatrichosoma sp., Capillariidae Gen. sp. 1, Capillariidae Gen. sp. 2, Chitwoodspirura sp., Subulura sp., spirurids [cf Protospirura muricola], Ternidens sp., Strongyloides sp., Trichostrongylus sp., and Trichuris sp.), and 1 trematode (Dicrocoelium sp.). Diversity indices and parasite richness were high for all monkey taxa, but C. diana, C. petaurista, C. atys, and C. campbelli exhibited a greater diversity of parasite species and a more equitable distribution. The parasitological data reported are the first available for these cercopithecid species within Taï National Park.
PMCID: PMC4306024  PMID: 25619957
Gastrointestinal parasites; Non-human primates; Prevalence; Côte d’Ivoire
4.  Long-term trends in Anopheles gambiae insecticide resistance in Côte d’Ivoire 
Parasites & Vectors  2014;7:500.
Malaria control is heavily dependent on the use of insecticides that target adult mosquito vectors via insecticide treated nets (ITNs) or indoor residual spraying (IRS). Four classes of insecticide are approved for IRS but only pyrethroids are available for ITNs. The rapid rise in insecticide resistance in African malaria vectors has raised alarms about the sustainability of existing malaria control activities. This problem might be particularly acute in Côte d’Ivoire where resistance to all four insecticide classes has recently been recorded. Here we investigate temporal trends in insecticide resistance across the ecological zones of Côte d’Ivoire to determine whether apparent pan-African patterns of increasing resistance are detectable and consistent across insecticides and areas.
We combined data on insecticide resistance from a literature review, and bioassays conducted on field-caught Anopheles gambiae mosquitoes for the four WHO-approved insecticide classes for ITN/IRS. The data were then mapped using Geographical Information Systems (GIS) and the IR mapper tool to provide spatial and temporal distribution data on insecticide resistance in An. gambiae sensu lato from Côte d’Ivoire between 1993 and 2014.
Bioassay mortality decreased over time for all insecticide classes, though with significant spatiotemporal variation, such that stronger declines were observed in the southern ecological zone for DDT and pyrethroids than in the central zone, but with an apparently opposite effect for the carbamate and organophosphate. Variation in relative abundance of the molecular forms, coupled with dramatic increase in kdr 1014F frequency in M forms (An. coluzzii) seems likely to be a contributory factor to these patterns. Although records of resistance across insecticide classes have become more common, the number of classes tested in studies has also increased, precluding a conclusion that multiple resistance has also increased.
Our analyses attempted synthesis of 22 years of bioassay data from Côte d’Ivoire, and despite a number of caveats and potentially confounding variables, suggest significant but spatially-variable temporal trends in insecticide resistance. In the light of such spatio-temporal dynamics, regular, systematic and spatially-expanded monitoring is warranted to provide accurate information on insecticide resistance for control programme management.
Electronic supplementary material
The online version of this article (doi:10.1186/s13071-014-0500-z) contains supplementary material, which is available to authorized users.
PMCID: PMC4269959  PMID: 25429888
Malaria intervention; Pyrethroid; Carbamate; Organochlorine; Organophosphate; Multiple resistance; kdr
5.  Mortality from external causes in Africa and Asia: evidence from INDEPTH Health and Demographic Surveillance System Sites 
Global Health Action  2014;7:10.3402/gha.v7.25366.
Mortality from external causes, of all kinds, is an important component of overall mortality on a global basis. However, these deaths, like others in Africa and Asia, are often not counted or documented on an individual basis. Overviews of the state of external cause mortality in Africa and Asia are therefore based on uncertain information. The INDEPTH Network maintains longitudinal surveillance, including cause of death, at population sites across Africa and Asia, which offers important opportunities to document external cause mortality at the population level across a range of settings.
To describe patterns of mortality from external causes at INDEPTH Network sites across Africa and Asia, according to the WHO 2012 verbal autopsy (VA) cause categories.
All deaths at INDEPTH sites are routinely registered and followed up with VA interviews. For this study, VA archives were transformed into the WHO 2012 VA standard format and processed using the InterVA-4 model to assign cause of death. Routine surveillance data also provide person-time denominators for mortality rates.
A total of 5,884 deaths due to external causes were documented over 11,828,253 person-years. Approximately one-quarter of those deaths were to children younger than 15 years. Causes of death were dominated by childhood drowning in Bangladesh, and by transport-related deaths and intentional injuries elsewhere. Detailed mortality rates are presented by cause of death, age group, and sex.
The patterns of external cause mortality found here generally corresponded with expectations and other sources of information, but they fill some important gaps in population-based mortality data. They provide an important source of information to inform potentially preventive intervention designs.
PMCID: PMC4220124  PMID: 25377327
external causes; accidents; suicide; assault; transport; drowning; Africa; Asia; mortality; INDEPTH Network; verbal autopsy; InterVA
6.  Cause-specific childhood mortality in Africa and Asia: evidence from INDEPTH health and demographic surveillance system sites 
Global Health Action  2014;7:10.3402/gha.v7.25363.
Childhood mortality, particularly in the first 5 years of life, is a major global concern and the target of Millennium Development Goal 4. Although the majority of childhood deaths occur in Africa and Asia, these are also the regions where such deaths are least likely to be registered. The INDEPTH Network works to alleviate this problem by collating detailed individual data from defined Health and Demographic Surveillance sites. By registering deaths and carrying out verbal autopsies to determine cause of death across many such sites, using standardised methods, the Network seeks to generate population-based mortality statistics that are not otherwise available.
To present a description of cause-specific mortality rates and fractions over the first 15 years of life as documented by INDEPTH Network sites in sub-Saharan Africa and south-east Asia.
All childhood deaths at INDEPTH sites are routinely registered and followed up with verbal autopsy (VA) interviews. For this study, VA archives were transformed into the WHO 2012 VA standard format and processed using the InterVA-4 model to assign cause of death. Routine surveillance data also provided person-time denominators for mortality rates. Cause-specific mortality rates and cause-specific mortality fractions are presented according to WHO 2012 VA cause groups for neonatal, infant, 1–4 year and 5–14 year age groups.
A total of 28,751 childhood deaths were documented during 4,387,824 person-years over 18 sites. Infant mortality ranged from 11 to 78 per 1,000 live births, with under-5 mortality from 15 to 152 per 1,000 live births. Sites in Vietnam and Kenya accounted for the lowest and highest mortality rates reported.
Many children continue to die from relatively preventable causes, particularly in areas with high rates of malaria and HIV/AIDS. Neonatal mortality persists at relatively high, and perhaps sometimes under-documented, rates. External causes of death are a significant childhood problem in some settings.
PMCID: PMC4220125  PMID: 25377325
Childhood; Africa; Asia; mortality; INDEPTH Network; verbal autopsy; InterVA
7.  Cause-specific mortality in Africa and Asia: evidence from INDEPTH health and demographic surveillance system sites 
Global Health Action  2014;7:10.3402/gha.v7.25362.
Because most deaths in Africa and Asia are not well documented, estimates of mortality are often made using scanty data. The INDEPTH Network works to alleviate this problem by collating detailed individual data from defined Health and Demographic Surveillance sites. By registering all deaths over time and carrying out verbal autopsies to determine cause of death across many such sites, using standardised methods, the Network seeks to generate population-based mortality statistics that are not otherwise available.
To build a large standardised mortality database from African and Asian sites, detailing the relevant methods, and use it to describe cause-specific mortality patterns.
Individual demographic and verbal autopsy (VA) data from 22 INDEPTH sites were collated into a standardised database. The INDEPTH 2013 population was used for standardisation. The WHO 2012 VA standard and the InterVA-4 model were used for assigning cause of death.
A total of 111,910 deaths occurring over 12,204,043 person-years (accumulated between 1992 and 2012) were registered across the 22 sites, and for 98,429 of these deaths (88.0%) verbal autopsies were successfully completed. There was considerable variation in all-cause mortality between sites, with most of the differences being accounted for by variations in infectious causes as a proportion of all deaths.
This dataset documents individual deaths across Africa and Asia in a standardised way, and on an unprecedented scale. While INDEPTH sites are not constructed to constitute a representative sample, and VA may not be the ideal method of determining cause of death, nevertheless these findings represent detailed mortality patterns for parts of the world that are severely under-served in terms of measuring mortality. Further papers explore details of mortality patterns among children and specifically for NCDs, external causes, pregnancy-related mortality, malaria, and HIV/AIDS. Comparisons will also be made where possible with other findings on mortality in the same regions. Findings presented here and in accompanying papers support the need for continued work towards much wider implementation of universal civil registration of deaths by cause on a worldwide basis.
PMCID: PMC4220126  PMID: 25377324
mortality; cause of death; Africa; Asia; verbal autopsy; INDEPTH Network
8.  Adult non-communicable disease mortality in Africa and Asia: evidence from INDEPTH Health and Demographic Surveillance System sites 
Global Health Action  2014;7:10.3402/gha.v7.25365.
Mortality from non-communicable diseases (NCDs) is a major global issue, as other categories of mortality have diminished and life expectancy has increased. The World Health Organization's Member States have called for a 25% reduction in premature NCD mortality by 2025, which can only be achieved by substantial reductions in risk factors and improvements in the management of chronic conditions. A high burden of NCD mortality among much older people, who have survived other hazards, is inevitable. The INDEPTH Network collects detailed individual data within defined Health and Demographic Surveillance sites. By registering deaths and carrying out verbal autopsies to determine cause of death across many such sites, using standardised methods, the Network seeks to generate population-based mortality statistics that are not otherwise available.
To describe patterns of adult NCD mortality from INDEPTH Network sites across Africa and Asia, according to the WHO 2012 verbal autopsy (VA) cause categories, with separate consideration of premature (15–64 years) and older (65+ years) NCD mortality.
All adult deaths at INDEPTH sites are routinely registered and followed up with VA interviews. For this study, VA archives were transformed into the WHO 2012 VA standard format and processed using the InterVA-4 model to assign cause of death. Routine surveillance data also provide person-time denominators for mortality rates.
A total of 80,726 adult (over 15 years) deaths were documented over 7,423,497 person-years of observation. NCDs were attributed as the cause for 35.6% of these deaths. Slightly less than half of adult NCD deaths occurred in the 15–64 age group. Detailed results are presented by age and sex for leading causes of NCD mortality. Per-site rates of NCD mortality were significantly correlated with rates of HIV/AIDS-related mortality.
These findings present important evidence on the distribution of NCD mortality across a wide range of African and Asian settings. This comes against a background of global concern about the burden of NCD mortality, especially among adults aged under 70, and provides an important baseline for future work.
PMCID: PMC4220128  PMID: 25377326
adults; non-communicable disease; Africa; Asia; mortality; INDEPTH Network; verbal autopsy; InterVA
9.  Malaria mortality in Africa and Asia: evidence from INDEPTH health and demographic surveillance system sites 
Global Health Action  2014;7:10.3402/gha.v7.25369.
Malaria continues to be a major cause of infectious disease mortality in tropical regions. However, deaths from malaria are most often not individually documented, and as a result overall understanding of malaria epidemiology is inadequate. INDEPTH Network members maintain population surveillance in Health and Demographic Surveillance System sites across Africa and Asia, in which individual deaths are followed up with verbal autopsies.
To present patterns of malaria mortality determined by verbal autopsy from INDEPTH sites across Africa and Asia, comparing these findings with other relevant information on malaria in the same regions.
From a database covering 111,910 deaths over 12,204,043 person-years in 22 sites, in which verbal autopsy data were handled according to the WHO 2012 standard and processed using the InterVA-4 model, over 6,000 deaths were attributed to malaria. The overall period covered was 1992–2012, but two-thirds of the observations related to 2006–2012. These deaths were analysed by site, time period, age group and sex to investigate epidemiological differences in malaria mortality.
Rates of malaria mortality varied by 1:10,000 across the sites, with generally low rates in Asia (one site recording no malaria deaths over 0.5 million person-years) and some of the highest rates in West Africa (Nouna, Burkina Faso: 2.47 per 1,000 person-years). Childhood malaria mortality rates were strongly correlated with Malaria Atlas Project estimates of Plasmodium falciparum parasite rates for the same locations. Adult malaria mortality rates, while lower than corresponding childhood rates, were strongly correlated with childhood rates at the site level.
The wide variations observed in malaria mortality, which were nevertheless consistent with various other estimates, suggest that population-based registration of deaths using verbal autopsy is a useful approach to understanding the details of malaria epidemiology.
PMCID: PMC4220130  PMID: 25377329
malaria; Africa; Asia; mortality; INDEPTH Network; verbal autopsy; InterVA
10.  HIV/AIDS-related mortality in Africa and Asia: evidence from INDEPTH health and demographic surveillance system sites 
Global Health Action  2014;7:10.3402/gha.v7.25370.
As the HIV/AIDS pandemic has evolved over recent decades, Africa has been the most affected region, even though a large proportion of HIV/AIDS deaths have not been documented at the individual level. Systematic application of verbal autopsy (VA) methods in defined populations provides an opportunity to assess the mortality burden of the pandemic from individual data.
To present standardised comparisons of HIV/AIDS-related mortality at sites across Africa and Asia, including closely related causes of death such as pulmonary tuberculosis (PTB) and pneumonia.
Deaths related to HIV/AIDS were extracted from individual demographic and VA data from 22 INDEPTH sites across Africa and Asia. VA data were standardised to WHO 2012 standard causes of death assigned using the InterVA-4 model. Between-site comparisons of mortality rates were standardised using the INDEPTH 2013 standard population.
The dataset covered a total of 10,773 deaths attributed to HIV/AIDS, observed over 12,204,043 person-years. HIV/AIDS-related mortality fractions and mortality rates varied widely across Africa and Asia, with highest burdens in eastern and southern Africa, and lowest burdens in Asia. There was evidence of rapidly declining rates at the sites with the heaviest burdens. HIV/AIDS mortality was also strongly related to PTB mortality. On a country basis, there were strong similarities between HIV/AIDS mortality rates at INDEPTH sites and those derived from modelled estimates.
Measuring HIV/AIDS-related mortality continues to be a challenging issue, all the more so as anti-retroviral treatment programmes alleviate mortality risks. The congruence between these results and other estimates adds plausibility to both approaches. These data, covering some of the highest mortality observed during the pandemic, will be an important baseline for understanding the future decline of HIV/AIDS.
PMCID: PMC4220131  PMID: 25377330
HIV/AIDS; tuberculosis; Africa; Asia; Mortality; INDEPTH Network; Verbal Autopsy; InterVA
11.  Pregnancy-related mortality in Africa and Asia: evidence from INDEPTH Health and Demographic Surveillance System sites 
Global Health Action  2014;7:10.3402/gha.v7.25368.
Women continue to die in unacceptably large numbers around the world as a result of pregnancy, particularly in sub-Saharan Africa and Asia. Part of the problem is a lack of accurate, population-based information characterising the issues and informing solutions. Population surveillance sites, such as those operated within the INDEPTH Network, have the potential to contribute to bridging the information gaps.
To describe patterns of pregnancy-related mortality at INDEPTH Network Health and Demographic Surveillance System sites in sub-Saharan Africa and southeast Asia in terms of maternal mortality ratio (MMR) and cause-specific mortality rates.
Data on individual deaths among women of reproductive age (WRA) (15–49) resident in INDEPTH sites were collated into a standardised database using the INDEPTH 2013 population standard, the WHO 2012 verbal autopsy (VA) standard, and the InterVA model for assigning cause of death.
These analyses are based on reports from 14 INDEPTH sites, covering 14,198 deaths among WRA over 2,595,605 person-years observed. MMRs varied between 128 and 461 per 100,000 live births, while maternal mortality rates ranged from 0.11 to 0.74 per 1,000 person-years. Detailed rates per cause are tabulated, including analyses of direct maternal, indirect maternal, and incidental pregnancy-related deaths across the 14 sites.
As expected, these findings confirmed unacceptably high continuing levels of maternal mortality. However, they also demonstrate the effectiveness of INDEPTH sites and of the VA methods applied to arrive at measurements of maternal mortality that are essential for planning effective solutions and monitoring programmatic impacts.
PMCID: PMC4220143  PMID: 25377328
maternal mortality; cause of death; Africa; Asia; verbal autopsy; INDEPTH Network
12.  Ecohealth Approach to Urban Waste Management: Exposure to Environmental Pollutants and Health Risks in Yamoussoukro, Côte d’Ivoire 
Poor waste management is a key driver of ill-health in urban settlements of developing countries. The current study aimed at assessing environmental and human health risks related to urban waste management in Yamoussoukro, the political capital of Côte d’Ivoire. We undertook trans-disciplinary research within an Ecohealth approach, comprised of a participatory workshop with stakeholders and mapping of exposure patterns. A total of 492 randomly selected households participated in a cross-sectional survey. Waste deposit sites were characterised and 108 wastewater samples were subjected to laboratory examinations. The physico-chemical parameters of the surface water (temperature, pH, conductivity, potential oxidise reduction, BOD5, COD, dissolved oxygen, nitrates, ammonia and total Kendal nitrogen) did not comply with World Health Organization standards of surface water quality. Questionnaire results showed that malaria was the most commonly reported disease. Diarrhoea and malaria were associated with poor sanitation. Households having dry latrines had a higher risk of diarrhoea (odds ratio (OR) = 1.8, 95% confidence interval (CI) 1.2–2.7) compared to latrines with septic tanks and also a higher risk for malaria (OR = 1.9, 95% (CI) 1.1–3.3). Our research showed that combining health and environmental assessments enables a deeper understanding of environmental threats and disease burdens linked to poor waste management. Further study should investigate the sanitation strategy aspects that could reduce the environmental and health risks in the study area.
PMCID: PMC4210979  PMID: 25279545
Ecohealth; risk factor; waste management; wastewater; tropical diseases; Côte d’Ivoire
13.  Genotyping Tools for Mycobacterium ulcerans-Drawbacks and Future Prospects 
Mycobacterium ulcerans infection (Buruli ulcer) is a neglected but treatable skin disease endemic in over 30 countries. M. ulcerans is an environmental mycobacteria with an elusive mode of transmission to humans. Ecological and Molecular epidemiological studies to identify reservoirs and transmission vectors are important for source tracking infections especially during outbreaks and elucidating transmission routes. Research efforts have therefore focused on genotyping strains of the mycobacteria from clinical and environmental samples. This review discusses genotyping tools for differentiating M. ulcerans strains from other environmental and Mycolactone Producing Mycobacteria (MPMs). We highlight tools that have been adapted from related fields and propose ways these could be enhanced to resolve intra-species variation for epidemiological, transmission, evolutionary studies, and detection of emerging drug resistant strains. In the wake of increasing cases of Buruli ulcer, cumulative efforts including improvement in diagnostic methods and fine-tuning of genotyping tools are crucial to complement public health efforts in reducing infections.
PMCID: PMC4040416  PMID: 24900947
14.  The INDEPTH standard population for low- and middle-income countries, 2013 
Global Health Action  2014;7:10.3402/gha.v7.23286.
Crude rates such as the crude death rate are functions of both the age-specific rates and the age composition of a population. However, differences in the age structure between two populations or two time periods can result in specious differences in the corresponding crude rates making direct comparisons between populations or across time inappropriate. Therefore, when comparing crude rates between populations, it is desirable to eliminate or minimize the influence of age composition. This task is accomplished by using a standard age structure yielding an age-standardized rate. This paper proposes an updated International Network for the Demographic Evaluation of Populations and Their Health (INDEPTH) standard for use in low- and middle-income countries (LMICs) based on newly available data from the health and demographic surveillance system site members of the INDEPTH network located throughout Africa and southern Asia. The updated INDEPTH standard should better reflect the age structure of LMICs and result in more accurate health indicators and demographic rates. We demonstrate use of the new INDEPTH standard along with several existing ‘world’ standards and show how resulting age-standardized crude deaths rates differ when using the various standard age compositions.
PMCID: PMC3969509  PMID: 24679543
crude death rate; age-specific mortality rate; age-standardized crude death rate; demography; standardized age structure; low- and middle-income countries
15.  Potential Risk of Regional Disease Spread in West Africa through Cross-Border Cattle Trade 
PLoS ONE  2013;8(10):e75570.
Transboundary animal movements facilitate the spread of pathogens across large distances. Cross-border cattle trade is of economic and cultural importance in West Africa. This study explores the potential disease risk resulting from large-scale, cross-border cattle trade between Togo, Burkina Faso, Ghana, Benin, and Nigeria for the first time.
Methods and Principal Findings
A questionnaire-based survey of livestock movements of 226 cattle traders was conducted in the 9 biggest cattle markets of northern Togo in February-March 2012. More than half of the traders (53.5%) operated in at least one other country. Animal flows were stochastically simulated based on reported movements and the risk of regional disease spread assessed. More than three quarters (79.2%, range: 78.1–80.0%) of cattle flowing into the market system originated from other countries. Through the cattle market system of northern Togo, non-neighbouring countries were connected via potential routes for disease spread. Even for diseases with low transmissibility and low prevalence in a given country, there was a high risk of disease introduction into other countries.
By stochastically simulating data collected by interviewing cattle traders in northern Togo, this study identifies potential risks for regional disease spread in West Africa through cross-border cattle trade. The findings highlight that surveillance for emerging infectious diseases as well as control activities targeting endemic diseases in West Africa are likely to be ineffective if only conducted at a national level. A regional approach to disease surveillance, prevention and control is essential.
PMCID: PMC3794041  PMID: 24130721
16.  Epidemiology of Brucellosis and Q Fever in Linked Human and Animal Populations in Northern Togo 
PLoS ONE  2013;8(8):e71501.
Although brucellosis (Brucella spp.) and Q Fever (Coxiella burnetii) are zoonoses of global importance, very little high quality data are available from West Africa.
Methods/Principal Findings
A serosurvey was conducted in Togo’s main livestock-raising zone in 2011 in 25 randomly selected villages, including 683 people, 596 cattle, 465 sheep and 221 goats. Additionally, 464 transhumant cattle from Burkina Faso were sampled in 2012. The serological analyses performed were the Rose Bengal Test and ELISA for brucellosis and ELISA and the immunofluorescence assay (IFA) for Q Fever Brucellosis did not appear to pose a major human health problem in the study zone, with only 7 seropositive participants. B. abortus was isolated from 3 bovine hygroma samples, and is likely to be the predominant circulating strain. This may explain the observed seropositivity amongst village cattle (9.2%, 95%CI:4.3–18.6%) and transhumant cattle (7.3%, 95%CI:3.5–14.7%), with an absence of seropositive small ruminants. Exposure of livestock and people to C. burnetii was common, potentially influenced by cultural factors. People of Fulani ethnicity had greater livestock contact and a significantly higher seroprevalence than other ethnic groups (Fulani: 45.5%, 95%CI:37.7–53.6%; non-Fulani: 27.1%, 95%CI:20.6–34.7%). Appropriate diagnostic test cut-off values in endemic settings requires further investigation. Both brucellosis and Q Fever appeared to impact on livestock production. Seropositive cows were more likely to have aborted a foetus during the previous year than seronegative cows, when adjusted for age. This odds was 3.8 times higher (95%CI: 1.2–12.1) for brucellosis and 6.7 times higher (95%CI: 1.3–34.8) for Q Fever.
This is the first epidemiological study of zoonoses in Togo in linked human and animal populations, providing much needed data for West Africa. Exposure to Brucella and C. burnetii is common but further research is needed into the clinical and economic impact.
PMCID: PMC3741174  PMID: 23951177
17.  Effects of Hygiene and Defecation Behavior on Helminths and Intestinal Protozoa Infections in Taabo, Côte d’Ivoire 
PLoS ONE  2013;8(6):e65722.
More than 1 billion people are currently infected with soil-transmitted helminths and schistosomes. The global strategy to control helminthiases is the regular administration of anthelmintic drugs to at-risk populations. However, rapid re-infection occurs in areas where hygiene, access to clean water, and sanitation are inadequate.
In July 2011, inhabitants from two villages and seven hamlets of the Taabo health demographic surveillance system in south-central Côte d’Ivoire provided stool and urine samples. Kato-Katz and ether-concentration methods were used for the diagnosis of Schistosoma mansoni, soil-transmitted helminths (Ascaris lumbricoides, Trichuris trichiura, and hookworm), and intestinal protozoa. Urine samples were subjected to a filtration method for the diagnosis of Schistosoma haematobium. A questionnaire was administered to households to obtain information on knowledge, attitude, practice, and beliefs in relation to hygiene, sanitation, and defecation behavior. Logistic regression models were employed to assess for associations between questionnaire data and parasitic infections.
Principal Findings
A total of 1,894 participants had complete data records. Parasitological examinations revealed prevalences of hookworm, S. haematobium, T. trichiura, S. mansoni, and A. lumbricoides of 33.5%, 7.0%, 1.6%, 1.3% and 0.8%, respectively. Giardia intestinalis and Entamoeba histolytica/E. dispar were detected in 15.0% and 14.4% of the participants, respectively. Only one out of five households reported the presence of a latrine, and hence, open defecation was common. Logistic regression analysis revealed that age, sex, socioeconomic status, hygiene, and defecation behavior are determinants for helminths and intestinal protozoa infections.
We found that inadequate sanitation and hygiene behavior are associated with soil-transmitted helminths and intestinal protozoa infections in the Taabo area of south-central Côte d’Ivoire. Our data will serve as a benchmark to monitor the effect of community-led total sanitation and hygiene education to reduce the transmission of helminthiases and intestinal protozoa infections.
PMCID: PMC3688730  PMID: 23840358
18.  An analysis of interprovincial migration in Vietnam from 1989 to 2009 
Global Health Action  2012;5:10.3402/gha.v5i0.9334.
In Vietnam, reports either present general patterns of internal migration or the migration characteristics of specific subgroups. Reports are often based on small numbers and do not examine the relationships between socioeconomic factors and migration. Different reports classify migrant populations differently, presenting difficulties for researchers and policymakers to gain a consistent picture of migration (particularly of interprovincial migration) and limiting the ability of policymakers to plan services appropriately. This study describes the characteristics of all migrants in Vietnam, focusing on interprovincial migrants, and examines age and sex trends and correlations among in-migration, urbanization, and individual income.
We analyzed data from the 15% sample survey in the 2009 Population and Housing Census, the 3% sample in the 1999 national census, the 5% sample in the 1989 national census, and selected data from the 2008 Vietnam Household Living Standards Survey. Logistic regression was used to identify socioeconomic factors related to migration.
In 2009, of 6.7 million internal migrants (approximately 6.5% of the total population), 3.4 million were interprovincial migrants. Three notable trends were observed between 1989 and 2009: (i) the total population is characterized by increasing proportions of migrants; (ii) the proportion of female migrants is growing; and (iii) the average age of migrants is decreasing. Socioeconomic factors related to interprovincial migration include provincial economic status (monthly income per capita: OR = 4.62, p = 0.005) and urbanization (proportion of urban population: OR = 3.47, p = 0.019), suggesting that provinces with high monthly income per capita and urbanization are more likely to have higher rates of in-migration.
These findings reflect the effects of unequally growing labor markets in Vietnamese provinces on migration, and are suggestive of infrastructure improvements and public service needs in these areas. Analysis of migration can provide useful information for planning health and social services and for policymaking for national economic development.
PMCID: PMC3535692  PMID: 23331992
Vietnam; interprovincial migration; trends; urbanization; migration rates; census
19.  Increase in susceptibility to insecticides with aging of wild Anopheles gambiae mosquitoes from Côte d’Ivoire 
BMC Infectious Diseases  2012;12:214.
Appropriate monitoring of vector insecticide susceptibility is required to provide the rationale for optimal insecticide selection in vector control programs.
In order to assess the influence of mosquito age on susceptibility to various insecticides, field-collected larvae of An. gambiae s.l. from Tiassalé were reared to adults. Females aged 1, 2, 3, 5 and 10 days were exposed to 5 insecticides (deltamethrin, permethrin, DDT, malathion and propoxur) using WHO susceptibility test kits. Outcome measures included the LT50 (exposure time required to achieve 50% knockdown), the RR (resistance ratio, i.e. a calculation of how much more resistant the wild population is compared with a standard susceptible strain) and the mortality rate following 1 hour exposure, for each insecticide and each mosquito age group.
There was a positive correlation between the rate of knockdown and mortality for all the age groups and for all insecticides tested. For deltamethrin, the RR50 was highest for 2 day old and lowest for 10 day old individuals. Overall, mortality was lowest for 2 and 3 day old individuals and significantly higher for 10 day old individuals (P < 0.05). With permethrin, the RR50 was highest for 1 to 3 day old individuals and lowest for 10 day old individuals and mortality was lowest for 1 to 3 day old individuals, intermediate for 5 day old and highest for 10 day old individuals. DDT did not display any knockdown effect and mortality was low for all mosquito age groups (<7%). With malathion, the RR50 was low (1.54 - 2.77) and mortality was high (>93%) for all age groups. With propoxur, no knockdown effect was observed for 1, 2 and 3 day old individuals and a very low level of mortality was observed (< 4%), which was significantly higher for 5 and 10 day old individuals (30%, P < 0.01).
Results indicate that for An. gambiae s.l. adults derived from wild-collected larvae, there was an influence of age on insecticide susceptibility status, with younger individuals (1 to 3 days old) more resistant than older mosquitoes. This indicates that the use of 1 – 2 day old mosquitoes in susceptibility assays as recommended by the WHO should facilitate detection of resistance at the stage where the highest rate of the resistance phenotype is present.
PMCID: PMC3482577  PMID: 22974492
Anopheles gambiae age; Insecticide resistance; Vector control
20.  Representative Seroprevalences of Brucellosis in Humans and Livestock in Kyrgyzstan 
Ecohealth  2011;9(2):132-138.
Kyrgyzstan reported 77.5 new human brucellosis cases per 100,000 people in 2007, which is one of the highest incidences worldwide. In Kyrgyzstan, the currently used diagnostic tests in humans and animals are the Rose Bengal Test and the Huddleson test. A national representative cross-sectional study using cluster sampling proportional to size in humans, cattle, sheep, and goats was undertaken to assess the apparent seroprevalence in humans and animals. A total of 4,936 livestock sera and 1,774 human sera were tested in Naryn, Chuy, and Osh Oblasts. The overall apparent seroprevalences of brucellosis were 8.8% in humans (95% CI 4.5–16.5), 2.8% (95% CI 1.6–4.9%) in cattle, 3.3% (95% CI 1.5–6.9%) in sheep, and 2.5% (95% CI 1.4–4.5%) in goats. Naryn Oblast had the highest seroprevalences in humans and sheep. More men than women were seropositive (OR = 1.96; P < 0.001). Human seroprevalence was significantly associated with small ruminant seroprevalence but not with cattle seroprevalence. Annual incidence of human brucellosis exposure, measured by serological tests, was more than ten times higher than the annual incidence of reported clinical brucellosis cases. This indicates an under-reporting of human brucellosis cases, even if only a fraction of seropositive people have clinical symptoms. In conclusion, this study confirms the high seroprevalence of brucellosis in Kyrgyzstan and warrants rapid effective intervention, among others, by mass vaccination of sheep and goats but also of cattle.
PMCID: PMC3415613  PMID: 22143553
apparent prevalence; incidence; brucellosis; human; livestock; serology; Kyrgyzstan
21.  No Paragonimus in high-risk groups in Côte d'Ivoire, but considerable prevalence of helminths and intestinal protozoon infections 
Parasites & Vectors  2011;4:96.
Paragonimiasis is a neglected tropical disease caused by an infection with lung flukes that is transmitted through the consumption of undercooked crabs. The disease is often confused with tuberculosis. Paragonimiasis is thought to be endemic in south-western Côte d'Ivoire.
Two cross-sectional surveys were carried out in the first half of 2009 in patients attending two tuberculosis centres of Abidjan. A third cross-sectional survey was conducted in May 2010 in children of two primary schools in Dabou, where crabs are frequently consumed. Patients with chronic cough provided three sputum samples plus one stool sample. Sputum samples were examined for tuberculosis with an auramine staining technique and for Paragonimus eggs using a concentration technique. Stool samples were subjected to the Ritchie technique. Schoolchildren provided a single stool sample, and samples were subjected to the Kato-Katz and an ether-concentration technique. A pre-tested questionnaire was administered to patients and schoolchildren to investigate food consumption habits. Additionally, between June 2009 and August 2010, shellfish were purchased from markets in Abidjan and Dabou and examined for metacercariae.
No human case of paragonimiasis was diagnosed. However, trematode infections were seen in 32 of the 272 shellfish examined (11.8%). Questionnaire results revealed that crab and pig meat is well cooked before consumption. Among the 278 patients with complete data records, 62 had tuberculosis, with a higher prevalence in males than females (28.8% vs. 13.9%, χ2 = 8.79, p = 0.003). The prevalence of helminths and intestinal protozoa was 4.6% and 16.9%, respectively. In the school survey, among 166 children with complete data records, the prevalence of helminths and intestinal protozoa was 22.3% and 48.8%, respectively. Boys had significantly higher prevalences of helminths and intestinal protozoa than girls. Hookworm was the predominant helminth species and Entamoeba coli was the most common intestinal protozoon species (13.8%).
Not a single case of Paragonimus was found in two high-risk groups of Côte d'Ivoire, most likely explained by food consumption habits. However, other helminth and intestinal protozoon infections were common.
PMCID: PMC3130684  PMID: 21639877
22.  African 1, an Epidemiologically Important Clonal Complex of Mycobacterium bovis Dominant in Mali, Nigeria, Cameroon, and Chad▿ † 
Journal of Bacteriology  2009;191(6):1951-1960.
We have identified a clonal complex of Mycobacterium bovis present at high frequency in cattle in population samples from several sub-Saharan west-central African countries. This closely related group of bacteria is defined by a specific chromosomal deletion (RDAf1) and can be identified by the absence of spacer 30 in the standard spoligotype typing scheme. We have named this group of strains the African 1 (Af1) clonal complex and have defined the spoligotype signature of this clonal complex as being the same as the M. bovis BCG vaccine strain but with the deletion of spacer 30. Strains of the Af1 clonal complex were found at high frequency in population samples of M. bovis from cattle in Mali, Cameroon, Nigeria, and Chad, and using a combination of variable-number tandem repeat typing and spoligotyping, we show that the population of M. bovis in each of these countries is distinct, suggesting that the recent mixing of strains between countries is not common in this area of Africa. Strains with the Af1-specific deletion (RDAf1) were not identified in M. bovis isolates from Algeria, Burundi, Ethiopia, Madagascar, Mozambique, South Africa, Tanzania, and Uganda. Furthermore, the spoligotype signature of the Af1 clonal complex has not been identified in population samples of bovine tuberculosis from Europe, Iran, and South America. These observations suggest that the Af1 clonal complex is geographically localized, albeit to several African countries, and we suggest that the dominance of the clonal complex in this region is the result of an original introduction into cows naïve to bovine tuberculosis.
PMCID: PMC2648362  PMID: 19136597
23.  Molecular characterisation of Mycobacterium bovis isolated from cattle slaughtered at the Bamako abattoir in Mali 
Mali is one of the most important livestock producers of the Sahel region of Africa. A high frequency of bovine tuberculosis (BTB) has been reported but surveillance and control schemes are restricted to abattoir inspections only. The objective of this study was to conduct, for the first time, molecular characterisation of Mycobacterium bovis strains isolated from cattle slaughtered at the Bamako abattoir. Of 3330 animals screened only 60 exhibited gross visible lesions. From these animals, twenty strains of M. bovis were isolated and characterised by spoligotyping.
Organ lesions typical of BTB were most often detected in the liver, followed by the lung and the peritoneum. M. bovis was isolated from 20 animals and 7 different spoligotypes were observed among these 20 strains; three of the patterns had not been previously reported. Spoligotype patterns from thirteen of the strains lacked spacer 30, a characteristic common in strains of M. bovis found in Chad, Cameroon and Nigeria. However, unlike the other three Central African countries, the majority of spoligotype patterns observed in Mali also lacked spacer 6. Of the remaining seven strains, six had spoligotype patterns identical to strains commonly isolated in France and Spain.
Two groups of M. bovis were detected in cattle slaughtered at the Bamako abattoir. The spoligotype pattern of the first group has similarities to strains previously observed in Chad, Cameroon and Nigeria. The additional absence of spacer 6 in the majority of these strains suggests a Mali specific clone. The spoligotype patterns of the remaining strains suggest that they may have been of European origin.
PMCID: PMC2483712  PMID: 18637160
24.  Human Benefits of Animal Interventions for Zoonosis Control  
Emerging Infectious Diseases  2007;13(4):527-531.
Animal interventions to control zoonoses save money, even in resource-limited countries.
Although industrialized countries have been able to contain recent outbreaks of zoonotic diseases, many resource-limited and transitioning countries have not been able to react adequately. The key for controlling zoonoses such as rabies, echinococcosis, and brucellosis is to focus on the animal reservoir. In this respect, ministries of health question whether the public health sector really benefits from interventions for livestock. Cross-sectoral assessments of interventions such as mass vaccination for brucellosis in Mongolia or vaccination of dogs for rabies in Chad consider human and animal health sectors from a societal economic perspective. Combining the total societal benefits, the intervention in the animal sector saves money and provides the economic argument, which opens new approaches for the control of zoonoses in resource-limited countries through contributions from multiple sectors.
PMCID: PMC2725951  PMID: 17553265
human health; society; benefits; interventions; livestock; brucellosis; rabies; avian influenza; synopsis

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