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1.  Associations between mild-to-moderate anaemia in pregnancy and helminth, malaria and HIV infection in Entebbe, Uganda 
It is suggested that helminths, particularly hookworm and schistosomiasis, may be important causes of anaemia in pregnancy. We assessed the associations between mild-to-moderate anaemia (haemoglobin >8.0 g/dl and <11.2 g/dl) and helminths, malaria and HIV among 2507 otherwise healthy pregnant women at enrolment to a trial of deworming in pregnancy in Entebbe, Uganda. The prevalence of anaemia was 39.7%. The prevalence of hookworm was 44.5%, Mansonella perstans 21.3%, Schistosoma mansoni 18.3%, Strongyloides 12.3%, Trichuris 9.1%, Ascaris 2.3%, asymptomatic Plasmodium falciparum parasitaemia 10.9% and HIV 11.9%. Anaemia showed little association with the presence of any helminth, but showed a strong association with malaria (adjusted odds ratio (AOR) 3.22, 95% CI 2.43–4.26) and HIV (AOR 2.46, 95% CI 1.90–3.19). There was a weak association between anaemia and increasing hookworm infection intensity. Thus, although highly prevalent, helminths showed little association with mild-to-moderate anaemia in this population, but HIV and malaria both showed a strong association. This result may relate to relatively good nutrition and low helminth infection intensity. These findings are pertinent to estimating the disease burden of helminths and other infections in pregnancy. [Clinical Trial No. ISRCTN32849447]
PMCID: PMC1950430  PMID: 17555783
Anaemia; Helminth; Pregnancy; HIV; Malaria; Uganda
2.  Associations Between Maternal Helminth and Malaria Infections in Pregnancy and Clinical Malaria in the Offspring: A Birth Cohort in Entebbe, Uganda 
The Journal of Infectious Diseases  2013;208(12):2007-2016.
Background. Helminth and malaria coinfections are common in the tropics. We investigated the hypothesis that prenatal exposure to these parasites might influence susceptibility to malaria in childhood.
Methods. In a birth cohort of 2345 mother–child pairs in Uganda, maternal helminth and malaria infection status was determined during pregnancy, and childhood malaria episodes were recorded from birth to age 5 years. We examined associations between maternal infections and malaria in the offspring.
Results. Common maternal infections were hookworm (45%), Mansonella perstans (21%), Schistosoma mansoni (18%), and Plasmodium falciparum (11%). At age 5 years, 69% of the children were still under follow-up. The incidence of malaria was 34 episodes per 100 child-years, and the mean prevalence of asymptomatic malaria at annual visits was 5.4%. Maternal hookworm and M. perstans infections were associated with an increased rate of childhood clinical malaria (adjusted hazard ratio [aHR], 1.24, 95% confidence interval [CI], 1.10–1.41; aHR, 1.20, 95% CI, 1.05–1.38, respectively). S. mansoni infection had no consistent association with childhood malaria.
Conclusions. This is the first report of an association between helminth infections in pregnancy and malaria in the offspring and indicates that helminth infections in pregnancy may increase the burden of childhood malaria morbidity.
PMCID: PMC3836463  PMID: 23904293
malaria; helminths; coinfections; pregnancy; childhood
3.  Effects of Deworming during Pregnancy on Maternal and Perinatal Outcomes in Entebbe, Uganda: A Randomized Controlled Trial 
Helminth infections during pregnancy may be associated with adverse outcomes, including maternal anemia, low birth weight, and perinatal mortality. Deworming during pregnancy has therefore been strongly advocated, but its benefits have not been rigorously evaluated.
In Entebbe, Uganda, 2507 pregnant women were recruited to a randomized, double-blind, placebo-controlled trial investigating albendazole and praziquantel in a 2 × 2 factorial design [ISRCTN32849447]. Hematinics and sulphadoxine-pyrimethamine for presumptive treatment of malaria were provided routinely. Maternal and perinatal outcomes were recorded. Analyses were by intention to treat.
At enrollment, 68% of women had helminths, 45% had hookworm, 18% had Schistosoma mansoni infection; 40% were anemic (hemoglobin level, <11.2 g/dL). At delivery, 35% were anaemic; there was no overall effect of albendazole (odds ratio [OR], 0.95; 95% confidence interval [CI], 0.79–1.15) or praziquantel (OR, 1.00; 95% CI, 0.83–1.21) on maternal anemia, but there was a suggestion of benefit of albendazole among women with moderate to heavy hookworm (OR, 0.45; 95% CI, 0.21–0.98; P = .15 for interaction). There was no effect of either anthelminthic treatment on mean birth weight (difference in mean associated with albendazole: −0.00 kg; 95% CI, −0.05 to 0.04 kg; difference in mean associated with praziquantel: −0.01 kg; 95% CI, −0.05 to 0.04 kg) or on proportion of low birth weight. Anthelminthic use during pregnancy showed no effect on perinatal mortality or congenital anomalies.
In our study area, where helminth prevalence was high but infection intensity was low, there was no overall effect of anthelminthic use during pregnancy on maternal anemia, birth weight, perinatal mortality, or congenital anomalies. The possible benefit of albendazole against anemia in pregnant women with heavy hookworm infection warrants further investigation.
PMCID: PMC2857962  PMID: 20067426
4.  Factors affecting the infant antibody response to measles immunisation in Entebbe-Uganda 
BMC Public Health  2013;13:619.
Vaccine failure is an important concern in the tropics with many contributing elements. Among them, it has been suggested that exposure to natural infections might contribute to vaccine failure and recurrent disease outbreaks. We tested this hypothesis by examining the influence of co-infections on maternal and infant measles-specific IgG levels.
We conducted an observational analysis using samples and data that had been collected during a larger randomised controlled trial, the Entebbe Mother and Baby Study (ISRCTN32849447). For the present study, 711 pregnant women and their offspring were considered. Helminth infections including hookworm, Schistosoma mansoni and Mansonella perstans, along with HIV, malaria, and other potential confounding factors were determined in mothers during pregnancy and in their infants at age one year. Infants received their measles immunisation at age nine months. Levels of total IgG against measles were measured in mothers during pregnancy and at delivery, as well as in cord blood and from infants at age one year.
Among the 711 pregnant women studied, 66% had at least one helminth infection at enrolment, 41% had hookworm, 20% M. perstans and 19% S. mansoni. Asymptomatic malaria and HIV prevalence was 8% and 10% respectively. At enrolment, 96% of the women had measles-specific IgG levels considered protective (median 4274 mIU/ml (IQR 1784, 7767)). IgG levels in cord blood were positively correlated to maternal measles-specific IgG levels at delivery (r = 0.81, p < 0.0001). Among the infants at one year of age, median measles-specific IgG levels were markedly lower than in maternal and cord blood (median 370 mIU/ml (IQR 198, 656) p < 0.0001). In addition, only 75% of the infants had measles-specific IgG levels considered to be protective. In a multivariate regression analysis, factors associated with reduced measles-specific antibody levels in infancy were maternal malaria infection, infant malaria parasitaemia, infant HIV and infant wasting. There was no association with maternal helminth infection.
Malaria and HIV infection in mothers during pregnancy, and in their infants, along with infant malnutrition, may result in reduction of the antibody response to measles immunisation in infancy. This re-emphasises the importance of malaria and HIV control, and support for infant nutrition, as these interventions may have benefits for vaccine efficacy in tropical settings.
PMCID: PMC3733798  PMID: 23816281
Infections; Co-infections; Measles; Helminth; Malaria; HIV; Maternal; Infants; Pregnancy; Immunisation
Human co-infection with Plasmodium falciparum and helminths is ubiquitous throughout Africa, although its public health significance remains a topic for which there are many unknowns. In this review we have adopted an empirical approach to investigating the geography and epidemiology of co-infection, and associations between patterns of co-infection and haemoglobin in different age groups. Analysis highlights the extensive geographic overlap between P. falciparum and the major human helminth infections in Africa, with the population at coincident risk of infection greatest for hookworm. Age infection profiles indicate that school-age children are at the highest risk of co-infection, and re-analysis of existing data suggests that co-infection with P. falciparum and hookworm has an additive impact on hemoglobin, exacerbating anemia-related malarial disease burden. We suggest that both school-age children and pregnant women – groups among the highest risk of anemia - would benefit from an integrated approach to malaria and helminth control.
PMCID: PMC2637949  PMID: 18165479
Malaria; helminths; hookworm; co-infection; anemia; epidemiology; disease burden; disease control; Africa
6.  The co-distribution of Plasmodium falciparum and hookworm among African schoolchildren 
Malaria Journal  2006;5:99.
Surprisingly little is known about the geographical overlap between malaria and other tropical diseases, including helminth infections. This is despite the potential public health importance of co-infection and synergistic opportunities for control.
Statistical models are presented that predict the large-scale distribution of hookworm in sub-Saharan Africa (SSA), based on the relationship between prevalence of infection among schoolchildren and remotely sensed environmental variables. Using a climate-based spatial model of the transmission potential for Plasmodium falciparum malaria, adjusted for urbanization, the spatial congruence of populations at coincident risk of infection is determined.
The model of hookworm indicates that the infection is widespread throughout Africa and that, of the 179.3 million school-aged children who live on the continent, 50.0 (95% CI: 48.9–51.1) million (27.9% of total population) are infected with hookworm and 45.1 (95% CI: 43.9–46) million are estimated to be at risk of coincident infection.
Malaria and hookworm infection are widespread throughout SSA and over a quarter of school-aged children in sub-Saharan Africa appear to be at risk of coincident infection and thus at enhanced risk of clinical disease. The results suggest that the control of parasitic helminths and of malaria in school children could be viewed as essential co-contributors to promoting the health of schoolchildren.
PMCID: PMC1635726  PMID: 17083720
7.  The effect of anthelminthic treatment during pregnancy on HIV plasma viral load; results from a randomised, double blinded, placebo-controlled trial in Uganda 
To investigate the effect of helminth infections and their treatment during pregnancy on HIV load, we conducted a 2×2 factorial randomised controlled trial of albendazole versus placebo and praziquantel versus placebo in pregnant women in Entebbe, Uganda
Two hundred and sixty-four HIV-infected women from the Entebbe Mother and Baby Study (ISRCTN32849447) were included in this analysis. Women were tested for helminth infections at enrolment and mean HIV load was compared between infected and uninfected groups. The effect of anthelminthic treatment on HIV load was evaluated at six weeks post-treatment and at delivery using linear regression and adjusting for enrolment viral load.
Hookworm and Trichuris infections were associated with higher mean viral load at enrolment (adjusted mean difference 0.24log10 copies/ml, 95% confidence interval (CI): 0.01 to 0.47, p=0.03 and 0.37log10 copies/ml, 95%CI: 0.00 to 0.74, p=0.05, respectively). There were no associations between viral load and other helminth species. There was some evidence that albendazole reduced viral load at six weeks post-treatment (adjusted mean difference −0.17, 95% CI: −0.36 to 0.01, p=0.07), however this effect did not differ according to mother’s hookworm infection status and had diminished at delivery (adjusted mean difference −0.11, 95% CI: −0.28 to 0.07, p=0.23). There was no effect of praziquantel treatment on HIV load at any time point.
Infection with some soil-transmitted helminth species is associated with increased HIV load in pregnancy. Treatment with albendazole causes a small decrease in HIV load, however this may not represent a direct effect of worm removal.
PMCID: PMC3383620  PMID: 22728750
HIV; viral load; helminths; anthelminthic treatment; clinical trial
8.  Birthweight in Offspring of Mothers with High Prevalence of Helminth and Malaria Infection in Coastal Kenya 
Results of studies on the associations of maternal helminth infection and malaria-helminth co-infection on birth outcomes have been mixed. A group of 696 pregnant women from the Kwale district in Kenya were recruited and tested for malaria and helminth infection at delivery. Birthweight was documented for 664 infants. A total of 42.7% of the mothers were infected with Plasmodium falciparum, 30.6% with Schistosoma haematobium, 36.2% with filariasis, 31.5% with hookworm, and 5.9% with Trichuris trichiura; co-infection was present in 46.7%. Low birthweight (LBW) (weight < 2,500 grams) was present in 15.4% of the offspring, and 8.3% had a weight z-score ≤ 2 SD below the World Health Organization mean. Only gravida, age, and locale had a significant association with LBW. The high prevalence of maternal infection coupled with a higher than expected percentage of LBW highlight a need for further investigation of the association of maternal co-infection with LBW.
PMCID: PMC3541745  PMID: 23166193
9.  Helminthic Infections Rates and Malaria in HIV-Infected Pregnant Women on Anti-Retroviral Therapy in Rwanda 
Within sub-Saharan Africa, helminth and malaria infections cause considerable morbidity in HIV-positive pregnant women and their offspring. Helminth infections are also associated with a higher risk of mother-to-child HIV transmission. The aim of this study was to determine the prevalence of, and the protective and risk factors for helminth and malaria infections in pregnant HIV-positive Rwandan women receiving anti-retroviral therapy (ART).
Methodology and principle findings
Pregnant females (n = 980) were recruited from health centres in rural and peri-urban locations in the central and eastern provinces of Rwanda. Helminth infection was diagnosed using the Kato Katz method whilst the presence of Plasmodium falciparum was identified from blood smears. The prevalence of helminth infections was 34.3%; of malaria 13.3%, and of co-infections 6.6%. Helminth infections were more common in rural (43.1%) than peri-urban (18.0%; p<0.0005) sites. A CD4 count ≤350 cells/mm3 was associated with a higher risk of helminth infections (odds ratio, 3.39; 95% CIs, 2.16–5.33; p<0.0005) and malaria (3.37 [2.11–5.38]; p<0.0005) whilst helminth infection was a risk factor for malaria infection and vice versa. Education and employment reduced the risk of all types of infection whilst hand washing protected against helminth infection (0.29 [0.19–0.46]; p<0.0005);). The TDF-3TC-NVP (3.47 [2.21–5.45]; p<0.0005), D4T-3TC-NVP (2.47 [1.27–4.80]; p<0.05) and AZT-NVP (2.60 [1.33–5.08]; p<0.05) regimens each yielded higher helminth infection rates than the AZT-3TC-NVP regimen. Anti-retroviral therapy had no effect on the risk of malaria.
HIV-positive pregnant women would benefit from the scaling up of de-worming programs alongside health education and hygiene interventions. The differential effect of certain ART combinations (as observed here most strongly with AZT-3TC-NVP) possibly protecting against helminth infection warrants further investigation.
Author Summary
There is an overlap in the worldwide distribution of intestinal worms (helminths), malaria and HIV. Co-infections with helminth and malaria parasites cause a significant problem in the host, particularly in the presence of HIV infection. The aim of this study was to assess the prevalence of intestinal worm and malaria infection and co-infections and the associated risk factors among HIV-positive pregnant women that attended rural and peri-urban health centers in Rwanda. Our findings indicate that intestinal worms were more common among HIV-infected pregnant women in the rural than peri-urban settings. HIV-positive pregnant women who had lower CD4 cell counts were more at risk of being infected by intestinal worms and malaria. Malaria also increased the risk of being infected by intestinal worms and vice versa. Socio-economic factors such as lack of education and unemployment were among the risk factors for intestinal worm infections and malaria. Hand washing was found to reduce the risk for worm infections; whilst one particular ART combination (AZT-3TC-NVP) led to a reduced rate of helminth infections when compared to others.
PMCID: PMC3744439  PMID: 23967365
10.  Risk Factors for Helminth, Malaria, and HIV Infection in Pregnancy in Entebbe, Uganda 
Infections during pregnancy may have serious consequences for both mother and baby. Assessment of risk factors for infections informs planning of interventions and analysis of the impact of infections on health outcomes.
To describe risk factors for helminths, malaria and HIV in pregnant Ugandan women before intervention in a trial of de-worming in pregnancy.
The trial recruited 2,507 pregnant women between April 2003 and November 2005. Participants were interviewed and blood and stool samples obtained; location of residence at enrolment was mapped. Demographic, socioeconomic, behavioral and other risk factors were modelled using logistic regression.
There was a high prevalence of helminth, malaria and HIV infection, as previously reported. All helminths and malaria parasitemia were more common in younger women, and education was protective against every infection. Place of birth and/or tribe affected all helminths in a pattern consistent with the geographical distribution of helminth infections in Uganda. Four different geohelminths (hookworm, Trichuris, Ascaris and Trichostrongylus) showed a downwards trend in prevalence during the enrolment period. There was a negative association between hookworm and HIV, and between hookworm and low CD4 count among HIV-positive women. Locally, high prevalence of schistosomiasis and HIV occurred in lakeshore communities.
Interventions for helminths, malaria and HIV need to target young women both in and out of school. Antenatal interventions for malaria and HIV infection must continue to be promoted. Women originating from a high risk area for a helminth infection remain at high risk after migration to a lower-risk area, and vice versa, but overall, geohelminths seem to be becoming less common in this population. High risk populations, such as fishing communities, require directed effort against schistosomiasis and HIV infection.
Author Summary
Infections in pregnancy can cause miscarriage, stillbirth, maternal mortality, and low birth weight and have other long-term complications for mother and baby, although the full impact of many infections, particularly worm infections, is not yet fully understood. There is a high burden of infectious disease in many developing countries. In this analysis, we identified which factors put pregnant women in Entebbe, Uganda, at particular risk for worm infections, malaria, HIV, and, where possible, rarer infections including syphilis. The women in this study, and their children, will be followed up to determine the long-term effects of exposure of the fetus to these maternal infections on health during childhood. The findings of this baseline analysis will help in the interpretation of the long-term outcomes. The findings also highlight which groups are most at risk of each infection, and this may help in targeting interventions to prevent, treat, or mitigate the impact of infections in pregnancy.
PMCID: PMC2696595  PMID: 19564904
11.  Parasite infection is associated with Kaposi's sarcoma associated herpesvirus (KSHV) in Ugandan women 
Immune modulation by parasites may influence susceptibility to bacteria and viruses. We examined the association between current parasite infections, HIV and syphilis (measured in blood or stool samples using standard methods) and antibodies against Kaposi's sarcoma herpesvirus (KSHV), measured by ELISA, in 1915 stored plasma samples from pregnant women in Entebbe, Uganda.
Seroprevalence of KSHV was higher in women with malaria parasitaemia (73% vs 60% p = 0.01), hookworm (67% vs 56% p = 0.001) and Mansonella perstans (69% vs 59% p = 0.05); seroprevalence increased with increasing intensity of hookworm infection (p < 0.001[trend]). No associations were found for HIV, five other parasites or active syphilis. These effects were not explained by socioeconomic status or education.
Specific parasite infections are associated with presence of antibodies against KSHV, perhaps mediated via their effect on immune function.
PMCID: PMC3197512  PMID: 21962023
12.  Impact of Plasmodium falciparum and hookworm infections on the frequency of anaemia in pregnant women of rural communities in Enugu, South East Nigeria 
Malaria and hookworm infections are common in sub-Saharan Africa and they increase the prevalence of anaemia in pregnancy with resultant poor pregnancy outcomes. This study was carried out to assess the impact of Plasmodium falciparum and hookworm infections on the frequency of anaemia among pregnant women in two rural communities in Enugu, South East Nigeria.
A cross sectional descriptive study was carried out in a total of 226 women attending antenatal clinics at two rural Primary Health Centres (PHC) from April 2011 to July 2011(each PHC with 113 subjects). Socio-demographic data were collected through a structured questionnaire. Blood and stool samples were evaluated for haemoglobin estimation and malaria parasites, and stool samples examined for parasitic infection in all the women. Data was analyzed using STATA 10 software statistical analysis package. Student t-test was used for comparing mean values and chi square test for comparing categorical variables and level of significance set at p<0.05 and logistic regression was used to identify the risk factors associated with malaria in pregnancy.
The mean age of the women was 27years with range 18 - 38years and SD of 5years. Most of the women were housewives and over 50% in their second trimester. 53% of them had malaria parasites while 27% had hookworm infection. About 40% of the women were anaemic (haemoglobin < 0.001). Similar association was found between hookworm infection and anaemia (p <0.001). Though both malaria and hookworm infections greatly increase the odds for anaemia (AOR 18.06, CI 18.15 -39.99, P<0.001) and (AOR 5.28, CI 2.26-12.38, P<0.001) respectively, the odds for having anaemia in pregnancy was higher for malaria than hookworm infections.
Plasmodium falciparum and hookworm infections have significant impact on the high frequency of anaemia in pregnancy in our rural communities. There is need to strengthen the control program that has been in place with an integrated intervention to combat these parasitic infections in our rural communities, with mass distribution of antihelminthics as one of the included relevant methods, among others.
PMCID: PMC3597852  PMID: 23503560
Malaria; hookworm; Enugu; parasites; Nigeria
13.  The Association of Parasitic Infections in Pregnancy and Maternal and Fetal Anemia: A Cohort Study in Coastal Kenya 
Relative contribution of these infections on anemia in pregnancy is not certain. While measures to protect pregnant women against malaria have been scaling up, interventions against helminthes have received much less attention. In this study, we determine the relative impact of helminthes and malaria on maternal anemia.
A prospective observational study was conducted in coastal Kenya among a cohort of pregnant women who were recruited at their first antenatal care (ANC) visit and tested for malaria, hookworm, and other parasitic infections and anemia at enrollment. All women enrolled in the study received presumptive treatment with sulfadoxine-pyrimethamine, iron and multi-vitamins and women diagnosed with helminthic infections were treated with albendazole. Women delivering a live, term birth, were also tested for maternal anemia, fetal anemia and presence of infection at delivery.
Principal Findings
Of the 706 women studied, at the first ANC visit, 27% had moderate/severe anemia and 71% of women were anemic overall. The infections with highest prevalence were hookworm (24%), urogenital schistosomiasis (17%), trichuria (10%), and malaria (9%). In adjusted and unadjusted analyses, moderate/severe anemia at first ANC visit was associated with the higher intensities of hookworm and P. falciparum microscopy-malaria infections. At delivery, 34% of women had moderate/severe anemia and 18% of infants' cord hemoglobin was consistent with fetal anemia. While none of the maternal infections were significantly associated with fetal anemia, moderate/severe maternal anemia was associated with fetal anemia.
More than one quarter of women receiving standard ANC with IPTp for malaria had moderate/severe anemia in pregnancy and high rates of parasitic infection. Thus, addressing the role of co-infections, such as hookworm, as well as under-nutrition, and their contribution to anemia is needed.
Author Summary
International guidelines recommend routine prevention and treatments which are safe and effective during pregnancy to reduce hookworm, malaria and other infections among pregnant women living in geographic areas where these infections are prevalent. Despite their effectiveness, programs to address common infections such as hookworm, schistosomiasis and malaria during pregnancy have not been widely adopted. Hookworm, malaria and other infections have been associated with anemia in children, but the studies on the impact of these infections on anemia in pregnancy have not been as clear. This study was undertaken to evaluate the prevalence of parasitic infections among women attending antenatal care which provided the nationally recommended malaria preventive treatment program in coastal Kenya. At the first ANC visit, more than 70% of women were anemic, nearly one-fourth had hookworm and about 10% had malaria. Women with high levels of hookworm or malaria infections were at risk of anemia.
PMCID: PMC3937317  PMID: 24587473
14.  Impact of Anthelminthic Treatment in Pregnancy and Childhood on Immunisations, Infections and Eczema in Childhood: A Randomised Controlled Trial 
PLoS ONE  2012;7(12):e50325.
Helminth infections may modulate immune responses to unrelated pathogens and allergens; these effects may commence prenatally. We addressed the hypothesis that anthelminthic treatment in pregnancy and early childhood would improve responses to immunisation and modulate disease incidence in early childhood with both beneficial and detrimental effects.
Methods and Findings
A randomised, double-blind, placebo-controlled trial was conducted in Entebbe, Uganda [ISRCTN32849447]. In three independent randomisations, 2507 pregnant women were allocated to receive single-dose albendazole or placebo, and praziquantel or placebo; 2016 of their offspring were randomised to receive quarterly single-dose albendazole or placebo from age 15 months to 5 years. Primary outcomes were post-immunisation recall responses to BCG and tetanus antigens, and incidence of malaria, diarrhoea, and pneumonia; incidence of eczema was an important secondary outcome. Analysis was by intention-to-treat. Of 2345 live births, 1622 (69%) children remained in follow-up at age 5 years. 68% of mothers at enrolment, and 11% of five-year-olds, had helminth infections. Maternal hookworm and Schistosoma mansoni were effectively treated by albendazole and praziquantel, respectively; and childhood hookworm and Ascaris by quarterly albendazole. Incidence rates of malaria, diarrhoea, pneumonia, and eczema were 34, 65, 10 and 5 per 100 py, respectively. Albendazole during pregnancy caused an increased rate of eczema in the children (HR 1.58 (95% CI 1.15–2.17), p = 0.005). Quarterly albendazole during childhood was associated with reduced incidence of clinical malaria (HR 0.85 (95% CI 0.73–0.98), p = 0.03). There were no consistent effects of the interventions on any other outcome.
Routine use of albendazole in pregnancy may not always be beneficial, even in tropical developing countries. By contrast, regular albendazole treatment in preschool children may have an additional benefit for malaria control where helminths and malaria are co-endemic. Given the low helminth prevalence in our children, the effect of albendazole on malaria is likely to be direct.
Trial registration
Current Controlled Trials ISRCTN32849447
PMCID: PMC3517620  PMID: 23236367
15.  Interactions and Potential Implications of Plasmodium falciparum-Hookworm Coinfection in Different Age Groups in South-Central Côte d'Ivoire 
Given the widespread distribution of Plasmodium and helminth infections, and similarities of ecological requirements for disease transmission, coinfection is a common phenomenon in sub-Saharan Africa and elsewhere in the tropics. Interactions of Plasmodium falciparum and soil-transmitted helminths, including immunological responses and clinical outcomes of the host, need further scientific inquiry. Understanding the complex interactions between these parasitic infections is of public health relevance considering that control measures targeting malaria and helminthiases are going to scale.
A cross-sectional survey was carried out in April 2010 in infants, young school-aged children, and young non-pregnant women in south-central Côte d'Ivoire. Stool, urine, and blood samples were collected and subjected to standardized, quality-controlled methods. Soil-transmitted helminth infections were identified and quantified in stool. Finger-prick blood samples were used to determine Plasmodium spp. infection, parasitemia, and hemoglobin concentrations. Iron, vitamin A, riboflavin, and inflammation status were measured in venous blood samples.
Principal Findings
Multivariate regression analysis revealed specific association between infection and demographic, socioeconomic, host inflammatory and nutritional factors. Non-pregnant women infected with P. falciparum had significantly lower odds of hookworm infection, whilst a significant positive association was found between both parasitic infections in 6- to 8-year-old children. Coinfected children had lower odds of anemia and iron deficiency than their counterparts infected with P. falciparum alone.
Our findings suggest that interaction between P. falciparum and light-intensity hookworm infections vary with age and, in school-aged children, may benefit the host through preventing iron deficiency anemia. This observation warrants additional investigation to elucidate the mechanisms and consequences of coinfections, as this information could have important implications when implementing integrated control measures against malaria and helminthiases.
Author Summary
In sub-Saharan Africa, parasitic worms (helminths) are among the most common chronic infections, malaria among the most deadly, and coinfection is the norm rather than the exception. Infections with hookworm and Plasmodium can decrease the level of hemoglobin and are therefore associated with anemia. Previous studies have investigated the consequences of coinfection in different age groups and settings, but results are conflicting. Indeed, there is no consensus about detrimental or beneficial effects of a coinfection for the host. We designed a cross-sectional study to determine risk factors for anemia and investigated interactions and discuss potential implications of P. falciparum and hookworm coinfection in three groups of people. Overall, 324 individuals were diagnosed for helminths and Plasmodium infections, anemia, subclinical inflammation, and micronutrient deficiencies, and household’s socioeconomic status was determined based on an asset-index. We found significant associations between hookworm and P. falciparum infections, depending on the age group. Interestingly, 6- to 8-year-old children harboring a coinfection showed significantly lower odds of anemia and iron deficiency than children infected with P. falciparum alone. This observation warrants follow-up studies, as there are important implications when implementing integrated control measures against malaria and helminthiases.
PMCID: PMC3486899  PMID: 23133691
16.  Heterogeneities and Consequences of Plasmodium Species and Hookworm Coinfection: A Population Based Study in Uganda 
The Journal of infectious diseases  2010;203(3):406-417.
Previous studies have suggested that helminth infection exacerbates malaria, but few existing epidemiological studies adequately control for infection heterogeneities and confounding factors. In this study, we investigate spatial and household heterogeneities, predictors, and consequences of Plasmodium species and hookworm coinfection in rural communities in Uganda.
A cross-sectional study was conducted among 1770 individuals aged 0–88 years in 4 villages. We recorded demographic, socioeconomic, and microgeographic factors during household surveys. We determined malaria parasitemia and hemoglobin concentration and collected stool samples on 2 consecutive days. For data analysis, we used a hierarchical, spatially explicit Bayesian framework.
Prevalence of Plasmodium-hookworm coinfection was 15.5% overall and highest among school-aged children. We found strong evidence of spatial and household clustering of coinfection and an enduring positive association between Plasmodium-species and hookworm infection among preschool-aged children (odds ratio [OR], 2.36; 95% Bayesian credible interval [BCI], 1.26–4.30) and adults (OR, 2.09; 95% BCI, 1.35–3.16) but not among school-aged children. Coinfection was associated with lower hemoglobin level only among school-aged children.
Plasmodium-hookworm coinfection exhibits marked age dependency and significant spatial and household heterogeneity, and among preschool-aged children and adults, occurs more than would be expected by chance. Such heterogeneities provide insight into factors underlying observed patterns and the design of integrated control strategies.
PMCID: PMC3038339  PMID: 21187338
17.  Heterogeneities and Consequences of Plasmodium Species and Hookworm Coinfection: A Population Based Study in Uganda 
The Journal of Infectious Diseases  2011;203(3):406-417.
Background. Previous studies have suggested that helminth infection exacerbates malaria, but few existing epidemiological studies adequately control for infection heterogeneities and confounding factors. In this study, we investigate spatial and household heterogeneities, predictors, and consequences of Plasmodium species and hookworm coinfection in rural communities in Uganda.
Methods. A cross-sectional study was conducted among 1770 individuals aged 0–88 years in 4 villages. We recorded demographic, socioeconomic, and microgeographic factors during household surveys. We determined malaria parasitemia and hemoglobin concentration and collected stool samples on 2 consecutive days. For data analysis, we used a hierarchical, spatially explicit Bayesian framework.
Results. Prevalence of Plasmodium-hookworm coinfection was 15.5% overall and highest among school-aged children. We found strong evidence of spatial and household clustering of coinfection and an enduring positive association between Plasmodium-species and hookworm infection among preschool-aged children (odds ratio [OR], 2.36; 95% Bayesian credible interval [BCI], 1.26–4.30) and adults (OR, 2.09; 95% BCI, 1.35–3.16) but not among school-aged children. Coinfection was associated with lower hemoglobin level only among school-aged children.
Conclusions. Plasmodium-hookworm coinfection exhibits marked age dependency and significant spatial and household heterogeneity, and among preschool-aged children and adults, occurs more than would be expected by chance. Such heterogeneities provide insight into factors underlying observed patterns and the design of integrated control strategies.
PMCID: PMC3038339  PMID: 21187338
18.  Effect of single-dose anthelmintic treatment during pregnancy on an infant's response to immunisation and on susceptibility to infectious diseases in infancy: a randomised, double-blind, placebo-controlled trial 
Lancet  2011;377(9759):52-62.
Helminth infections affect the human immune response. We investigated whether prenatal exposure to and treatment of maternal helminth infections affects development of an infant's immune response to immunisations and unrelated infections.
In this randomised, double-blind, placebo-controlled trial, we enrolled 2507 women in the second or third trimester of pregnancy who were planning to deliver in Entebbe General Hospital, Entebbe, Uganda. With a computer-generated random number sequence in blocks of 100, we assigned patients to 440 mg albendazole and 40 mg/kg praziquantel (n=628), 440 mg albendazole and a praziquantel-matching placebo (n=625), 40 mg/kg praziquantel and an albendazole-matching placebo (n=626), or an albendazole-matching placebo and praziquantel-matching placebo (n=628). All participants and hospital staff were masked to allocation. Primary outcomes were immune response at age 1 year to BCG, tetanus, and measles immunisation; incidence of infectious diseases during infancy; and vertical HIV transmission. Analysis was by intention-to-treat. This trial is registered, number ISRCTN32849447.
Data were available at delivery for 2356 women, with 2345 livebirths; 2115 (90%) of liveborn infants remained in follow-up at 1 year of age. Neither albendazole nor praziquantel treatments affected infant response to BCG, tetanus, or measles immunisation. However, in infants of mothers with hookworm infection, albendazole treatment reduced interleukin-5 (geometric mean ratio 0·50, 95% CI 0·30–0·81, interaction p=0·02) and interleukin-13 (0·52, 0·34–0·82, 0·0005) response to tetanus toxoid. The rate per 100 person-years of malaria was 40·9 (95% CI 38·3–43·7), of diarrhoea was 134·1 (129·2–139·2), and of pneumonia was 22·3 (20·4–24·4). We noted no effect on infectious disease incidence for albendazole treatment (malaria [hazard ratio 0·95, 95% CI 0·79–1.14], diarrhoea [1·06, 0·96–1·16], pneumonia [1·11, 0·90–1·38]) or praziquantel treatment (malaria [1·00, 0·84–1·20], diarrhoea [1·07, 0·98–1·18], pneumonia [1·00, 0·80–1·24]). In HIV-exposed infants, 39 (18%) were infected at 6 weeks; vertical transmission was not associated with albendazole (odds ratio 0·70, 95% CI 0·35–1·42) or praziquantel (0·60, 0·29–1·23) treatment.
These results do not accord with the recently advocated policy of routine antenatal anthelmintic treatment, and the value of such a policy may need to be reviewed.
Wellcome Trust.
PMCID: PMC3018567  PMID: 21176950
19.  Efficacy of integrated school based de-worming and prompt malaria treatment on helminths -Plasmodium falciparum co-infections: A 33 months follow up study 
The geographical congruency in distribution of helminths and Plasmodium falciparum makes polyparasitism a common phenomenon in Sub Saharan Africa. The devastating effects of helminths-Plasmodium co-infections on primary school health have raised global interest for integrated control. However little is known on the feasibility, timing and efficacy of integrated helminths-Plasmodium control strategies. A study was conducted in Zimbabwe to evaluate the efficacy of repeated combined school based antihelminthic and prompt malaria treatment.
A cohort of primary schoolchildren (5-17 years) received combined Praziquantel, albendazole treatment at baseline, and again during 6, 12 and 33 months follow up surveys and sustained prompt malaria treatment. Sustained prompt malaria treatment was carried out throughout the study period. Children's infection status with helminths, Plasmodium and helminths-Plasmodium co-infections was determined by parasitological examinations at baseline and at each treatment point. The prevalence of S. haematobium, S. mansoni, STH, malaria, helminths-Plasmodium co-infections and helminths infection intensities before and after treatment were analysed.
Longitudinal data showed that two rounds of combined Praziquantel and albendazole treatment for schistosomiasis and STHs at 6 monthly intervals and sustained prompt malaria treatment significantly reduced the overall prevalence of S. haematobium, S. mansoni, hookworms and P. falciparum infection in primary schoolchildren by 73.5%, 70.8%, 67.3% and 58.8% respectively (p < 0.001, p < 0.001, p < 0.001, p < 0.001 respectively). More importantly, the prevalence of STH + schistosomes, P. f + schistosomes, and P. f + STHs + schistosomes co-infections were reduced by 68.0%, 84.2%, and 90.7%, respectively. The absence of anti-helminthic treatment between the 12 mth and 33 mth follow-up surveys resulted in the sharp increase in STHs + schistosomes co-infection from 3.3% at 12 months follow up survey to 10.7%, slightly more than the baseline level (10.3%) while other co-infection combinations remained significantly low. The overall prevalence of heavy S. haematobium, S. mansoni and hookworms infection intensities were significantly reduced from: 17.9-22.4% to 2.6-5.1%, 1.6-3.3% to 0.0% and 0.0-0.7% to 0.0% respectively.
Biannual Integrated school based antihelminthic and sustained prompt malaria treatment has a potential to reduce the burden of helminths-plasmodium co-infections in primary school children. In areas of stable malaria transmission, active case finding is recommended to track and treat asymptomatic malaria cases as these may sustain transmission in the community.
PMCID: PMC3141662  PMID: 21696629
co-infection; malaria; schistosomiasis; STHs; deworming
20.  Infection and Co-infection with Helminths and Plasmodium among School Children in Côte d’Ivoire: Results from a National Cross-Sectional Survey 
Helminth infection and malaria remain major causes of ill-health in the tropics and subtropics. There are several shared risk factors (e.g., poverty), and hence, helminth infection and malaria overlap geographically and temporally. However, the extent and consequences of helminth-Plasmodium co-infection at different spatial scales are poorly understood.
This study was conducted in 92 schools across Côte d’Ivoire during the dry season, from November 2011 to February 2012. School children provided blood samples for detection of Plasmodium infection, stool samples for diagnosis of soil-transmitted helminth (STH) and Schistosoma mansoni infections, and urine samples for appraisal of Schistosoma haematobium infection. A questionnaire was administered to obtain demographic, socioeconomic, and behavioral data. Multinomial regression models were utilized to determine risk factors for STH-Plasmodium and Schistosoma-Plasmodium co-infection.
Principal Findings
Complete parasitological and questionnaire data were available for 5,104 children aged 5-16 years. 26.2% of the children were infected with any helminth species, whilst the prevalence of Plasmodium infection was 63.3%. STH-Plasmodium co-infection was detected in 13.5% and Schistosoma-Plasmodium in 5.6% of the children. Multinomial regression analysis revealed that boys, children aged 10 years and above, and activities involving close contact to water were significantly and positively associated with STH-Plasmodium co-infection. Boys, wells as source of drinking water, and water contact were significantly and positively associated with Schistosoma-Plasmodium co-infection. Access to latrines, deworming, higher socioeconomic status, and living in urban settings were negatively associated with STH-Plasmodium co-infection; whilst use of deworming drugs and access to modern latrines were negatively associated with Schistosoma-Plasmodium co-infection.
More than 60% of the school children surveyed were infected with Plasmodium across Côte d’Ivoire, and about one out of six had a helminth-Plasmodium co-infection. Our findings provide a rationale to combine control interventions that simultaneously aim at helminthiases and malaria.
Author Summary
Parasitic worm infection and malaria are common in tropical and subtropical countries and many people suffer from multiple parasite infections concurrently. It is important to gain knowledge on co-endemicity patterns because such information can help to design and prioritize interventions and control strategies focusing on areas at highest risk of co-infection. We carried out the first national survey on parasitic worm and Plasmodium infection among children in 92 schools all over Côte d’Ivoire. Questionnaires were administered to determine the children's socioeconomic status and infection-related risk factors. We found an overall prevalence of Plasmodium infection of 63.3%. Hookworm was the most common parasitic worm infection (17.2%), whereas schistosome worms were more focally distributed (9.1%). One out of six children was co-infected with parasitic worms and Plasmodium. Children from the poorest households living in rural areas were at highest risk of co-infection. The lack of sanitation facilities, and activities like swimming or fishing in nearby rivers were found to be positively associated with multiple species parasite infection. Our study motivates the integration of combined intervention measures that concurrently target neglected tropical diseases and malaria in highly resource-constrained settings.
PMCID: PMC4046940  PMID: 24901333
21.  Neglected Tropical Diseases in Sub-Saharan Africa: Review of Their Prevalence, Distribution, and Disease Burden 
The neglected tropical diseases (NTDs) are the most common conditions affecting the poorest 500 million people living in sub-Saharan Africa (SSA), and together produce a burden of disease that may be equivalent to up to one-half of SSA's malaria disease burden and more than double that caused by tuberculosis. Approximately 85% of the NTD disease burden results from helminth infections. Hookworm infection occurs in almost half of SSA's poorest people, including 40–50 million school-aged children and 7 million pregnant women in whom it is a leading cause of anemia. Schistosomiasis is the second most prevalent NTD after hookworm (192 million cases), accounting for 93% of the world's number of cases and possibly associated with increased horizontal transmission of HIV/AIDS. Lymphatic filariasis (46–51 million cases) and onchocerciasis (37 million cases) are also widespread in SSA, each disease representing a significant cause of disability and reduction in the region's agricultural productivity. There is a dearth of information on Africa's non-helminth NTDs. The protozoan infections, human African trypanosomiasis and visceral leishmaniasis, affect almost 100,000 people, primarily in areas of conflict in SSA where they cause high mortality, and where trachoma is the most prevalent bacterial NTD (30 million cases). However, there are little or no data on some very important protozoan infections, e.g., amebiasis and toxoplasmosis; bacterial infections, e.g., typhoid fever and non-typhoidal salmonellosis, the tick-borne bacterial zoonoses, and non-tuberculosis mycobaterial infections; and arboviral infections. Thus, the overall burden of Africa's NTDs may be severely underestimated. A full assessment is an important step for disease control priorities, particularly in Nigeria and the Democratic Republic of Congo, where the greatest number of NTDs may occur.
PMCID: PMC2727001  PMID: 19707588
22.  Gastrointestinal Helminth Infection in Pregnancy: Disease Incidence and Hematological Alterations 
Iranian Journal of Public Health  2013;42(5):497-503.
The incidence and hematological effects of helminth infection during pregnancy were investigated among pregnant women in Isiala, Mbano, Southeast Nigeria.
Totally 282 pregnant women were enlisted for the study between October 2011 and September 2012. Stool samples were examined for intestinal helminths using formalin-ether sedimentation technique. Hemoglobin (Hb) and Packed Cell Volume (PCV) levels were evaluated in venous blood samples using Sahli’s and microhaematocrit methods respectively.
Forty six (16.3%) subjects were infected with at least one helminth parasite; 24 (8.5%) hookworm, 14(5.0%) and 2(0.7%) A. lumbricoides and Trichuris trichiura infections respectively. Intestinal helminthiases in pregnant women was significantly associated with age (P<0.05). The prevalence of intestinal helminthiases by parity was also significantly different (P<0.05) with primigravidae having the highest infection rate (27.5%). Hematological assessment showed that the prevalence of anemia among the women was 58.9% (mean±SD = 9.3±1.0). The differences in hemoglobin levels by age groups was statistically significant (P <0.05). The contributory effect of gastrointestinal helminths in anemia showed that infected pregnant women had lower mean hemoglobin (8.60±0.22g/dl) than the uninfected (9.72±0.07g/dl). Significant difference (t-value = 5.660, P<0.05) was observed between the Hb of the infected and uninfected pregnant women. In addition, infected pregnant women had mean PCV of 26.09±0.65% while the uninfected had 34.54±2.96%. The mean PCV of infected pregnant women was significantly different (t-value= 0.013, P<0.05) from that of the uninfected.
Anti-helminthic therapy after the first trimester should be part of the antenatal programme. Intestinal helminth infection showed significant negative correlation with Hb and PCV and contributed moderately to anemia.
PMCID: PMC3684458  PMID: 23802107
Anemia; Hematology; Hookworm; Hemoglobin; Packed cell volume
23.  Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo 
Malaria Journal  2014;13:132.
In areas of high malaria transmission, Plasmodium falciparum infection during pregnancy is characterized by malaria-related anaemia, placental malaria and does not always result in clinical symptoms. This situation is associated with poor pregnancy outcomes. The aim of this study was to determine the extent of asymptomatic P. falciparum infection, its relation with anaemia as well as the most cost-effective technique for its diagnosis in healthy pregnant women living in Kinshasa, Democratic Republic of the Congo.
In a cross-sectional study design, information on socio-demographic characteristics and cost data were collected in healthy pregnant women attending antenatal care consultations. Plasmodium falciparum infection was diagnosed using rapid diagnostic test (RDT), microscopy and polymerase chain reaction (PCR). Haemoglobin concentration was also determined.
In total, 332 pregnant women were enrolled. RDT and microscopy data were available for all the blood samples and 166 samples were analysed by PCR. The prevalence of asymptomatic P. falciparum infection using microscopy, RDTs and PCR, were respectively 21.6%, 27.4% and 29.5%. Taking PCR as a reference, RDTs had a sensitivity of 81.6% and a specificity of 94.9% to diagnose asymptomatic P. falciparum infection. The corresponding values for microscopy were 67.3% and 97.4%. The prevalence of anaemia was 61.1% and asymptomatic malaria increased five times the odds (p < 0.001) of having anaemia. RDTs were more cost-effective compared to microscopy. Incremental cost-effectiveness ratio was US$ 63.47 per microscopy adequately diagnosed case.
These alarming results emphasize the need to actively diagnose and treat asymptomatic malaria infection during all antenatal care visits. Moreover, in DRC, malaria and anaemia control efforts should be strengthened by promoting the use of insecticide-treated nets, intermittent preventive treatment with sulphadoxine-pyrimethamine and iron and folic acid supplements.
PMCID: PMC3976674  PMID: 24690179
Asymptomatic P. falciparum infection; Anaemia; Pregnancy; Cost-effectiveness; Democratic Republic of the Congo
24.  Molecular identification of Wolbachia from the filarial nematode Mansonella perstans 
Wolbachiae are bacterial endosymbionts of insects and many filarial nematodes whose products trigger inflammation in filarial infections. The dependence of the parasites on their endosymbionts has also led to the use of antibiotics directed against the Wolbachiae, therapy that has been demonstrated to have a profound salutary effect on filarial infections. The identification of Wolbachiae in Mansonella species has been conclusively shown for Mansonella ozzardi (Mo), but not for Mansonella perstans (Mp) Using primers known to amplify the 16S ribosomal DNA of other filarial Wolbachiae, an identical 1393 bp band was found in all samples tested. Sequence analysis of these samples demonstrated a single consensus sequence for Mp Wolbachia 16S rDNA that was most similar to Wolbachia sequences from other filarial nematodes. When aligned with the only other Mansonella Wolbachia sequence (Mo) there were only 8 nucleotide differences in the 1369 bp overlapping sequence. Phylogenetic dendrograms, showing the relationship of the Mp Wolbachia to other Wolbachia 16S rDNA, tracked almost identically to the 5S rRNA of their parasite host. Wolbachia surface protein (WSP) was also demonstrated in protein extracted from Mp-containing whole blood. In advance of a treatment trial of Mp, a method for the quantitation of Mp Wolbachia was developed and used to demonstrate not only a relationship between microfilarial numbers and Wolbachia copy numbers, but also to demonstrate the effect of antibiotic on ridding Mp of Wolbachia.
PMCID: PMC2497444  PMID: 18538871
Wolbachia; endosymbiont; Mansonella; ribosomal
25.  Malaria, Intestinal Helminths and Other Risk Factors for Stillbirth in Ghana 
Objective. The objective of the study was to assess Plasmodium/intestinal helminth infection in pregnancy and other risk factors for stillbirth in Ghana. Methods. A cross-sectional study of women presenting for delivery in two hospitals was conducted during November-December 2006. Data collected included sociodemographic information, medical and obstetric histories, and anthropometric measures. Laboratory investigations for the presence of Plasmodium falciparum and intestinal helminths, and tests for hemoglobin levels were also performed. Results. The stillbirth rate was relatively high in this population (5%). Most of the stillbirths were fresh and 24% were macerated. When compared to women with no malaria, women with malaria had increased risk of stillbirth (OR = 1.9, 95% CI = 1.2–9.3). Other factors associated with stillbirth were severe anemia, low serum folate concentration, past induced abortion, and history of stillbirth. Conclusion. The fact that most of the stillbirths were fresh suggests that higher quality intrapartum care could reduce stillbirth rates.
PMCID: PMC2850132  PMID: 20379355

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