INTRODUCTION
Anemia is regarded worldwide as a medical condition deserving of sustained public health intervention. Anemia in pregnant women is defined as hemoglobin levels less than 11 g/dL.1 It is usually caused by iron deficiency, which is the most common nutrient deficiency in the world. It has been estimated that, at any one time in developing countries, half of the population (mainly children and women of reproductive age) is affected by anemia.2 During pregnancy, approximately 75% of all anemias diagnosed are due to iron deficiency.3 In Peru, 35% of women of reproductive age and 50% of pregnant women were found to be anemic.4
Iron deficiency is highest in population subgroups that are at peak rates of growth; namely, infants, young children, and pregnant women. Pregnancy is a time during which the risk for developing iron deficiency anemia is greatest as iron requirements are substantially higher than average.5,6 Furthermore, WHO considers that women in developing countries may be pregnant for as much as one half of their reproductive lives and therefore are at increased risk of anemia during this time.1
Anemia in pregnancy has been associated with poor birth outcome, such as low birth weight7–10 and increased maternal morbidity and mortality.1,11,12 It has been reported that close to 500,000 maternal deaths occur every year, the vast majority taking place in the developing world. Anemia is thought to be the major contributory cause of death in 20–40% of these maternal deaths.13 Furthermore, it has been estimated that 16–20% of all maternal deaths are associated with iron deficiency anemia.14
In developing countries, both nutritional deficiencies and parasitic infection, specifically hookworm and malaria infection, contribute most to anemia. In fact, hookworm infections are recognized as the leading cause of pathologic blood loss in tropical and subtropical countries.15 Hookworm infections contribute to anemia by causing blood loss directly through ingestion and mechanical damage of the mucosa, and indirectly, by affecting the supply of nutrients necessary for erythropoiesis.14,16 It has been estimated that, on average, blood losses into the feces (measured as fecal hemoglobin) increase by 0.825 mg per gram of feces for every increment of 1,000 hookworm eggs per gram (epg) of feces.17 Lack of iron in the diet, especially in rural and poor communities, is critical during pregnancy.18
Bundy and colleagues19 have estimated that approximately one-third of all pregnant women in developing countries are infected with hookworm infection (44 million out of 124 million pregnancies). It has been suggested that the impact of hookworm infection on maternal morbidity “may well be very considerable.”20 Hookworm-attributable anemia, induced by deficiencies of iron, total energy, protein and possibly folate and zinc, is a significant cause of intrauterine growth retardation and low birth weight.21,22 Evidence also suggests that both iron deficiency anemia and, separately, hookworm infection, will inhibit appetite resulting in low pregnancy weight gain and intrauterine growth retardation followed by low infant birth weight.21 It has even been suggested that the hookworm-attributable burden of disease in girls and women, especially during pregnancy, may constitute the most important component of their global disease burden.22 Added to this is the impact of concurrent parasitic coinfections and other co-morbid conditions.
In 1998, WHO proposed a classification for intensities for each soil-transmitted helminth infection (based on quantitative counts obtained using the Kato-Katz method).23 Especially in hookworm infection, the degree of severity of morbidity varies not only according to the number of worms present but also according to determinants of the host (e.g., age), parasite (e.g., species), and host-parasite interaction (e.g., nutritional intake of iron). The intensity classes for hookworm set by WHO were based on data published by Stoltzfus and others17 using fecal blood loss as measured in Zanzibari children. There exists the possibility that the epg limits of the different classes could change in different populations and with different proportions of hookworm species. Indeed, in a study population that included both children and adults in western Kenya, Olsen and others24 found that a cutoff of 300 epg differentiated anemic from nonanemic individuals.
Numerous studies have found a significant correlation between lower hemoglobin levels and higher fecal egg counts of hookworm.24–27 Stoltzfus and colleagues28 reported that the relationship between hookworm infection and hemoglobin concentration may be apparent only above a threshold worm burden. Heavy intensity Trichuris infection, which is associated with decreased food intake and blood loss, has also been associated with anemia.29,30
In this study, we assess the relationship between the intensity of soil-transmitted helminths (hookworm, Trichuris and Ascaris) and anemia in a population of pregnant women in Iquitos, Peru, a highly hookworm-endemic area.
MATERIALS AND METHODS
Study area.
The current study was carried out in Iquitos, Peru, a tropical and humid jungle area. Iquitos is situated in the Department of Loreto, which comprises nearly one-fourth of the landmass of Peru and has the ecologic characteristics of the Amazon lowlands (Figure 1).
Soil-transmitted helminth infections, malaria, and anemia are endemic. Living conditions are characterized by poor sanitation and limited access to tap water. Maternal and Child Programs are run at the hospitals (Hospital Apoyo de Iquitos and Hospital Regional de Iquitos) and at various “posta medica” (health centers) in the towns and villages. In 2000, approximately 40% of pregnant women in Loreto failed to make at least one visit to a health center before delivery.31
Study design and population.
This baseline survey took place between April 2003 and November 2003. The inclusion criteria were second trimester pregnant women aged between 18 to 44 years; not having received anthelminthic treatment for 6 months prior to recruitment into the study; residence in rural or semiurban areas (defined as having no running water or toilet facilities in their house), and consent to participate. Exclusion criteria were having severe anemia (< 7 mg/dL)1 or having a medical condition for which follow-up was required. All pregnant women attending health centers for their periodic prenatal care visits who met the inclusion criteria were invited to participate in the study. Recruitment also included canvassing (door-to-door) in neighborhoods in the more rural catchment areas because it was known that many pregnant women did not seek prenatal care.
Questionnaire.
An interviewer-administered questionnaire was used to obtain sociodemographic information, reproductive health characteristics, medication history, and environmental characteristics. It was adapted from two that had previously been used in recent studies on pregnant women in Peru.18,32 It was first written in English and then translated and pretested in Spanish. Interviewers were qualified midwives (i.e., “obstetrices”) and were trained in questionnaire administration to attain standardization and maximize inter-interviewer reliability. Quality control was performed by daily review of each questionnaire by the project director (R. L.) and immediate remedy of any error or problem.
Measurement of anemia.
Hemoglobin concentration was obtained from fingerprick blood using Hemo-Cue assessment. The accuracy of the battery-operated Hemo-Cue photometer has been determined to be within ± 1.5%.33 Each Hemo-Cue photometer was checked for calibration every morning before use.
Measurement of parasite infections.
Containers for stool specimens were given to each woman at the time of questionnaire administration. Women were asked to return the next day with the fecal sample. The fecal samples were examined on the same day they were returned by two trained biologists using two study-dedicated Nikon microscopes. The biologists had a total of more than 25 years of laboratory and microscopy experience and, in addition, they received a specialized 2-week training in the parasitology laboratory of the “Instituto de Medicina Tropical Alexander von Humboldt” at the Universidad Peruana Cayetano Heredia in Lima, Peru. The Kato-Katz technique for quantification of helminth infection was used.34 Intensity of infection was expressed as eggs per gram of feces. The WHO23 categories for light, moderate, and heavy levels of intensities of soil-transmitted helminth infections were used. Because of the extremely hot and humid weather in Iquitos, which accelerated the clearing process for hookworm eggs, the slides were read within 25 minutes. Quality control measures (e.g., daily supervision, re-reading of all negative slides, external evaluator, storage of slides) were strictly enforced.
Presence of malaria infection was determined from finger-prick blood. Examination of Giemsa-stained thick and thin smears was used to determine the presence/absence of the malaria parasite. Interviewers were trained by the biologists to make the smears. Again, strict quality control measures were put in place.
Statistical methods.
Descriptive statistics included frequencies and means (and standard deviations). Frequencies of sociodemographic variables were also presented in subgroups defined by the presence or absence of anemia and presence or absence of hookworm infection. P values based on χ2 test (for proportions) and t test (for means) were calculated. For univariate analysis, odds ratios (ORs) and 95% confidence intervals (95% CI) were computed for each categorical variable; Pearson correlation coefficients were examined for continuous variables; and Spearman correlation coefficients (rs) were calculated for correlations between continuous and categorical variables. The correlation between parasite egg counts and hemoglobin was also examined at various egg count thresholds (> 1,000 epg, > 2,000 epg, > 3,000 epg, and > 5,000 epg). A χ2 test for trend was used to compare proportions of anemic women with proportions of nonanemic women in terms of categories of intensity (none and light versus moderate versus heavy).
The association between anemia (Hb < 11 g/dL or Hb ≥ 11 g/dL) and its determinants was examined by univariate and multivariate logistic regression analysis. A multiple linear regression analysis was also performed to identify predictors of hemoglobin concentration. A stepwise approach was used with variables significant at the P < 0.05 being kept in the final model. Variables were included in the multivariate model if, in the univariate analysis, they had a P value of ≤ 0.25 or if they had been previously identified as potential confounders or effect modifiers in the published literature. When variables were found to be highly correlated, the most informative variable was kept for further modeling. Age and marital status were correlated (rs = 0.20, P < 0.0001), so age was selected for model-building. Additionally, type of housing and presence of toilet facilities in the home were highly correlated with the environment variable (rural or periurban area) (P = 0.0016 and P = 0.020, respectively); therefore only environment was used for further modeling. Wearing sandals inside the house was correlated with wearing sandals outside the house (P < 0.001); therefore wearing sandals outside the house was retained. Parasite egg intensities were summarized as geometric means and log transformed (base 10) for comparison and analyses. All statistical analyses were carried out using the SAS software package (SAS Institute, Cary, NC).
Ethics approval.
Ethics approval was obtained from these ethics review committees: Research Institute of the McGill University Health Center (Canada); the “Comite Institucional de Etica de la Universidad Peruana Cayetano Heredia”; and the “Comite Etica de la Direccion General de Salud de las Personas del Ministerio de Salud de Peru.”
RESULTS
Population characteristics.
A total of 1,042 second trimester pregnant women were recruited. The sociodemographic characteristics of this study population are summarized in Table 1. The women were on average 25.2 years old (range, 18–42), had less than a secondary school education, were married or “conviviente” (i.e., living with partner but not married), were in their fourth month of pregnancy, and lived in a periurban type of environment. Most lived in homes with roofs made out of tree leaves and floors of earth. Access to drinking water was primarily from community installations, such as pipes of water functioning only at certain times of the day.
Anemia.
The prevalence of anemia was 47.31%; the mean hemoglobin level was 11.04 ± 1.10 g/dL (range, 7.0–14.4 g/dL). More single women were anemic than married (or conviviente) women (Table 1). Increasingly higher proportions of anemia were found with longer gestational age. Women who used latrines had a higher level of anemia than women who had more modern types of toilet facilities in their house. Women living in concrete houses were found to be more anemic than women living in either brick or wooden houses. Lastly, women who always wore sandals either inside or outside their houses had a higher prevalence of anemia than women who reported not wearing sandals either inside or outside of their houses.
Prevalence and intensity of parasites.
The overall prevalences were 47.22% for hookworm, 82.25% for Trichuris, and 63.92% for Ascaris. Only 9.31% of the pregnant women were free of any parasite infection; 20.25% of the women had a single infection, 38.96% had two infections, and 31.48% were infected with all three worm infections. The prevalence of Trichuris and hookworm coinfections was 44.05%.
Several determinants influenced the prevalence of hookworm infection. Women living in rural areas had a significantly higher prevalence of hookworm infection compared with women living in periurban areas (Table 1). Hookworm-infected women were generally married or conviviente and multiparous, with less than a secondary school education. Women with animals in their house were found to have a significantly lower prevalence than women not having animals in their house. Women not wearing sandals either inside or outside of their houses had higher hookworm prevalences than women wearing sandals. Anemia was also more prevalent in women living in houses constructed of palm leaves, where the floor was of wood or earth, and where there was no toilet facility or nearby latrine.
Only 1.63% of women had heavy intensity hookworm infection, 3.84% had a moderate intensity infection, and 41.75% had a light infection (52.78% having no infection) (Table 2). Geometric mean egg counts among infected women were 347 for hookworm (range, 24–13,848 epg), 571 for Trichuris (range, 24–25,200 epg), and 3,490 for Ascaris (range: 24–166,800 epg). When intensity categories were combined into none and light versus moderate and heavy, 5.47% of women had moderate to heavy hookworm infection. As for Trichuris infection, only 2.21% had a heavy infection, 26.78% had a moderate infection, and 53.26% had a light infection (17.75% having no infection). A total of 28.98% of women had a moderate to heavy Trichuris infection. Only 3.84% (N = 40), however, had both moderate and heavy hookworm and moderate and heavy Trichuris infections. In Ascaris infection, only 2.11% of women had a heavy infection, while 30.61% had a moderate infection and 31.19 had a light infection (36.08% having no infection). Approximately one third (32.73%) of women had a moderate to heavy Ascaris infection.
Even though this region of Peru is known as a malaria-endemic zone, only 2 women were found to be smear-positive, while 13 were taking chloroquine treatment. Malaria therefore was not included as a variable in any analysis.
Relationship between soil-transmitted helminths and anemia.
No single prevalence of any parasite infection was associated with anemia. However, several intensity measurements were found to be associated with anemia. There was a significant correlation between increasing hookworm egg counts and decreasing hemoglobin levels, however, this correlation was weak (r = −0.12, P < 0.001). No correlation was found between either Trichuris or Ascaris egg counts and hemoglobin. Examining egg count thresholds, the strongest statistically significant association with hemoglobin was found at the > 2,000 epg threshold for hookworm (r = −0.30, P = 0.020). No significant association was found at any threshold for Trichuris and Ascaris. When using the log-transformed eggs per gram count data, no significant association with hemoglobin was found for any of the three parasite species.
The mean hemoglobin of pregnant women having moderate and heavy intensity hookworm infection was significantly lower than women with no or light hookworm infection (10.75 g/dL versus 11.05 g/dL; P = 0.042). Similarly, a higher proportion of women having moderate and heavy infections of hookworm were anemic than women having no or light infection (OR = 1.84; 95% CI: 1.06, 3.18) (Table 3). Additionally, we found increasing proportions of anemic women with increasing intensity categories of hookworm infection (χ 2(trend)= 7.08; P = 0.027). Women having moderate and heavy Trichuris infection were just as likely to have anemia as women having no infection or light Trichuris infection (OR = 1.26; 95% CI: 0.96, 1.65). Women having moderate and heavy Ascaris infection were less likely to have anemia than women having no or light Ascaris infection (OR = 0.75; 95% CI: 0.58, 0.98).
Women with moderate and heavy intensities of both hookworm and Trichuris infections were more than twice as likely to have anemia (OR = 2.14; 95% CI: 1.10, 4.14). No other combination of coinfections or combinations of intensities of coinfections had a strong association with anemia.
Two parasite variables were found to be highly statistically significantly associated with anemia (moderate and heavy hookworm infection and co-infection of moderate and heavy hookworm and Trichuris infections) (Table 3). As these two variables were also highly correlated (P < 0.001), they were used separately in two models to examine the determinants of anemia.
On multivariate analysis, and considering moderate and heavy hookworm infection, after adjusting for age, education, environment, gestational age, wearing sandals outside the house and taking iron supplements, the sole determinant of anemia was found to be moderate and heavy hookworm infection (OR = 1.84; 95% CI: 1.06, 3.17). Similarly, after adjustment, coinfection of moderate and heavy hookworm and Trichuris infections was found to be statistically significantly associated with anemia (OR = 2.13; 95% CI: 1.10, 4.13).
In the multivariate linear regression analysis, where hemoglobin was the dependent variable, hookworm intensity in addition to age and gestational age was retained in the final model (Table 4). The regression coefficient of hookworm epg corresponded to a 0.107 g/dL decline in hemoglobin per 1,000 epg increase. The estimated effect of gestational age (weeks) corresponded to a 0.027 g/dL decrease in hemoglobin per additional week.
DISCUSSION
To our knowledge this is one of the largest studies of the occurrence of helminth infection in pregnant women in South America. It confirms the high prevalence of soil-transmitted helminth infections, particularly that of hookworm infection, in this vulnerable population. It also confirms the critical importance of ascertaining the intensity of infection. The higher the intensity of hookworm infection, the higher the proportion of anemic women. No association was found with prevalence. Although more than 90% of our population had no or light infections, we found a statistically significant association between moderate and heavy hookworm infection and anemia. This type of association has previously been demonstrated in Nepal35 and in Kenya.36 In both these studies, it appeared that intensity was associated with anemia after a threshold of infection had been reached (2,000 epg and 1,000 epg, respectively). We also observed a threshold at 2,000 epg in our study. The 2,000 epg threshold is consistent with the lower bound of the WHO category of moderate hookworm infection. Therefore, although the WHO categories of hookworm intensity are based on data obtained in child populations, our data suggest that the same categories may be applicable in pregnant populations.
The association between moderate and heavy hookworm infection and anemia was strengthened when there was co-infection with moderate and heavy Trichuris infection. It is of interest to note that, after adjusting for known covariates, these “infection” determinants were the only statistically significant determinants of anemia. This result also highlights the potential role of Trichuris infection in anemia. Being able to rule out malaria as a determinant of anemia in our study population likely contributed to these observations.
Further understanding of parasite determinants of anemia would be beneficial. In particular, it would be important to corroborate our findings in other pregnant populations in other geographical areas. This would produce evidence from populations having different hookworm species (and in different ratios), different intensities of hookworm (and other soil-transmitted helminths) and different anemia profiles (e.g., proportion iron-deficiency) among other concurrent host, parasite and host-parasite interaction determinants.
Our results provide additional evidence in support of the recommendation of WHO, UNICEF and INACG to include anthelminthic treatment in prenatal programs, in areas where the prevalence of hookworm infection exceeds 20–30%.37 Anthelminthic therapy is inexpensive, and in areas participating in the Global Program for the Elimination of Lymphatic Filariasis, albendazole is free of charge. An evaluation of the cost-effectiveness of including anthelminthics within prenatal care programs is urgently required. Benefits would also follow from an increased understanding of the effects of prenatal anthelminthic treatment on infant outcomes such as birth-weight, growth and development.
Prevalence of anemia and hookworm infection in 1,042 second trimester pregnant women living in Iquitos, Peru, 2003, by socio-demographic characteristics
| Variable | N (1,042) | Frequency (%) | Prevalence anemia (%) (Total: 47.31%) | P value* | Prevalence hookworm (%) (Total 47.22%) | P value* |
|---|---|---|---|---|---|---|
| * P values were based on χ2 test. | ||||||
| Age | ||||||
| < 25 years | 556 | 53.36 | 48.92 | 46.04 | ||
| ≥ 25 years | 486 | 46.64 | 46.64 | 0.462 | 48.56 | 0.417 |
| Environment | ||||||
| Live in periurban area | 968 | 92.90 | 47.73 | 46.07 | ||
| Live in rural area | 74 | 7.10 | 40.54 | 0.229 | 62.16 | 0.007 |
| Marital status | ||||||
| Married or “conviviente” | 970 | 93.09 | 46.39 | 47.84 | ||
| Single or other | 72 | 6.91 | 58.33 | 0.051 | 38.89 | 0.138 |
| Gestational age | ||||||
| Fourth month | 532 | 51.06 | 44.55 | 46.43 | ||
| Fifth month | 337 | 32.34 | 48.66 | 0.237 | 47.77 | 0.700 |
| Sixth month | 173 | 16.60 | 52.60 | 0.066 | 48.55 | 0.628 |
| Iron supplementation | ||||||
| Yes | 154 | 14.78 | 53.25 | 43.51 | ||
| No | 888 | 85.22 | 46.17 | 0.105 | 47.86 | 0.317 |
| First pregnancy | ||||||
| Yes | 195 | 18.71 | 47.18 | 37.44 | ||
| No | 847 | 81.29 | 47.23 | 0.990 | 49.47 | 0.002 |
| Have animals | ||||||
| No | 514 | 49.33 | 47.76 | 51.07 | ||
| Yes | 528 | 50.67 | 46.78 | 0.752 | 43.56 | 0.015 |
| Wear sandals outside the house | ||||||
| Yes | 950 | 91.17 | 48.11 | 46.53 | ||
| No | 92 | 8.80 | 37.90 | 0.058 | 54.95 | 0.123 |
| Wear sandals inside the house | ||||||
| Yes | 724 | 69.55 | 48.62 | 44.34 | ||
| No | 318 | 30.45 | 44.34 | 0.202 | 54.09 | 0.004 |
| House | ||||||
| Concrete | 97 | 9.31 | 49.48 | 25.77 | ||
| Brick | 65 | 6.24 | 38.46 | 0.164 | 41.54 | 0.039 |
| Wood | 347 | 33.30 | 33.30 | 0.005 | 42.07 | 0.002 |
| Palm tree material | 533 | 51.15 | 48.22 | 0.819 | 55.16 | < 0.001 |
| Floor | ||||||
| Concrete | 172 | 16.51 | 44.19 | 35.47 | ||
| Wood | 345 | 33.11 | 46.38 | 0.637 | 56.52 | < 0.001 |
| Dirt | 525 | 50.38 | 48.76 | 0.296 | 44.95 | 0.026 |
| Water | ||||||
| Bottled water | 60 | 5.76 | 46.67 | 33.33 | ||
| River | 78 | 7.50 | 52.56 | 0.494 | 57.69 | 0.004 |
| Well | 360 | 34.55 | 49.17 | 0.720 | 42.78 | 0.158 |
| Drinkable water from truck | 123 | 11.80 | 54.47 | 0.322 | 42.28 | 0.238 |
| Drinkable community water | 421 | 40.40 | 42.52 | 0.868 | 52.49 | 0.005 |
| Type of toilet facilities | ||||||
| Modern facilities | 23 | 2.21 | 34.78 | 26.09 | ||
| Latrines | 945 | 90.69 | 47.62 | 0.217 | 47.09 | 0.031 |
| Nothing | 74 | 7.10 | 45.95 | 0.339 | 55.41 | 0.01 |
| Schooling | ||||||
| Secondary completed | 263 | 25.19 | 48.09 | 24.81 | ||
| <secondary completed | 779 | 74.81 | 46.92 | 0.742 | 54.76 | <0.001 |
Prevalence and intensity of hookworm infection, and prevalence of anemia, in 1,042 second trimester pregnant women living in Iquitos, Peru, 2003
| Intenstiy categories | N | Prevalence of hookworm (%) | Prevalence of anemia (%) |
|---|---|---|---|
| Presence of infection | 492 | 47.22 | 48.78 |
| Absence of infection | 550 | 52.78 | 45.82 |
| None | 550 | 52.78 | 45.82 |
| Light | 435 | 41.75 | 47.13 |
| Moderate | 40 | 3.84 | 55.00 |
| Heavy | 17 | 1.63 | 76.47 |
| None and light | 985 | 94.53 | 46.40 |
| Moderate and heavy | 57 | 5.47 | 61.40 |
Relationship between intensity of soil-transmitted helminth infections and anemia (< 11 g/dL) during pregnancy, based on data from 1,042 second trimester pregnant women living in Iquitos, Peru, 2003
| Crude | Adjusted | ||||
|---|---|---|---|---|---|
| Variable | Reference group | OR | 95% CI | OR | 95% CI |
| OR, odds ratio; CI, confidence interval. | |||||
| Any hookworm | No hookworm | 1.13 | 0.88, 1.44 | ||
| Any Trichuris trichuria | No Trichuris | 1.01 | 0.73, 1.39 | ||
| Any Ascaris lumbricoides | No Ascaris | 0.83 | 0.64, 1.06 | ||
| Moderate and heavy hookworm | None and light | 1.84 | 1.06, 3.18 | 1.84 | 1.06, 3.17 |
| Moderate and heavy Trichuris | None and light | 1.26 | 0.96, 1.65 | ||
| Moderate and heavy hookworm and Trichuris | None and light hookworm and Trichuris | 2.14 | 1.10, 4.14 | 2.13 | 1.10, 4.13 |
Regression coefficients (β) and corresponding P values of variables found to be determinants of hemoglobin (g/dL) in 1,042 pregnant women living in Iquitos, Peru, 2003
| Variable | β | 95% CI | P value |
|---|---|---|---|
| CI, confidence interval. | |||
| Hookworm egg count (per 1000 epg) | −0.107 | −0.162, −0.052 | 0.0002 |
| Age | 0.012 | −0.0001, 0.023 | 0.0527 |
| Gestational age (per week) | −0.027 | −0.053, −0.001 | 0.0405 |
Iquitos, Department of Loreto, Peru.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 4; 10.4269/ajtmh.2005.73.783
Iquitos, Department of Loreto, Peru.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 4; 10.4269/ajtmh.2005.73.783
Iquitos, Department of Loreto, Peru.
Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 73, 4; 10.4269/ajtmh.2005.73.783
Address correspondence to Theresa W. Gyorkos, Division of Clinical Epidemiology, Livingston Hall, Room L10-420, Montreal General Hospital, 1650 Cedar Ave, Montreal, Quebec, Canada H3G 1A4. E-mail: theresa.gyorkos@mcgill.ca.
Authors’ addresses: Renee Larocque and Theresa W. Gyorkos, Division of Clinical Epidemiology, Livingston Hall, Room L10-420, Montreal General Hospital, 1650 Cedar Ave, Montreal, Quebec, Canada H3G 1A4, Telephone: 514-934-1934 ext 44721 or 44729, Fax: 514-934-8293, E-mail: renee.larocque@mail.mcgill.ca, theresa.gyorkos@mcgill.ca. Eduardo Gotuzzo, Instituto de Medicina Tropical Alexander von Humboldt, Universidad Peruana Cayetano Heredia, Honorio Delgado ave. 430, Urb. Ingeneria, San Martin de Porres, Peru, Telephone: 511-482-3903, Fax: 511-482-3404. Martin Casapia, Asociacion Civil Selva Amazonica, Urb. Jardin No. 27, Iquitos-Loreto, Peru, Telephone: 51-65-23-6277, Fax: 51-65-22-1827.
Acknowledgments: This study would not have been possible without the dedication and commitment of our research and administrative team in Iquitos, especially Obst. Carmen Nunez Rengifo, our local coordinator. We are grateful for the support of the DISA (Direccion de la Salud)-Loreto throughout the duration of this study. We also salute the personnel of the prenatal programs in the health centers attended by our study population who welcomed and assisted members of our research team enthusiastically and without any expectation of payment. We also express our deep gratitude to all the women who participated in our study, especially those who traveled great distances to attend our clinics. Finally, we acknowledge the statistical advice provided by Dr. Elham Rahme and Mr. Youssef Toubouti.
Financial support: This study was supported by a Canadian Institutes for Health Research (CIHR) operating grant no. MCT-53575 to Theresa W. Gyorkos.
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