Original Article

European Journal of Clinical Nutrition (2010) 64, 1108–1115; doi:10.1038/ejcn.2010.146; published online 11 August 2010

Trichuriasis and low-iron status in schoolchildren from Northwest Mexico

Guarantor: DWT Crompton and SP Diaz-Camacho. Contributors: LQC was the project leader and carried out most of the design, fieldwork, sample and data collection, parasitological and biochemical analysis, and writing of the paper. GGM carried out the data collection and preparation of the database and the paper. JER carried out the statistical analysis, data interpretation and writing of the paper. MEV supervised, assessed and supported the field study and wrote some parts of the paper. HA-G contributed with the data interpretation and writing of the paper. RO-M contributed with the data interpretation and writing of the paper. BIP-M contributed with the haematological and biochemical analyses. DWTC supervised the field study and assessed the writing content of the paper. SPD-C contributed with the design and logistic coordination of the study.

L Quihui-Cota1, G G Morales-Figueroa1, J Esparza-Romero1, M E Valencia1, H Astiazarán-García1, R O Méndez1, B I Pacheco-Moreno1, D W T Crompton2 and S P Diaz-Camacho3

  1. 1Department of Public Nutrition and Health, Centro de Investigación en Alimentación y Desarrollo AC, Sonora, México
  2. 2Department of Zoology, Institute of Biomedical and Life Sciences, University of Glasgow, Scotland, UK
  3. 3Department of Biological Sciences and Public Health, Universidad Autónoma de Sinaloa, Culiacán Sinaloa, México

Correspondence: Dr L Quihui-Cota, Department of Public Nutrition and Health, Centro de Investigación en Alimentación y Desarrollo AC, Carretera a la Victoria Km 0.6, Apartado Postal 1735, Hermosillo, Sonora, CP 83000, Mexico. E-mail: lquihui@ciad.mx

Received 25 May 2010; Revised 27 May 2010; Accepted 11 June 2010; Published online 11 August 2010.





The aim of this study was to investigate the association between trichuriasis and iron status in rural schoolchildren from Northwest Mexico.



A total of 73 schoolchildren (37 boys, 36 girls) between the ages of 6 and 10 years were voluntarily recruited from the public primary school of the rural community of El Higueral in Culiacan, Sinaloa (Northwest Mexico) for a cross-sectional study with a longitudinal follow-up of 5 weeks. Data were collected on socioeconomic status, anthropometry, haematological and biochemical indices of iron status, daily iron intake, and prevalence and intensity of trichuriasis. Multiple regression models, independent t-test and paired t-test were used to analyse the association between trichuriasis and iron status in cross-sectional and longitudinal samples, respectively. Adjusted models were tested for linear regression assumptions using residual plots.



The mean age of the Trichuris-free and Trichuris-infected groups was 7.7±1.3 and 7.7±1.5 years respectively (P=0.92). The height for age was significantly higher in the Trichuris-free group than the Trichuris-infected group (P=0.02). No differences were found in the socioeconomic variables between the two groups. At baseline, significantly higher concentrations of haemoglobin, haematocrit, blood cell count (RBC) and serum iron were measured in the Trichuris-free group compared with the Trichuris-infected children (P<0.05). An association was found between trichuriasis and haemoglobin adjusted for socioeconomic variables, age and sex. Haemoglobin, RBC and serum ferritin concentrations were significantly increased in the infected children 5 weeks after treatment (P<0.05).



Trichuriasis could be a risk factor for low-iron status in the schoolchildren of Northwest Mexico.


trichuriasis; iron status; Northwest Mexico; schoolchildren; rural area



Trichuriasis remains among the major intestinal helminth infections extending through tropic and subtropic areas worldwide. In 1979, the infection affected 500–700 million people in Africa, Asia and Latin America (Walsh and Warren, 1979). In 1999, the infection rate increased to 1049 million cases, including 114 and 233 million preschool and schoolchildren, respectively, and caused 220 million deaths (Crompton, 1999; Stephenson et al., 2000). In 2003, a global prevalence of 28, 24, 20, 19, 17, 7 and 2% was estimated for East Asia and the Pacific Islands, Sub-Saharan Africa, South Asia, China, India, the Middle East and North Africa, respectively, and 795 million people were suffering from trichuriasis, particularly younger people (De Silva et al., 2003). Conversely, iron deficiency remains the most prevalent and common micronutrient deficiency in the developing world (Tatala et al., 1998; Asobayire et al., 2001; Abalkhail and Shawky, 2002; Keskin et al., 2005). In 1991, iron deficiency anaemia (IDA) affected 1.3 billion people (Gillespie et al., 1991); in 2003, the figure increased to about 2 billion (Black, 2003). In 1989, 50% of schoolchildren in developing countries were anaemic (DeMaeyer et al., 1989) and IDA was estimated to have a prevalence of 23.4% in children aged 14–59 months in Mexico (Martínez-Salgado et al., 2008). Low education levels, poor quality of drinking water and sanitation, and crowding conditions can increase the prevalence of trichuriasis (Belo et al., 2005; Wani et al., 2007). A combination of these factors along with low dietary iron and increased requirements in infancy, adolescence and pregnancy can contribute to IDA (Fomon et al., 2003). The association between trichuriasis and IDA has been well documented (Otto, 1935; Burrows and Lillis, 1964; Layrisse et al., 1967; Robertson et al., 1992; Ramdath et al., 1994; Brito et al., 2003, 2006), as well as an association of IDA with premature delivery, low birth weight, altered gastrointestinal function, perinatal morbidity, decreased growth (Garn et al., 1981; Steer, 2000; Hamalainen et al., 2003), changes in behaviour, mental and motor development (Beard, 2003), lower iron transference to the foetus (Ramakrishnan, 2001), reduced physical work capacity (Haas and Brownlie, 2001) and an impaired immune system (Dallman, 1987). In Mexico, trichuriasis has remained an important human helminthiasis since the 1950s (Carrada-Bravo, 1988; Tay et al., 1995). Recently, a prevalence of 16% was estimated for trichuriasis in Northwest Mexico (Gutiérrez et al., 2007). However, a Mexican survey in 1999 revealed a prevalence of 14–22% in 8111 schoolchildren and 26% in the northern region (Villalpando et al., 2003) for anaemia, which remains a public health problem (Villalpando et al., 2006). The aim of this study was to investigate the association between trichuriasis and iron status in rural schoolchildren from Northwest Mexico. Specific objectives included (1) measuring iron status (serum iron, ferritin, transferrin and total iron-binding capacity (TIBC)) in Trichuris-free and Trichuris-infected schoolchildren; (2) investigating iron status after deworming in Trichuris-infected children and (3) measuring nutritional status in regards to growth, weight, diet, and environmental and socio-demographic factors. We hypothesized that, under the local living conditions, schoolchildren from Northwest Mexico may be at risk for low-iron status associated with trichuriasis.


Subjects and methods

Study population

This study was conducted from January to June in a public primary school of the rural community of El Higueral in the municipality of Culiacan, Sinaloa in Northwest Mexico. The study site was selected on the basis of having a population less than 2500 inhabitants, low socioeconomic status (INEGI, 1990), and a high rate of ascariasis and trichuriasis infections associated with high morbidity rates in the general population (Secretaría de Salud, 1998, 1999). There were official meetings with personnel from Health Services, city councils and the primary school, as well as parents and schoolchildren from the study site to explain the purpose of the study. In total, 47% (n=101) of the registered school population (n=215) between the ages of 6 and 10 years at the study site (Secretaría de Educación Pública, 1999) agreed to participate in the intestinal parasite screening. Plastic containers were distributed and faecal samples were requested. A total of 73 children (72%) met the study criteria (voluntary participation supported by their parents, no immediate medical treatment, and no minerals or vitamins supplementation and/or anti-parasitic treatment) and they were categorized as 33 and 40 Trichuris-infected and Trichuris-free schoolchildren, respectively. Excluded children included 14 (14%) who provided fewer than three faecal samples, 6 (6%) infected with T. trichiura plus another pathogen (Ascaris lumbricoides, Hymenolepis nana and Entamoeba histolytica/dispar), 5 (5%) with current parasitic treatment or iron supplementation and 3 (3%) with anaemia lower than 90g/l.

Ethical considerations

Written consent for the children to take part in the study was obtained from their parents or guardians. Children requiring medical attention were properly treated. Children older than 10 years were not included because gender has an effect on serum iron levels after the first decade of life (Pilch and Senti, 1984).

The ethical committee of the Centro de Investigación en Alimentación y Desarrollo AC (CIAD AC) and the Facultad de Ciencias Biologicas and Departmento de Salud Pública de la Universidad Autónoma de Sinaloa granted approval to conduct this study.

Study design

This study was cross-sectional with a longitudinal follow-up of 5 weeks after anti-parasitic treatment. Data collection, collection and processing of stool samples, anthropometry measurements and iron status determinations were performed at baseline and repeated 5 weeks after treatment.

Stool sample collection and analysis

A total of 219 and 180 stool samples were collected at baseline and follow-up, respectively (3 per subject), over a 5-day period in the selected school. The plastic containers were labelled properly and contaminated stool samples (water, urine and sand) were rejected. Iceboxes were used during sampling and transportation, and samples were kept between 4 and 7°C until analysis.

Each stool sample was analysed 1–10h after collection using the techniques of Faust and Kato Katz according to international recommendations (WHO, 1991; Markell and Voge, 1992). The intensity of infection was indirectly estimated by counting the number of eggs per gram of faeces (epg) (Stephenson and Holland, 1987). The infection status was categorized as 0 or 1 for the absence or presence of Trichuris infection, respectively, and 0 or 1 for an epg less than or greater than 100, respectively.

Anthelmintic treatment

Albendazole was orally administered to Trichuris-infected schoolchildren in a 400mg per day dose for 2 successive days. Treatment was repeated when necessary to ensure the elimination of Trichuris infection. A qualified physician prescribed the treatment.

Dietary assessment

Daily intake of iron was estimated using the 24h recall method (Sanjur and Rodríguez, 1997). Two interviews were administered to the children in the presence of their mother or tutor. The first interview was performed during blood sample collections and repeated 5 weeks later. A dietary intake of 4.1mg of iron per day is recommended for children aged 4–8 years, and 5.9 and 5.7mg for boys and girls aged 9–13 years, respectively (IOM, 2001). Dietary intake was categorized as 1 or 0 for intake equal/above or below the recommendation.


Socioeconomic status (Méndez, 1978) was assessed by parent employment status (employed=0; unemployed=1) and parents’ education in years assessed on a scale ranging from 1 to 6 years of primary school, and incomplete (0) or complete primary (1). Household conditions were assessed as the type of material used for walls, roofs and floors, and categorized on the basis of local costs. Sanitation facilities were assessed as defecation in open area (0), pit/latrine (1), and drinking water was assessed as tap water (0) or treated water (chlorine/boiled) (1). Family size and crowding index (number of people per room) was categorized into <2 people (0) or >2 people (1). Family income was assessed as a continuous variable and estimated as the number of minimum daily wages by dividing the daily family income by the minimum daily wage (Comisión Nacional de Salarios Mínimos, 1999).

Standing height was measured using a stadiometer (Holtain Ltd, Dyfed, UK) with 2.05±0.0005m capacity, and weight was measured to the nearest 50g using a digital electronic scale (AND FV-150 KA1; A&D Co. Ltd., Tokyo, Japan). Ages were validated from birth certificates. Undernutrition was defined as below −2 standard deviation units (−2 Z-scores) from the median reference values defined by the World Health Organization (WHO, 1986), using the nutritional indices of height for age (H/A; stunting), weight for age (W/A) and weight for height (W/H; wasting) (NCHS, 1978).

Under fasting conditions, a 10ml sample of venous blood was taken from the cubital vein of each child using a set of needles (23 × 19mm) and Vacutainer glass tubes (13 × 100mm) with SST Gel and Clot activator to separate the serum fraction. A 3ml whole-blood sample (heparinized) was analysed within 2h to determine the red blood cell (RBC) count, mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH) and mean corpuscular haemoglobin concentration (MCHC) as well as haemoglobin (Hb) using Drabkin's technique and haematocrit using capillary tubes (Dacie and Lewis, 1991). The remaining 7ml lacking anti-coagulant was kept at room temperature (2h) and allowed to clot for serum separation by centrifugation (1100g for 10min) at the laboratory of the Autonomous University of Sinaloa. Aliquots of 2.5ml were poured into cryogenic glass screw-cap vials and stored at −20°C until iron-indicator determinations. Serum iron and TIBC were measured using the Beckman Synchron CX System (chemical information for in vitro diagnostic use of reactives; Beckman Instruments Inc., Brea, CA, USA). Transferrin saturation was calculated by dividing the serum iron by TIBC. Serum ferritin was measured using Coat-A-Coat Ferritin IRMA (For in vitro diagnostic use of reactives; Diagnostic Products Corporation, Los Angeles, CA, USA). Iron deficiency and IDA were defined as a serum ferritin concentration less than 15μg/l and Hb concentration less than 120g/l, respectively, using the age- and sex-specific thresholds proposed in 2001 by UNICEF and WHO (WHO, 2001).

Statistical analysis

Data were analysed using NCSS 2000 (NCSS Statistical Software, Kaysville, UT, USA) and Pless than or equal to0.05 was considered statistically significant. Descriptive statistics were expressed as mean±standard deviation (s.d.) in the case of age, height, Z-scores and monthly family income. Proportions were used for infection, gender, employed parents, type of house material and sanitation facilities. χ2-Test and t-test were used to compare proportions and continuous variables, respectively, between the groups. Logarithmic transformation was used for continuous variables with skewed distribution. Geometric mean±confidence interval was used to express epg counts.

The association between trichuriasis and iron status in rural schoolchildren from Northwest Mexico was analysed in cross-sectional and longitudinal data using multiple regression model independent t-test and paired t-test. In all models, the dependent variable was the indicator that defined iron status. In the cross-sectional analysis, the independent variable was the absence (0) or presence (1) of Trichuris infection, and 0 or 1 when Trichuris infection intensity was less than or equal to500 or >500 epg. In addition, age (Bundy et al., 1987), socioeconomic status (Belo et al., 2005; Wani et al., 2007), Z-scores (Saldiva et al., 1999) and daily iron intake (Holland, 1987) were considered as potential co-variables. In the longitudinal analysis, the indicators that defined iron were compared between them at baseline and after treatment in the infected group.

The adjusted multiple regression models were constructed using the variables significantly associated with infection by using bivariate analysis and stepwise model selection. In addition, sex and age were introduced in the adjusted model 1, although they were not significant in the bivariate and stepwise analysis. Final adjusted models were tested for linear regression assumptions using residual plots.



The average age of the schoolchildren was 7.6±1.1 years at baseline. Of them, 49% were girls (n=36). The proportion below −2s.d. in W/A and H/A (stunting) was 5.5 and 4%, respectively, and no cases of wasting (W/H) were detected in this study. Means for W/A, H/A and W/H were −0.09±1.07, −0.26±1.08 and 0.17±0.91, respectively, and no significant differences were found between boys and girls (P>0.05). The mean ages of the Trichuris-free and -infected groups were 7.7±1.3 and 7.7±1.5 years, respectively (P=0.9), and the geometric mean of epg for T. trichiura was 719.4 (95% CI, 572–820). The H/A was significantly higher in the Trichuris-free group compared with the Trichuris-infected group (−0.006 vs −0.57, P=0.02). No difference was found in the W/A, W/H and daily iron intake between the groups (P=0.38, 0.97 and 0.10 respectively; Table 1).

Approximately 95% of the fathers and 71% of the mothers had formal jobs at the time of the interviews. The fathers and mothers represented the family economic support. Primary education was completed by 13.4 and 11.3% of the fathers and mothers, respectively. χ2-Analysis showed no significant difference between the Trichuris-free and -infected groups in parental employment and education (P>0.05), the quality of walls (P>0.05) and roof (P>0.05), the use of bare-earth floor (P>0.05), pits for faeces disposal (P>0.05), treated drinking water (P>0.05), overcrowding (P>0.05) or family income (P>0.05).

The two-sample independent t-test analysis showed significantly higher concentrations of Hb (127 vs 122, P=0.0006), haematocrit (38.5 vs 37.3, P=0.03), RBC (4.4 vs 4.3, P=0.03) and serum iron (101.2 vs 82.3, P=0.04) in the Trichuris-free children compared with the Trichuris-infected children. No difference was found in the rest of the iron indicators between the groups (P>0.05; Table 2).

Because covariates other than Trichuris infection may influence iron status, different models were constructed to analyse the differences after adjusting for significant and/or biologically related variables. The negative effect of T. trichuris on iron status was shown in different adjusted models (model 1: β=−0.044, P=0.001; model 2: β=−0.044, P=0.001, for Trichuris-infected vs Trichuris-free children). Table 3 shows the association between trichuriasis and Hb (log-transformed) adjusted for the socioeconomic variables along with age and sex (Model 1) and the association between trichuriasis and Hb (log-transformed) adjusted for the socioeconomic variables (Model 2), which includes only significant variables. Finally, in the longitudinal data analysis a significant increase was found in the Hb, RBC and serum ferritin concentrations after 5 weeks of treatment in 33 Trichuris-infected schoolchildren. No change was observed in the rest of the iron indicators (Table 4). Mean daily iron intake before and after treatment was 15.5 and 14.8mg per day respectively (P=0.610).



Of the Trichuris-free and Trichuris-infected children, 30% (n=12) and 24% (n=8) consumed 81% and 75% of the recommended daily iron intake respectively (IOM, 2001). It was in agreement with Villalpando et al. (2003) who found similar percentages of recommended daily iron intakes (70–80%) in 2057 Mexican children aged 5–11 years in 1999 (Villalpando et al., 2003). This study noted a high percentage of schoolchildren on iron-deprived diets in the country. Iron deficiency is one of the major micronutrient deficiencies in Mexico (Martínez-Salgado et al., 2008). The prevalence of anaemia in children between 5 and 11 years of age from the north, south and central Mexican regions was 23.8, 21.6 and 18, respectively, in 1999 (Villalpando et al., 2003). In this study, 8 (11%) of the 73 recruited schoolchildren (4 Trichuris infected and 4 Trichuris free) had Hb concentrations less than 115g/l. The prevalence of anaemia was lower than that reported for the northern region, but our sample size cannot provide a representative figure for anaemia. IDA and trichuriasis have been found to be associated conditions that result independently from multiple factors. It has been well documented that low socioeconomic conditions promote Trichuris transmission. Belo et al. (2005) found an association between lax sanitation practices and trichuriasis in 514 schoolchildren. Wani et al. (2007) associated untreated water, lax hygiene, maternal education and bare-earth floors in the households with a high prevalence of trichuriasis in India. The metal laminate used for walls was a risk factor in this study in comparison with the use of brick/cement material. Our study was carried out in an underprivileged area. Therefore, no difference was found in the socioeconomic characteristics between the recruited Trichuris-free and Trichuris infected children (Data no shown). On the other hand, trichuriasis has been recurrently associated with undernutrition. Gutierrez-Rodríguez et al. (2007) showed an association between trichuriasis and stunting in 243 children (65.3±8.7 months) in a southwest region of Mexico. A similar association was also found in this study, but no association was observed between trichuriasis and W/A. In this study, no case of wasting was observed. It is likely that children with chronic nutrient deficiency and infections have a stature adapted to the lower weight and appear to have a normal W/H, but they show ‘homeorrhesis’ (Flores et al., 1983). Trichuriasis is recognized as an insidious disease and is rarely present as an acute infection (Cooper and Bundy, 1988). A total of 150 cases of non-acute trichuriasis were recorded from 1993 to 1996 in the general population of the study site (Secretaría de Salud, 1998). The chronic condition makes it easier for trichuriasis to act as a risk factor for decreased iron status. Ramdath et al. (1995) observed an association between trichuriasis and lower Hb, MCV, MCH and MCHC. A study in Brazil associated IDA with chronic trichuriasis in 299 children aged between 4 and 14 years (Ferreira et al., 1998). Our cross-sectional data associated trichuriasis with lower Hb, haematocrit, RBC and serum iron, but not MCV, MCH, MCHC, TIBC, transferrin saturation or serum ferritin. However, only heavy trichuriasis has been associated with anaemia. In 1954, Brown found an association between epg counts ranging from 17000 to 224000 and anaemia (<100g/l) in eight patients (Brown, 1954). Ramdath et al. (1995) associated lower Hb (115±13g/l) concentrations with Trichuris infections of more than 10000 epg in 421 schoolchildren. Greenberg and Cline (1979) studied 86 Trichuris-infected children and found an association between epg counts ranging from 10500 to 32860 and anaemia (<119g/l). However, more slightly Trichuris-infected children did not show anaemia (Hb, 120–124g/l). In this study, epg counts no higher than 900 were found, and Hb values indicative of anaemia were not associated with the slight intensity of trichuriasis, but significantly lower Hb was observed in the Trichuris-infected group in agreement with Greenberg and Cline (1979). In addition, an association was not found between trichuriasis intensity and Hb concentration and no difference was found in the Hb concentrations between children with lower and higher intensity of trichuriasis. Notably, albendazole administered by the Mexican campaign (WHO, 1996) is probably affecting the Trichuris egg excretion, masking the real epg counts in infected children and the association of Trichuris intensity with iron status in this study. However, the follow-up analysis revealed a significant increase in the Hb and RBC concentrations in the treated children. Also, 2 from the 4 anaemic of the 33 Trichuris-infected children had improved Hb concentrations from 94 to 124g/l and from 110 to 128g/l after treatment and they had 100 and 200 epg counts respectively. It is noteworthy to mention that dietary iron showed no association with the iron indicators and questionnaires revealed that iron or any other nutrients supplementation was not given at any time during the study course (before starting and follow-up).

Because no difference was found in the ferritin concentrations of infected and non-infected children, its significant increase after treatment was carefully interpreted. Ferritin is recognized to be an acute-phase reactant in the responses to multiple infections (Baynes, 1996). Unfortunately, C-reactive protein was not included in our study to clarify this finding (Karyadi et al., 1996). Although limitations exist, such as the lack of a placebo-matched group, albendazole treatment being the sole intervention, and no association found between trichuriasis and IDA or Trichuris-intensity and iron status in the cross-sectional analysis, the significant increase of Hb adjusted by covariates in the treated group is strong evidence that trichuriasis may be a contributing factor for low-iron status. The national deworming campaign is administering a twice yearly single dose a day of albendazole (WHO, 1996) but it is recognized that multiple doses of albendazole are needed to attain complete parasitological and clinical cure of trichuriasis (Geltman et al., 2003). Therefore, Mexican populations with low intake of dietary iron, high iron requirements and inhabiting in trichuris endemic areas are at high risk of iron deficiency, even in those areas with probably low prevalence and intensity of trichuriasis such as in our study. This health scenario will not improve unless the Mexican health programmes generate information regarding the epidemiology of intestinal parasite infections that is required to redesign the current national deworming programme and others related to micronutrient supplementation or fortification, to improve the quality of life of the most vulnerable populations.


Conflict of interest

The study protocol was approved by the research and ethical review boards of the Center of Research on Food and Development (CIAD) unit of Hermosillo Sonora, and the Health Public Department of the Autonomous University of Sinaloa, in Mexico. Informed consent was obtained from children's parents or legal guardians. RIMSA Laboratories, which sponsored the drug albendazole used in this study, did not participate in the study protocol, analysis of results, manuscript redaction, the reference used and the journal selection for publication. In addition, none of the authors had commercial links or work relationship with RIMSA Laboratories at the time of the study development. The Consejo Nacional de Ciencia y Tecnología CONACYT), the University of Glasgow, the Universidad Autonoma de Sinaloa, the Secretaría de Educación Pública and the Centro de Investigación en Alimentación y Desarrollo AC provided economic support to this study and they had no competing interests for the study development. Luis Quihui-Cota was a recipient of a research scholarship from CONACYT and he declares that the work described in this study is a part of the entire work of his PhD thesis. In addition, it is entirely of his own composition and was not in whole or part submitted for any other degree or international or national publication. In fact, results were re-analysed by an expert using the most appropriate statistical methods and revised by the authors. All authors have knowledge about it and the participant institutions have signed copies of the technical reports sent to CONACYT by Luis Quihui Cota as a supported PhD student of the University of Glasgow. Therefore, the authors do not have competing or financial interests in publishing this study. If complete information for academic purposes is required from the PhD thesis of Luis Quihui, a special authorization must be requested to the Head of the Division of Infection and Immunity of the University of Glasgow, Joseph Black Building, Glasgow G12 8QQ, UK.



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