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2 Department of Human Nutrition, The Royal Veterinary and Agricultural University, Frederiksberg, Denmark; 3 International Centre for Diarrhoeal Disease Research, Bangladesh (ICDDR,B): Centre for Health and Population Research, Dhaka, Bangladesh; and 4 Department of Epidemiology, Institute of Public Health, University of Copenhagen, Copenhagen, Denmark
* To whom correspondence should be addressed. Email: kak{at}kvl.dk, katjakongsbak{at}yahoo.dk.
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ABSTRACT |
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 TOP ABSTRACT IntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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1-antichymotrypsin, reported morbidity, Ascaris lumbricoides and Trichuris trichiura infections, parental education as well as stunting, underweight, and wasting on serum zinc were estimated. Serum zinc (mean ± SD) was 9.7 ± 1.1 µmol/L. Elevated serum CRP levels, T. trichiura infection, and stunting were negative predictors of serum zinc, whereas maternal education was a positive predictor. Compared with serum CRP <1 mg/L, CRP levels of 2 to <5, 5 to <10 and 
10 mg/L were associated with 0.33, 0.73, and 0.89 µmol/L lower serum zinc, respectively. The prevalence of low serum zinc (<9.9 µmol/L) fell from 59.3 to 49.7% in the whole population, after correcting for the effect of CRP and was 50.0% in the healthy subgroup (CRP <2 mg/L). The prevalence of low serum zinc was high but overestimated due to the effect of the acute phase response. Interventions to address low serum zinc in Bangladesh are warranted. Controlling T. trichiura infection and improving maternal education may be important interventions. The use of multiple categories of acute phase proteins and cut-off values that indicate elevated levels warrant further research.
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Introduction |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Plasma and serum zinc concentrations are widely used biochemical indicators of zinc status to identify populations at risk of zinc deficiency. However, the acute phase response (APR)5 which may occur in infections and/or trauma, is associated with depressed serum zinc concentration (serum zinc) in some studies (10–15), whereas in 3 community-based studies in children, no depression in serum zinc was found (11). Because subclinical infections are common in populations at risk of zinc deficiency, the interpretation of serum zinc may be hampered and the prevalence of low serum zinc may be overestimated because the proposed cut-off value (1) does not take this into account. It has been suggested that acute phase proteins (APPs) may be used to control for the confounding effect of the APR (16) and, when assessing the prevalence of low serum zinc, by correcting individual serum zinc values and identifying the healthy subgroup (individuals with no elevated APP) (13). To our knowledge, no studies in apparently healthy children (3–7 y old) have examined the effect of serum concentrations of C-reactive protein (CRP), 1-antichymotrypsin (ACT), or other APPs on serum zinc or attempted to quantify the fall in serum zinc due to the APR by using multiple categories for CRP and ACT.
Better identification of populations at risk of low serum zinc as well as predictors that may have a positive or negative effect on serum zinc is important for designing targeted interventions aimed at improving zinc status in children. We therefore conducted a cross-sectional study in apparently healthy children from a Dhaka slum with the following specific objectives: 1) to investigate the effects of age, gender, reported morbidity, helminthic infections, parental education, as well as anthropometric indicators on serum zinc, while controlling for APPs (CRP and ACT); and 2) to estimate the fall in serum zinc due to the effect of the APPs as well as assess the prevalence of low serum zinc, in both the whole population after correcting for the effect of CRP and in the healthy subgroup.
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Subjects and Methods |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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This study was conducted primarily to screen children for low serum retinol with subsequent enrollment in a vitamin A efficacy trial. Children of both genders (3–7 y old) were identified from 4 selected neighboring camps through a house-to-house survey by field assistants familiar with the area. Children who had received vitamin A supplements within the preceding 6 mo were excluded. Severely undernourished children [weight-for-height <70% and weight-for-age <60% of the United States National Center for Health Statistics (NCHS)/WHO international reference median] and those with serious illnesses such as clinical signs of vitamin A deficiency, measles, and tuberculosis as well as chronic diseases were excluded and referred to the Dhaka Pediatric Hospital, Dhaka Medical College Hospital, or Chest Disease Hospital for diagnosis and treatment. Bitot's spots (X1B) were treated with an oral dose of vitamin A [retinyl palmitate; 200,000 IU (60 mg)] twice, with a 14-d interval. Children (n = 579) were apparently healthy, showing no signs and symptoms of acute illness such as fever, acute diarrhea, dysentery, pneumonia, or acute respiratory tract infection, at the time of blood collection.
Before conducting the study, it was presented to and accepted by the community leaders. Written or oral informed consent was obtained from each child's parent or legal guardian. The study protocol was approved by the Research Review Committee and Ethical Review Committee, International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B). All children and their family members had free access to the health services including medicines given by the physicians at the health clinic/project office. Records were kept of diseases and medicines provided to the study children. Children with serum retinol <0.35 µmol/L received an oral dose of vitamin A (200,000 IU), and were excluded from further study.
Data collection. After consent and household socioeconomic status (SES) information were obtained, feces collection, clinical examination, and anthelminthic treatment were conducted. Later, a 2-wk morbidity recall interview and clinical examination including blood collection were completed on the same day.
Clinical examination. Signs and symptoms of illness in the children were obtained by history from their parents/caregivers, and they were examined clinically using a structured questionnaire by 2 experienced physicians. Body temperature, pulse, and respiration rate were measured and an appraisal was made on the basis of appearance, pallor, edema, condition of the skin, throat, heart, lungs, and abdomen, and signs of vitamin A deficiency. Information on the date of the most recent intake of a vitamin A capsule and immunization status was obtained from parents/caregivers or health cards.
Height and weight were measured with the child wearing light clothing and no shoes. Height was measured to the nearest 0.1 cm using a locally made wooden height board. Weight was measured to the nearest 0.1 kg using an electronic scale (Seca), which was calibrated daily. Mid upper arm circumference (MUAC) was measured to the nearest 2 mm using Teaching Aids at Low Cost insertion tapes. Height and MUAC measurements were made twice (CVs <1%) and the mean was used as the reported value. Weight was measured once. All measurements were performed by trained nutritionists and monitored by a senior nutritionist. The CVs of intra-and interobserver variations were <1%. Z-scores of height-for-age (HAZ), weight-for-age (WAZ), and weight-for-height (WHZ) were calculated using the NCHS/WHO international reference population (19) and ANTHRO software (20). Children with HAZ, WAZ, and WHZ less than –2 were considered stunted, underweight, and wasted, respectively (19).
Blood collection. Venous blood (4 mL) was collected from nonfasting children between 0900 and 1300, using trace element–free plastic syringes and stainless steel needles. Blood was injected into evacuated tubes (Venoject II, Terumo Europe), which were wrapped in aluminum foil, transported to the Nutritional Biochemistry Laboratory, ICDDR,B, and centrifuged (1000 x g for 10 min at room temperature) within 5 h. Serum was transferred using trace element–free pipettes into cryovials (Simport) and stored immediately at –20°C until analyzed for zinc and CRP at ICDDR,B. Serum was transported on dry ice to Denmark for analysis of ACT at the Department of Human Nutrition, The Royal Veterinary and Agricultural University.
Socioeconomic status and morbidity.
Eight trained female field assistants, assisted by 8 local women maintained close contact and motivated the families; they also conducted the SES and the 2-wk morbidity recall interviews. Data were collected through household visits, using precoded and pretested questionnaires in Bangla. On the day consent was obtained, SES information was collected. Only data on household size and parental education are presented here. On the day of blood collection, morbidity data were collected and the mother/caregiver was interviewed about the presence or absence of 6 symptoms in the past 2 wk. Physicians at the project office supervised the work and attended to sick children. Diarrhea was defined as 3 loose or watery stools in a 24-h period. To ensure good data quality, the SES and morbidity questionnaires were checked for inconsistencies just after collection. SES supervisors and physicians made spot checks and reinterviewed a random subsample of 5% of the households. A few minor adjustments were made and feedback given to the interviewers.
Feces collection, feces examination, and anthelminthic treatment. A plastic container was provided by the field assistant during the collection of SES data. The parent/caregiver was asked to collect a feces sample from the child in the early morning of the following day. The fresh feces sample in normal saline was examined microscopically by direct smear and the presence of trophozoites of Giardia intestinalis and Entamoeba histolytica was verified. In addition, 1–2 g of fresh feces were fixed in 10% formalin in normal saline and later processed by a quantitative ether sedimentation technique (21) before microscopic examination to estimate the intensity of helminthic infections of Ascaris lumbricoides, Trichuris trichiura, and hookworm, expressed as eggs per gram feces (epg). Feces samples were analyzed at the Parasitology Laboratory, ICDDR,B by an experienced laboratory technician.
After collection of the feces sample, the child was given anthelminthic treatment. A chewable tablet of 400 mg albendazole (Albizol, Opsonin Chemical Industries) was given under supervision to each child twice, with a 2-wk interval. The second dose was given 3–5 wk before blood collection.
Biochemical analyses. Serum samples (n = 579; 150 µL) were diluted (1:12) with deionized water, and zinc concentration was measured using flame atomic absorption spectrophotometry (Shimadzu AA-6501S) (22). A standard curve was prepared from a commercial zinc nitrate standard solution (BDH Laboratory Supplies) in concentrations of 0.1, 0.2, 0.3, and 0.4 mg/L. The accuracy was verified with each set of samples using commercial serum zinc quality controls (Utak Laboratories) of normal (12–18 µmol/L) and high (34–52 µmol/L) levels as well as triplicate forms of a pooled human serum sample. For normal and high levels of zinc quality controls, the within-day CVs were 2.6 and 1.0%, respectively, and the between-day CVs were 3.4 and 1.8%, respectively. Serum CRP (n = 577, insufficient serum from 2 children) was measured by immunoturbidimetric assay (Hitachi 902 Automatic Analyzer) using commercial kits and quality control materials (Roche Diagnostics). The recovery of serum CRP was 95–105%. The accuracy was verified with each run by analyzing quality controls of serum CRP of low (13.9–22.9 mg/L) and high (35.6–58.4 mg/L) levels. For low and high levels of controls, the within-day CVs were 2.5 and 1.0%, respectively, and the between-day CVs were 3.4 and 1.2%, respectively. Serum ACT (n = 566, insufficient serum from 13 children) was measured by turbidimetry (Cobas Mira Plus Automatic Analyzer, Roche) as described by Friis et al. (23). The accuracy was verified by daily runs of commercial human serum protein quality controls (DAKO) of low (0.21–0.29 g/L) and high (0.51–0.69 g/L) levels. Within-day and between-day CVs for ACT were 2.1 and 3.2%, respectively.
Statistical methods.
Data were entered twice and cleaned in Fox Pro (Microsoft) and analyzed using SPSS for Windows (version 12.0, SPSS). Normal probability plots were used to assess whether continuous variables were normally distributed. The outcome variable, serum zinc, conformed with normality. A 2-sample t test or 1-way ANOVA with Tukey's multiple comparison post hoc tests was used to test for differences in means. Differences in proportions were compared using Pearson's 
2 test or continuity correction test when appropriate. Multiple linear regression analysis was used to identify and estimate statistical effects of predictors of serum zinc. Variables assessed were age, gender, serum CRP and ACT, reported diarrhea, nasal discharge, cough, fever, common cold and angular stomatitis, T. trichiura and A. lumbricoides infections, as well as maternal and paternal education. Age and gender were forced into the model. In another multiple linear regression model, stunting, underweight, and wasting were included. Age (y) was a continuous variable. Dummy variables were used to assess the effects of gender, reported morbidity, presence of helminthic infections, anthropometric indicators, APPs, and parental education. Serum CRP was arbitrarily categorized as <1, 1 to <2, 2 to <5, 5 to <10 and 10 mg/L and ACT as <0.3, 0.3–0.4, and > 0.4 g/L. Education was categorized as 0, 1–5, and 6+ y of schooling. If helminthic infections were found to be predictors, the effect of the intensity of infection was assessed after log10(epg+1) transformation. Interaction between age and gender was tested. Serum zinc values <9.9 µmol/L were considered low (1). To calculate the prevalence of low serum zinc in the whole population corrected for the APR, 3 dummy variables, serum CRP, serum ACT, and gender as well as age, were tested in the multiple linear regression analysis. Subsequently, the individual serum zinc concentrations were increased by the estimated fall due to the effect of CRP before categorization. Data were analyzed using stepwise selection, and variables with P-values < 0.10 were retained in the multiple regression model. P-values < 0.05 were considered significant. Residual analysis including normal distribution, and homogeneity of variance of standardized residuals was carried out by investigating normal probability plots and plotting standardized residuals against predicted values.
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Results |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Helminthic infections of A. lumbricoides and T. trichiura were common (Table 1), whereas hookworm (1.2%, n = 7) as well as trophozoites of Giardia intestinalis (0.9%, n = 5) and Entamoeba histolytica (0.7%, n = 4) were rare. Among the 579 children, the prevalence of reported morbidity was cough, 25.4%; nasal discharge, 19.7%; fever, 19.3%; common cold, 18.0%; diarrhea, 13.8%, and angular stomatitis, 3.3%. More than half of the children had low serum zinc (Table 2), and 52.5% had serum CRP 2 mg/L. Among 296 children with serum CRP 2 mg/L, 83.5% had serum ACT 
0.4 g/L.
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0.4 g/L and >0.4 g/L, the proportions of children with low serum zinc were 57.9% (n = 294/508) and 69.0% (n = 40/58), respectively.
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Stunted children had 0.27 µmol/L (95% CI: 0.09, 0.45; P = 0.003) lower mean serum zinc than those not stunted. Similarly, mean serum zinc was 0.19 µmol/L (95% CI: 0.01, 0.37; P = 0.04) lower in underweight children than in those not underweight. Among wasted children, the mean serum zinc tended to be lower (0.25 µmol/L; 95% CI: –0.02, 0.53; P = 0.07) than those not wasted.
Predictors of serum zinc. Using multiple linear regression analysis, elevated serum CRP levels, T. trichiura infection, and maternal education were predictors of serum zinc (Table 4). Even though age was not a predictor, there was a tendency for mean serum zinc to increase with every 1 y increase. Gender, serum ACT, reported diarrhea, nasal discharge, cough, fever, common cold and angular stomatitis, A. lumbricoides infection, and paternal education were not associated with serum zinc and there was no interaction between age and gender.
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10 mg/L were associated with lower serum zinc (Table 4). The depression in serum zinc was similar in the categories of CRP 5 to <10 and 10 mg/L (P = 0.59) and higher (P = 0.005 and P = 0.006, respectively) than that in the category of CRP 2 to <5 mg/L. T. trichiura assessed as the intensity of infection after log10(epg+1) transformation was also a negative predictor of serum zinc (P = 0.001). The regression coefficient of –0.12 µmol/L (95% CI: –0.19, –0.05) corresponded to a 0.12 µmol/L decline in serum zinc/unit increase in log10(epg+1). When serum CRP was taken out of the model, the regression coefficients of the predictors T. trichiura and maternal education did not change considerably. However, reported nasal discharge approached significance as a negative predictor (P = 0.05), suggesting that its effect, unlike that of the other predictors, tended to be mediated or confounded by the APR (data not shown).
Elevated serum ACT was found to be a predictor of serum zinc but only when serum CRP was not included in the model (intercept: 9.6 µmol/L (95% CI: 9.2, 9.9); adjusted R2 = 0.051; n = 547). Using serum ACT 0.3 g/L as the reference category, serum ACT > 0.4 g/L was associated with 0.56 µmol/L (95% CI: 0.25, 0.86; P < 0.001) lower serum zinc, whereas serum ACT 0.3–0.4 g/L was not a predictor of serum zinc (regression coefficient = –0.07 µmol/L (95% CI: –0.27, 0.12); P = 0.47). The predictors of serum zinc in this model were similar to those found in the model with serum CRP, and the regression coefficients did not change considerably (data not shown).
In the multiple linear regression model including the anthropometric indicators, stunting was associated with 0.20 µmol/L (95% CI: 0.02, 0.37; P = 0.03) lower serum zinc than no stunting (intercept: 10.2 µmol/L (95% CI: 9.9, 10.4); adjusted R2 = 0.097; n = 558). Underweight and wasting were not associated with serum zinc, and the estimates of the predictors elevated serum CRP levels, T. trichiura infection, and maternal education were not affected. The significant difference observed in mean serum zinc in children underweight and not underweight in the bivariate analysis, suggests that the difference was mediated or confounded by the other predictors in the multiple regression analysis. When age and gender were retained in the model (P = 0.19 and P = 0.37, respectively), stunting tended to be associated with lower serum zinc (regression coefficient = –0.17 µmol/L (95% CI: –0.35, 0.009); P = 0.06).
Estimated effects of serum C-reactive protein for correcting the prevalence of low serum zinc.
In the multiple linear regression model, only elevated serum CRP levels were predictors of serum zinc (intercept: 10.0 µmol/L (95% CI: 9.8, 10.2); adjusted R2 = 0.061; n = 577) whereas serum ACT, age, and gender were not. Using serum CRP <1 mg/L as the reference category, the estimated effect of serum CRP levels 1 to <2, 2 to <5, 5 to <10 and 10 mg/L on serum zinc, expressed as regression coefficients were: –0.08 µmol/L (95% CI: –0.33, 0.18; P = 0.55); –0.33 µmol/L (95% CI: –0.57, –0.09; P = 0.006); –0.73 µmol/L (95% CI: –1.02, –0.43; P < 0.001) and –0.89 µmol/L (95% CI: –1.27, –0.50; P < 0.001), respectively. The prevalence of low serum zinc decreased by 10 percentage points in the whole population, after correction of serum zinc values for the effect of serum CRP and was similar to that in the group with serum CRP <2 mg/L (healthy subgroup) (Table 5).
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Discussion |
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TOPABSTRACTIntroductionSubjects and MethodsResultsDiscussionLITERATURE CITED |
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Relation between acute phase proteins and serum zinc.
There are no standardized cut-off values for serum CRP and ACT for assessing elevated APR, although serum CRP of 5 (24), 8 (12), or 10 (13) mg/L and serum ACT of 0.4 (23,26) or 0.6 (13) g/L are commonly used. Because the relation between changes in APP and serum zinc is nonlinear, we used several categories of APP to evaluate the effect on serum zinc. In this study, elevated APPs during subclinical infection were associated with depressed serum zinc, when APPs were as low as 2 to <5 mg/L serum CRP and > 0.4 g/L serum ACT (23,26). This indicated that serum zinc is depressed at a much lower level of CRP than previously anticipated. Furthermore, our study also showed that the degree of depression in serum zinc seemed to be related to the category, i.e., the magnitude of serum CRP, indicating the usefulness of more than one cut-off value for CRP. We therefore suggest studies to estimate the effect of APPs using multiple categories. However, standardized cut-off values for APPs from different analytical methods are required to compare the estimated effects of APPs from different studies and populations. Using multiple categories and a high reference category for serum CRP of <8 mg/L, Strand et al. (14) found that serum CRP levels of 8–15 and >15 mg/L were associated with 0.70 and 0.94 µmol/L lower plasma zinc, respectively, in Nepalese children (6–35 mo) with acute diarrhea.
In the multiple regression analysis in this study, serum CRP was more closely associated with serum zinc than was serum ACT, suggesting that CRP is a more suitable marker for the depression of serum zinc in apparently healthy children.
During the APR, several factors can contribute to the decrease in serum zinc (27). The mechanism suggested is a redistribution without a quantity change in total zinc body content, by rapid hepatic uptake and sequestration of zinc through cytokine-stimulated synthesis of hepatic metallothioneins (28). However, diminished total zinc body content caused by reduced dietary intake and absorption and losses via feces, urine, and sweat may also contribute to the decrease in serum zinc (27,29).
Relation between morbidity, helminths, parental education and anthropometric indicators, and serum zinc. In the present study, multiple linear regression analysis was used to test the associations while controlling for the effect of the APR. However, this does not necessarily elucidate causal relations. None of the reported illnesses or A. lumbricoides were associated with serum zinc. In contrast, serum zinc was estimated to be 0.12 µmol/L lower/unit increase in log10(epg+1) T. trichiura, even though the children had received the second dose of anthelminthic treatment 3–5 wk before blood collection. Human studies looking at this association are scarce. In a cross-sectional study in Jamaican children, plasma zinc concentrations were significantly negatively correlated with the number of T. trichiura worms (30). If causal, the direction of cause and the effect of the relation between zinc deficiency and T. trichiura are unknown. However, zinc deficiency is associated with increased susceptibility toward gastrointestinal nematodes likely through a weakening of the gut epithelial barrier, allowing greater penetration and establishment of the larval stages as well as a profound impairment of the gut immune response (31). Several controlled experimental animal models showed that dietary zinc deficiency improved the survival of intestinal nematode parasites and the effect depended on the severity of zinc deficiency and nature of infection (31). On the other hand, T. trichiura infection may contribute to reduced serum zinc caused by reduced zinc intake due to anorexia and/or vomiting, increased requirement, and loss due to diarrhea (29,32).
Maternal but not paternal education was associated with higher serum zinc. This indicated that girls' school attendance is important to improve low serum zinc levels in their children. Because about two thirds of the mothers had no education, it may be worthwhile to investigate whether health and nutrition education to mothers who never attended school can also improve low serum zinc in their children.
Stunting but not underweight or wasting was associated with lower serum zinc. This indicated that improving low serum zinc levels may improve linear growth. A meta-analysis, examining the overall magnitude of growth responses to zinc supplementation, indicated that children with stunting are likely to be zinc deficient (2). It is suggested that the prevalence of stunting in preschool children can be used as an indirect indicator of a population's risk of zinc deficiency, with a prevalence of >20% indicating a high risk (1,2). Thus, the prevalence of stunting (45.1%) in this population indicated a high risk of zinc deficiency, which was substantiated by the prevalence of low serum zinc.
Potential limitations of the study. The usefulness of serum zinc concentration to assess zinc status has several limitations. Serum zinc is homeostatically controlled (33). In addition to the APR, various factors, including hypoalbuminemia may affect or confound the interpretation of serum zinc concentrations (1,11). Moreover, the APR itself can be impaired in severely undernourished children (34). Undernutrition (based on anthropometric indices) could have been a problem in our population.
Anthelminthic treatment was given to rule out helminthic infections as a possible confounder in a subsequent vitamin A efficacy trial. A. lumbricoides and T. trichiura infections have previously been shown to be prevalent in this slum, with >80% of children being infected (35,36). Studies on the effect of anthelminthic treatment on serum zinc are not available to our knowledge.
In conclusion, the present study showed a high prevalence of low serum zinc in this group of apparently healthy children in a Dhaka slum. After correcting for the effect of CRP in the whole population, the prevalence of low serum zinc remained high, even though reduced, and it was similar to that in the healthy subgroup with CRP <2 mg/L. Our results suggest that interventions to address low serum zinc in Bangladesh are warranted. Elevated serum CRP and ACT levels, T. trichiura, and stunting were negative predictors of serum zinc, whereas maternal education was a positive predictor. Thus, controlling T. trichiura infection and improving school attendance of girls may be important interventions to improve low serum zinc levels in children. Stunting was associated with lower serum zinc. Our results indicate that elevated APPs during subclinical infection depress serum zinc and as a result hamper the interpretation of serum zinc. Thus, when using serum zinc, APPs must be taken into consideration. The use of multiple categories of APPs and cut-off values that indicate elevated levels warrant further research.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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5 Abbreviations used: ACT, 1-antichymotrypsin; APP, acute phase protein; APR, acute phase response; CRP, C-reactive protein; DANIDA, Danish International Development Assistance; epg, eggs per gram feces; HAZ, height-for-age Z-score; ICDDR,B, International Centre for Diarrhoeal Disease Research, Bangladesh; MUAC, mid upper arm circumference; NCHS, National Center for Health Statistics; serum zinc, serum zinc concentration; SES, socioeconomic status; WAZ, weight-for-age Z-score; WHZ, weight-for-height Z-score; X1B, Bitot's spots.
Manuscript received 5 January 2006. Initial review completed 16 February 2006. Revision accepted 24 May 2006.
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LITERATURE CITED |
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1. International Zinc Nutrition Consultative Group (IZiNCG). Assessment of the risk of zinc deficiency in populations and options for its control. Hotz C, Brown KH, editors. Food Nutr Bull. 2004;25:S91–202.
2. Brown KH, Peerson JM, Rivera J, Allen LH. Effect of supplemental zinc on the growth and serum zinc concentrations of prepubertal children: a meta-analysis of randomized controlled trials. Am J Clin Nutr. 2002;75:1062–71.
3. Shankar AH, Prasad AS. Zinc and immune function: the biological basis of altered resistance to infection. Am J Clin Nutr. 1998;68:447S–63.[Abstract]
4. Fischer Walker C, Black RE. Zinc and the risk for infectious disease. Annu Rev Nutr. 2004;24:255–75.[Medline]
5. Bhutta ZA, Black RE, Brown KH, Gardner JM, Gore S, Hidayat A, Khatun F, Martorell R, Ninh N, et al. Prevention of diarrhea and pneumonia by zinc supplementation in children in developing countries: pooled analysis of randomized controlled trials. J Pediatr. 1999;135:689–97.[Medline]
6. Brooks WA, Yunus M, Santosham M, Wahed MA, Nahar K, Yeasmin S, Black RE. Zinc for severe pneumonia in very young children: double-blind placebo-controlled trial. Lancet. 2004;363:1683–8.[Medline]
7. Sazawal S, Black RE, Menon VP, Dinghra P, Caulfield LE, Dhingra U, Bagati A. Zinc supplementation in infants born small for gestational age reduces mortality: a prospective, randomized, controlled trial. Pediatrics. 2001;108:1280–6.
8. Black MM. Zinc deficiency and child development. Am J Clin Nutr. 1998;68:464–9.
9. Gibson RS. Zinc nutrition in developing countries. Nutr Res Rev. 1994;7:151–73.
10. Beisel WR. Zinc metabolism in infection. In: Brewer GJ, Prasad AS, editors. Zinc metabolism: current aspects in health and disease. New York: Alan R Liss; 1977. p. 155–76.
11. Brown KH. Effect of infections on plasma zinc concentration and implications for zinc status assessment in low-income countries. Am J Clin Nutr. 1998;68:425–9.
12. Lartey A, Manu A, Brown KH, Dewey KG. Predictors of micronutrient status among six- to twelve-month-old breast-fed Ghanaian infants. J Nutr. 2000;130:199–207.
13. Wieringa FT, Dijkhuizen MA, West CE, Northrop-Clewes CA, Muhilal. Estimation of the effect of the acute phase response on indicators of micronutrient status in Indonesian infants. J Nutr. 2002;132:3061–6.
14. Strand TA, Adhikari RK, Chandyo RK, Sharma PR, Sommerfelt H. Predictors of plasma zinc concentrations in children with acute diarrhea. Am J Clin Nutr. 2004;79:451–6.
15. Duggan C, MacLeod WB, Krebs NF, Westcott JL, Fawzi WW, Premji ZG, Mwanakasale V, Simon JL, Yeboah-Antwi K, et al. Plasma zinc concentrations are depressed during the acute phase response in children with falciparum malaria. J Nutr. 2005;135:802–7.
16. Tomkins A. Assessing micronutrient status in the presence of inflammation. J Nutr. 2003;133:1649S–55.
17. Haque R, Mondal D, Kirkpatrick BD, Akther S, Farr BM, Sack RB, Petri WA Jr. Epidemiologic and clinical characteristics of acute diarrhea with emphasis on Entamoeba histolytica infections in preschool children in an urban slum of Dhaka, Bangladesh. Am J Trop Med Hyg. 2003;69:398–405.
18. Whitaker B, Guest I, Anonymous, Ennals D. The Biharis in Bangladesh. 4th edition. London: Minority Rights Group Ltd.; 1982. Report No.: 11.
19. WHO. Measuring change in nutritional status. Geneva: WHO; 1983.
20. Sullivan KM, Gorstein J. ANTHRO Software for calculating anthropometry [computer program]. Version 1.02–Y2K compliant. Atlanta: CDC and Geneva: WHO; 1999.
21. Hall A. Quantitative variability of nematode egg counts in faeces: a study among rural Kenyans. Trans R Soc Trop Med Hyg. 1981;75:682–7.[Medline]
22. AOAC. Zinc in serum. In: Official methods of analysis of the AOAC. 15th edition. Arlington, VA: AOAC; 1991;Suppl 2:81.
23. Friis H, Gomo E, Kæstel P, Ndhlovu P, Nyazema N, Krarup H, Michaelsen KF. HIV and other predictors of serum ß-carotene and retinol in pregnancy: a cross-sectional study in Zimbabwe. Am J Clin Nutr. 2001;73:1058–65.
24. Maqsood M, Dancheck B, Gamble MV, Palafox NA, Ricks MO, Briand K, Semba RD. Vitamin A deficiency and inflammatory markers among preschool children in the Republic of the Marshall Islands. Nutr J. 2004;3:21–6.[Medline]
25. Bloem MW, Moench-Pfanner R, Panagides D, editors. Health and nutritional surveillance for development. Singapore: Helen Keller Worldwide; 2003.
26. Friis H, Gomo E, Kæstel P, Ndhlovu P, Nyazema N, Krarup H, Michaelsen KF. HIV and other predictors of serum folate, serum ferritin, and hemoglobin in pregnancy: a cross-sectional study in Zimbabwe. Am J Clin Nutr. 2001;73:1066–73.
27. Beisel WR. Metabolic response of the host to infections. In: Feigin RD, Cherry JD, editors. Textbook of pediatric infectious diseases. Vol 1. 4th edition. Philadelphia: WB Saunders Co; 1998. p. 54–69.
28. Sobocinski PZ, Canterbury WJ Jr, Mapes CA, Dinterman RE. Involvement of hepatic metallothioneins in hypozincemia associated with bacterial infection. Am J Physiol. 1978;234:E399–406.[Medline]
29. Castillo-Duran C, Vial P, Uauy R. Trace mineral balance during acute diarrhea in infants. J Pediatr. 1988;113:452–7.[Medline]
30. Bundy DAP, Golden MHN. The impact of host nutrition on gastrointestinal helminth populations. Parasitology. 1987;95:623–35.
31. Scott ME, Koski KG. Zinc deficiency impairs immune responses against parasitic nematode infections at intestinal and systemic sites. J Nutr. 2000;130:1412S–20.
32. Stephenson LS, Holland CV, Cooper ES. The public health significance of Trichuris trichiura. Parasitology. 2000;121:S73–95.
33. King JC. Assessment of zinc status. J Nutr. 1990;120:1474–9.
34. Doherty JF, Golden MHN, Raynes JG, Griffin GE, McAdam KPWJ. Acute-phase protein response is impaired in severely malnourished children. Clin Sci. 1993;84:169–75.[Medline]
35. Hall A, Anwar KS, Tomkins AM. Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control. Lancet. 1992;339:1253–7.[Medline]
36. Hall A, Nahar Q. Albendazole and infections with Ascaris lumbricoides and Trichuris trichiura in children in Bangladesh. Trans R Soc Trop Med Hyg. 1994;88:110–2.[Medline]
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