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© 2007 American Society for Nutrition J. Nutr. 137:2140-2146, September 2007

Community and International Nutrition

Intake of Alcoholic Beverages Is a Predictor of Iron Status and Hemoglobin in Adult Tanzanians1,2

Wabyahe Malenganisho3, Pascal Magnussen4, Birgitte Jyding Vennervald4, Henrik Krarup5, Pernille Kæstel6, Julius Siza3, Godfrey Kaatano3, Mansuet Temu3 and Henrik Friis6,*

3 National Institute for Medical Research, Mwanza Medical Research Centre, Mwanza, Tanzania; 4 DBL Institute for Health Research and Development, 2920 Charlottenlund, Denmark; 5 Department of Clinical Biochemistry, Aalborg University Hospital, 9100 Aalborg, Denmark; and 6 Department of Human Nutrition, Faculty of Life Sciences, University of Copenhagen, 1958 Frederiksberg, Denmark

* To whom correspondence should be addressed. E-mail: hfr{at}life.ku.dk.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 
Iron deficiency is widespread in sub-Saharan Africa, but its predictors are not fully understood. We conducted a cross-sectional study among adults around Lake Victoria to describe iron status and asses the role of dietary and infectious predictors. Linear regression analyses were used to assess the role of infections and intake of meat, fish, fruit/vegetables, alcoholic beverages, and soil on hemoglobin and serum ferritin, while controlling for elevated serum {alpha}1-antichymotrypsin (ACT). Among 1498 participants, the mean age was 33.3 (14–87) y with 53.9% females. More than one-half ate fish daily, 6% ate fruit/vegetables daily, and only 11% ate meat weekly. One-third consumed alcoholic beverages and one-fifth of females consumed soil. Hookworm (80.3%), Schistosoma mansoni (64.7%), and HIV (7.3%) infection were common. Anemia was found in 48.2% of females (<120 g/L hemoglobin) and 40.1% of males (<130 g/L hemoglobin), and 22.3% of females and 7.0% of males had depleted iron stores (serum ferritin <12 µg/L). In multivariate analyses, alcoholic beverage consumption and HIV were positive, whereas soil eating and hookworm infection were negative predictors of serum ferritin. Alcoholic beverage consumption was a positive predictor of hemoglobin, and soil eating, HIV, and hookworm infection were negative predictors. Intakes of meat, fish, and fruit or vegetables were not predictors. Elevated serum ACT was a predictor of both hemoglobin and serum ferritin. Anemia and depleted iron stores were common, whereas iron overload was rare. In conclusion, the associations between alcoholic beverage intake and hemoglobin and iron status suggest that alcoholic beverages may contain micronutrients essential to erythropoiesis. The role of alcoholic beverage intake and other determinants of hemoglobin and iron status in low-income populations needs to be better elucidated.


   Introduction
TOP
 ABSTRACT
 Introduction
Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 
Iron deficiency is widespread in low-income countries, contributing to morbidity and mortality and impaired mental development and working capacity, thus impairing socioeconomic development (1,2).

Low content and bioavailability of iron in the typical cereal-based diet is a major cause of iron deficiency (3,4). This is due to the high content of antinutrients in maize and other staple foods and inadequate intake of animal foods in the diet. Animal foods, including seafood, provide the more easily absorbed heme-iron as well as a meat-factor facilitating the absorption of iron. A number of other food groups/factors may further enhance or inhibit iron absorption. For example, fruits and vegetables contain vitamin C, which enhances absorption (3,5). Similarly, even moderate alcoholic beverage consumption may promote iron status (6,7), probably through increased gastric acid secretion, iron solubilization, and absorption (8,9). Soil, which is commonly eaten among children and women (10,11), may contain iron (12), but at the same time impairs absorption of dietary iron (13,14).

Infections causing loss of blood (e.g. hookworm and Schistosome spp.) may further exacerbate a poor iron status and cause iron deficiency anemia (15). In contrast, malaria causes anemia through hemolysis and suppression of the hemopoiesis, with dislocation of iron to the stores. If infections eliciting an acute phase response or otherwise causing sequestration of iron are widespread in a population, then iron status will be overestimated if based on serum concentrations of ferritin (serum ferritin) (16).

Studies on iron status often assess only a few potential predictors. For example, studies on dietary predictors often ignore alcoholic beverage and soil consumption as well as infectious diseases. Studies on infectious predictors often fail to adjust for accompanying or background acute phase responses that affect the markers of status and as such may confound the associations.

We conducted a cross-sectional study in a population living on the shores of Lake Victoria with an aim to describe iron status and assess a range of potential dietary and infectious predictors, while adjusting for the acute phase response.


   Subjects and Methods
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
Results
 Discussion
 LITERATURE CITED
 
The study was conducted among adult males and females in 2 villages, Msozi and Sangabuye, in Ukerewe and Ilemela districts of Mwanza region, Tanzania, in February–May, 2001, at the end of the rainy seasons. The common diet was maize or cassava, sweet potatoes, rice and millet eaten with fish, and occasionally meat. Fruits or vegetables were consumed when seasonally available. Most of the study participants were engaged in peasant farming and commercial fishing activities and kept cattle, goats, and chickens for domestic consumption and sale. According to the national census of 2002, the adult population was 3225 in Msozi and 3184 in Sangabuye. Information about the study was provided at public meetings and nonpregnant adults were invited to participate. The first 1000 registering from Msozi were included. From Sangabuye, only those from one-half of the sub-villages were invited and the first 500 from these were included.

After obtaining informed consent, we used a questionnaire to obtain data on sociodemography. In addition, data on the frequency of intake of beef, goat, and chicken, tilapia (a large fish of which the filet is eaten), dagaa (sardine-like fish eaten whole in a dried form), and fruits and vegetables within the last 3 mo was obtained. Categories were: never, <1 d/wk, 1–6 d/wk, or daily. Information was also obtained on the intake of alcoholic beverages and soil, categorized as: never, <1 d/wk, or 1–7 d/wk. Information on the type of alcoholic beverage and type of soil was also obtained.

    Biochemical measurements. Blood samples were taken from the cubital vein between 0800 and 1300. A drop of blood was used to determine hemoglobin using a portable battery-operated hemoglobinometer (Hemocue). Anemia was defined as <120 g/L hemoglobin for women and <130 g/L for men (2). From the remaining blood, serum was separated and placed in ice-cooled insulated boxes and later transported to the laboratory and kept at –70°C until further analyses. Serum ferritin and {alpha}1-antichymotrypsin (ACT)7 were determined at the Department of Human Nutrition, Denmark. Serum ferritin was measured by a fluoroimmunoassay kit (DELFIA Ferritin, Wallac) and values <12 and 12–24 µg/L defined depleted and low iron stores. Serum ACT was measured by automated turbidimetry (Cobas Mira Plus, Roche). Rabbit antihuman ACT (DAKO) was used to precipitate ACT and turbidity was measured at 345 nm after incubation for 8.3 min at 37°C. The results are given as grams per liter serum on the basis of a standard curve from commercial calibrators (DAKO).

    Examination for infections. A single stool sample was processed to make duplicate 50-mg Kato thick smears covered with cellophane soaked in glycerin and malachite green (17). The Kato smears were examined for hookworm and other helminths eggs within 1 h after preparation. Examination for Schistosoma mansoni was conducted at least 24 h later to allow for clearing. The mean egg counts of the 2 slides were computed and then multiplied by 20 to obtain the number of eggs per gram feces (epg). Urine specimens were collected and examined for S. hematobium using the filtration technique with Nuclepore membranes (18).

Thick and thin blood smears were prepared for malaria examination and stained with Giemsa. The films were considered negative if no parasites were found in 100 high-power fields on the thick film (19). The number of parasites was counted against 200 white blood cells and expressed as parasites per microliter, assuming 8000 white blood cells/µL.

We conducted HIV testing using 2 enzyme immunological assays. Samples found negative using UNIFORM I Vironistika HIV-MIXT (Organon) were considered negative, whereas samples found positive or indeterminate were tested with a confirmatory enzyme immunological assay, UNIFORM II, Enzygnost anti-HIV1/HIV2 (Behring). Hepatitis B virus (HBV) surface antigen and hepatitis C virus (HCV) antibodies were determined using Abbott Axsym System (Abbott Diagnostics A/S).

    Statistical analysis. Data on serum ferritin was log10(x)-transformed and data on malaria parasitaemia and helminths egg output were log10(x+1)-transformed to achieve normal distributions. Two sample t tests and one-way ANOVA were used to test for differences in means and the chi-square test was to test for differences in proportions between groups. Multiple linear regression analysis was done to identify predictors of hemoglobin and serum ferritin, using backward elimination strategy based on P > 0.10. Variables assessed were site, sex, infections, and intake of alcoholic beverages, soil, meat, fish, and fruit/vegetables. Type of alcoholic beverage was not included, because most were taking several types. Based on the food frequency data, we computed variables for intake of meat (coded 1 for ≥1 d/wk and 0 for less), fish (coded 1 for daily and 0 for less than daily), and fruit/vegetables (coded 1 for daily and 0 for less than daily). Adjustment for age used dummy variables based on 5-y-age intervals, with 20–30 y as reference. Dummy variables were used for categorical variables and for variables where the relationship was not linear. Two-way interactions between predictors in the final models were assessed for. The final models were presented with and without adjustment for elevated serum ACT and the hemoglobin model was also presented with adjustment for depleted and low-iron stores. Normal and residual-vs.-fitted plots were examined to assess normality and homoscedasticity of residuals. P-values < 0.05 were considered significant. Stata version 9.0 (StataCorp) was used for all analyses.

    Ethical consideration. The study was approved by the Ethics Committee of the National Institute for Medical Research in Tanzania and recommended by the Danish National Committee on Biomedical Research Ethics. Full information about the study was given to all participants and oral consent was obtained from all study participants before inclusion. Pretest HIV counseling was mandatory; post-test counseling was given to those who wanted to know their HIV results.


   Results
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
Discussion
 LITERATURE CITED
 
Of 1498 individuals included, the age range was 14–87 y (33.3 y mean) with 54% females. Maize was the staple food for 84%, while the remaining participants reported cassava or a combination of staples. Fish, mainly tilapia and to a lesser extent dagaa, were eaten daily by 57%, whereas only 11% reported eating meat once or more per week. Daily intake of vegetables or fruits was reported by only 6%. Regular alcoholic beverage consumption was reported by 33%, 22% of whom drank less than weekly and 11% more than once per week up to daily. Most drank several types of alcoholic beverages, such as traditional liquor or beer made from maize, cassava, millet, or sorghum or occasionally factory-brewed beer. Soil eating was reported by 12%, but more often in females than in males (19 vs. 4%; P < 0.001). Among females, 16% were eating soil less than weekly and 4% once or more per week. The preferred soil consumed was from termite hills, sold in molded form (locally known as udongo wa Pemba). Helminth infections were prevalent, especially with hookworm (80%) and S. mansoni (65%) and less so S. hematobium (4%), whereas A. lumbricoides, T. trichiura, and S. stercoralis were not endemic (<1%). The prevalence of malaria was 9%, and 7% had HIV, 12% had HBV, and 4% had HCV infection. Baseline characteristics by study site are presented in Table 1.


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  		TABLE 1 Baseline characteristics of 1498 study participants from Msozi and Sangabuye villages1

 
    Hemoglobin and serum ferritin. Data on hemoglobin and serum ferritin were available for 1479 (98.7%) and 1467 (97.9%) participants, respectively. The mean hemoglobin concentrations were 119.2 g/L in females and 134.0 g/L in males (P < 0.001). Anemia was found in 48.2% of females and 40.1% of males (P < 0.001). Geometric mean serum ferritin concentrations were 23.1 µg/L among females and 36.0 µg/L among males (P < 0.001). Depleted iron stores were seen in 22.3% of females and 7.0% of males (P < 0.001). Only 43 (2.9%) had serum ferritin above 150 µg/L. The prevalence of anemia and depleted iron stores by site and sex are shown in Table 2. Mean serum ACT was 0.32 g/L, with 23.4% having values above 0.35 g/L and 8.6% having values above 0.4 g/L (20). Hemoglobin declined and geometric mean serum ferritin increased as serum ACT increased (Table 3). Increasing hookworm intensity was accompanied by declining serum ferritin in both males and females (Table 4).


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  		TABLE 2 Hemoglobin and serum ferritin concentrations and proportions with low levels by study site and sex

 

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  		TABLE 3 Hemoglobin and serum ferritin concentrations by serum ACT category by sex for both sites combined

 

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  		TABLE 4 Hemoglobin and serum ferritin concentrations by intensity of hookworm infection category by sex for both sites combined

 
    Predictors of serum ferritin. In multiple linear regression analysis adjusted for age (Table 5, model 1), females had 20% lower serum ferritin than males. Alcoholic beverage intake less than weekly and weekly was associated with 19% and 30% higher serum ferritin, respectively, compared with participants not drinking alcoholic beverages. In contrast, less than weekly and weekly intake of soil was associated with 32% and 49% lower serum ferritin. HIV-infected individuals had 48% higher serum ferritin than uninfected participants, whereas serum ferritin declined with increased hookworm intensity. With all predictors in the model, serum ferritin was 18% lower in Msozi. Serum ACT concentrations between 0.35–0.4, 0.4–0.5, and above 0.5 g/L were associated with 1.2, 1.6, and 2.8 times higher serum ferritin, respectively, compared with serum ACT <0.35 g/L (Table 5, model 2), but its inclusion had little effect on other predictors. Daily intake of fish, weekly intake of meat, and daily intake of vegetables were not predictors and no 2-way interactions between the predictors were identified.


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  		TABLE 5 Predictors of serum ferritin (µg/L, log10-transformed), with regression coefficients (B), 95% CI, and corresponding P-values1

 
    Predictors of hemoglobin. Alcoholic beverage intake was associated with higher hemoglobin, whereas female sex, soil eating, and HIV and hookworm infection were associated with lower hemoglobin (Table 6, model 1). Less than weekly and weekly intake of alcoholic beverages were associated with 3.2 and 5.5 g/L higher hemoglobin, while less than weekly and weekly intake of soil were associated with 2.7 and 13.6 g/L lower hemoglobin. HIV infection was associated with 5.9 g/L lower hemoglobin, whereas only hookworm intensities above 200 epg were associated with lower hemoglobin. Mean hemoglobin declined considerably with increased serum ACT, but inclusion of elevated serum ACT had little effect on other predictors (Table 6, model 2). Low and depleted iron stores were associated with 6.1 and 18.6 g/L lower hemoglobin (Table 6, model 3) and explained one-half of the effect of soil eating and hookworm infection but only little of the effect of female sex and alcoholic beverage intake. No 2-way interactions were found between the predictors.


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  		TABLE 6 Predictors of hemoglobin concentration (g/L) with regression coefficients (B), 95% CI, and P-values1

 

   Discussion
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
 Discussion
LITERATURE CITED
 
Depleted iron stores and anemia were widespread in the 2 communities in and around Lake Victoria. Depleted iron stores were more common among females but did not explain the lower hemoglobin in women. Deficiencies of other micronutrients essential to erythropoiesis or to utilization of iron for erythropoiesis [e.g. B vitamins, vitamin A, and zinc (3,21)] may explain some of the 13-g/L hemoglobin sex difference, although most may reflect the genuine sex difference. Other studies have reported sex differences in iron status or hemoglobin not likely explained by differences in dietary intake, growth, and infections (22–24).

    Dietary intake. Although meat is rich in highly bioavailable heme-iron and, like seafood, contains the so-called meat-factor facilitating absorption of non-heme iron (3,25), frequent intake of neither meat nor fish was associated with iron status. Similarly, frequent intake of fruit/vegetables was not associated with iron status despite vitamin C enhancing non-heme iron absorption (3,25). The lack of association could be due to misclassification of intake, to iron status being dependent on prior intake, to limited contrasts in intake, or to lack of other nutrients important to absorption and utilization of iron. The low intake of fruits and vegetables, with only 6% of participants reporting a daily intake, is in accord with the previously reported low intake of yellow-orange fruits among pregnant Tanzanian women (26) and the very low serum ß-carotene previously observed in Tanzanian adults (27).

Alcoholic beverage consumption was associated with higher serum ferritin, which increased with frequency of intake. We were not able to quantify the intake or distinguish between different types of alcoholic beverages, but most participants were drinking traditional alcoholic beverages brewed from maize, cassava, millet, and sorghum. Factory-brewed beer was consumed only occasionally, due to the high cost. Although the association could be due to alcohol-induced liver damage (28), it could also be due to alcohol enhancing iron absorption (8,9), probably because of increased gastric acid secretion and iron solubilization. It could also be due to the iron content of the beverage, either from the raw material or from the fermentation vessel. Socioeconomic confounding is not likely to explain the association, because it persisted after adjustment for frequent intake of meat. Because alcoholic beverage consumption was also a predictor of hemoglobin, which was only partly explained by size of iron stores, it could also be that the alcoholic beverages contain B vitamins or other nutrients otherwise lacking in the diet and of importance to erythropoiesis (3,21). Studies from Tanzania and other Sub-Saharan countries (29–31) have reported iron overload due to a high intake of traditional beer fermented in iron containers. A study in rural Zimbabwe found serum ferritin above 250 µg/L in almost one-half of the males (29).

Geophagy was common among females and was a strong negative predictor of both hemoglobin and serum ferritin, as previously reported among children (32) and pregnant women (10). When adjusting for low serum ferritin, the association between soil eating and hemoglobin declined, suggesting that the association is partly explained by underlying iron depletion. It is not clear if soil eating leads to smaller iron stores due to chelation of dietary iron in the intestinal tract, or if soil eating is the result of a craving for soil caused by iron deficiency (33,34). The latter may seem likely, because termite soil contains more minerals and has a fine texture (35), but a recent trial found no effect of iron supplementation on soil intake (14). Nonetheless, because soil eating seems to be a strong risk factor of both ascaris and trichuris infection (36,37), soil eating should not be recommended.

    Infections and the acute phase response. Hepcidin is the principal iron-regulatory hormone. It inhibits intestinal iron absorption, iron recycling from senescent erythrocytes engulfed by macrophages, and iron release from hepatic stores (38). Iron deficiency, anemia, and hypoxemia suppress hepcidin production, thereby increasing dietary iron absorption and release of iron to plasma. In contrast, inflammation induces hepcidin production, mediated by the inflammatory cytokine IL-6. This results in sequestration of iron in the stores and iron-limited erythropoiesis and eventually anemia of inflammation (38). We used serum ACT, an acute phase protein also produced in hepatocytes in response to infections and mediated by IL-6 (39). By adjusting for elevated serum ACT, we attempted to explain the variation in serum ferritin and hemoglobin due to infection through IL-6-mediated hepcidin-production. Consistent with other studies (16), serum ACT between 0.4–0.5 and >0.5 g/L was associated with ~1.5 and 3 times higher serum ferritin and 6 and 15 g/L lower hemoglobin, respectively.

HIV infection was associated with lower hemoglobin, although only significantly so in males, and with higher serum ferritin. Since HIV infection was associated with only a slightly increased serum ACT, adjustment for elevated serum ACT had only negligible effect on the relationship between HIV infection and serum ferritin, and hemoglobin. So, if the effects of infection occur through increased production of hepcidin, then our data seem to suggest that it is not necessarily IL-6 mediated but either directly through hepcidin or through other mechanisms.

As expected, hookworm infection was a negative predictor of hemoglobin but, in contrast to HIV, was associated with lower serum ferritin. Hookworm infection leads to chronic blood loss and if the iron intake is inadequate, this will eventually lead to depletion of iron stores and iron deficiency anemia. We found that even intensities <100 epg were associated with lower serum ferritin, but only intensities >200 epg were associated with reduced hemoglobin. Other studies have found even lower intensities of hookworm infection to be associated with hemoglobin (40). Obviously, the relationship between hookworm intensity and hemoglobin depends on the background iron status, so that even high intensities may not cause anemia in population with high iron stores, whereas mild intensities may cause anemia in populations with marginal iron stores. Controlling for depleted and low iron stores in the model explained only some of the effect of hookworm on hemoglobin, possibly due to inaccuracy of serum ferritin as a measure of iron stores. The helminth data were based on only 1 stool sample, known to have a low sensitivity and specificity given the high day-to-day variation in egg output (41). Thus, light infections in those found egg-negative cannot be excluded, which may also explain why S. mansoni was not a predictor of serum ferritin and hemoglobin. The lack of effect of malaria may be due to partial immunity and hence low risk of malaria morbidity despite the intense transmission at the end of the rainy season when the study was conducted.

The associations between alcoholic beverage intake and hemoglobin and iron status suggest that alcoholic beverages may contain not only iron but also other micronutrients essential to erythropoiesis. The role of alcoholic beverages and other determinants of hemoglobin and iron status in low-income populations needs to be better elucidated.


   FOOTNOTES
 
1 Supported by the Danish International Development Assistance through the DBL Institute of Health Research and Development, Denmark. Back

2 Author disclosures: W. Malenganisho, P. Magnussen, B. Jyding Vennervald, H. Krarup, P. Kæstel, J. Siza, G. Kaatano, M. Temu, and H. Friis, no conflicts of interest. Back

7 Abbreviations used: ACT, {alpha}1-antichymotrypsin; epg, eggs per gram feces; HBV, hepatitis B virus, HCV, hepatitis C virus. Back

Manuscript received 26 December 2006. Initial review completed 14 February 2007. Revision accepted 19 June 2007.


   LITERATURE CITED
TOP
 ABSTRACT
 Introduction
 Subjects and Methods
 Results
 Discussion
 LITERATURE CITED
 

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