Claudia E. Lazarte^1,2*, Andrea Soto^2,3, Leovegildo Alvarez⁴, Björn Bergenståhl¹, Nora Medrano³, Yvonne Granfeldt¹

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¹ Department of Food Technology, Engineering and Nutrition, Lund University, Lund, Sweden.
² Food and Natural Products Center, San Simón University, Cochabamba, Bolivia.
³ Chagas Disease and Immunoparasitology Laboratory, San Simón University, Cochabamba, Bolivia.
⁴ Albina Patino Pediatrics Hospital, Cochabamba, Bolivia.
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Abstract: Malnutrition and parasitic diseases are within the major issues in rural areas in developing countries. In this study, the nutritional status, dietary intake including mineral absorption inhibitor (phytate), hematological indicators and trace element status (zinc, iron) were evaluated and associated to the presence of intestinal parasites in a group of children from a rural area of Bolivia. The results showed that 96% of the children had intestinal parasites; 7 types of parasites (Ascaris lumbricoides, Giardia lamblia, Ancylostoma duodenale, Entamoeba histolytica, Entamoeba coli, Trichuris trichiura, Strongyloides stercolaris) were identified. Anthropometric measurements indicated that 37% of the children were stunted and 17% were underweight. Iron and zinc intake showed that 34% and 30% of children had inadequate intake of these nutrients respectively. Phytate: zinc molar ratios were between 6.5 and 21, and from 6.2 to 15 for phytate: iron, indicating that the absorption of zinc and iron might be compromised by the level of phytate in the diet. The serum zinc was below the lower cut-off in 87% of the children, indicating zinc deficiency. Moreover, a multiple regression model showed the significant effect of the presence of the parasite Giardia lamblia and phytate intake on the serum zinc levels. Regarding the iron status, 30% of the children presented with anemia and about 66% had iron deficiency; a simple linear regression model showed the significant negative effect of the presence of the parasite Ancylostoma duodenale on iron status. In conclusion, the levels of zinc and iron, which were low in this child population, were greatly affected by the presence of intestinal parasites; in addition, the consumption of plant-based diets with high levels of phytate also impaired the zinc absorption.

Keywords: Nutritional Status, Dietary Intake, Zinc, Iron, Deficiency, Phytate, Intestinal Parasites

Cite this paper: Lazarte, C. , Soto, A. , Alvarez, L. , Bergenståhl, B. , Medrano, N. and Granfeldt, Y. (2015) Nutritional Status of Children with Intestinal Parasites from a Tropical Area of Bolivia, Emphasis on Zinc and Iron Status. Food and Nutrition Sciences, 6, 399-411. doi: 10.4236/fns.2015.64041.

References

[1]   Amare, B., Moges, B., Fantahun, B., Tafess, K., Woldeyohannes, D., et al. (2012) Micronutrient Levels and Nutritional Status of School Children Living in Northwest Ethiopia. Nutrition Journal, 11, 108.
http://dx.doi.org/10.1186/1475-2891-11-108

[2]   Coop, R.L. and Holmes, P.H. (1996) Nutrition and Parasite Interaction. International Journal for Parasitology, 26, 951-962.
http://dx.doi.org/10.1016/S0020-7519(96)80070-1

[3]   Walravens, P.A., Krebs, N.F. and Hambidge, K.M. (1983) Linear Growth of Low Income Preschool Children Receiving a Zinc Supplement. The American Journal of Clinical Nutrition, 38, 195-201.

[4]   Black, R.E. (2003) Zinc Deficiency, Infectious Disease and Mortality in the Developing World. Journal of Nutrition, 133, 1485S-1489S.

[5]   Gibson, R. (2005) Principles of Nutritional Assessment. Oxford University Press, New York.

[6]   Hotz, C., Lowe, N.M., Araya, M. and Brown, K.H. (2003) Assessment of the Trace Element Status of Individuals and Populations: The Example of Zinc and Copper. The Journal of Nutrition, 133, 1563S-1568S.

[7]   Prasad, A.S. (2009) Impact of the Discovery of Human Zinc Deficiency on Health. Journal of the American College of Nutrition, 28, 257-265.
http://dx.doi.org/10.1080/07315724.2009.10719780

[8]   Shetty, P. (2010) Zinc Deficiency and Infections. In: Nutrition, Immunity and Infection. Cabi Publishing, Wallingford, Oxon, 101-113.

[9]   Caulfield, L.E. and Black, R.E. (2004) Zinc Deficiency. In Comparative Quantification of Health Risks. WHO, World Health Organization. Geneva.

[10]   Cook, J.D., Baynes, R.D. and Skikne, B.S. (1992) Iron Deficiency and the Measurement of Iron Status. Nutrition Research Reviews, 5, 198-202.
http://dx.doi.org/10.1079/NRR19920014

[11]   UNICEF/UNU/WHO (2001) Iron Deficiency Anaemia: Assessment, Prevention, and Control.
http://www.who.int/nutrition/publications/en/ida_assessment_prevention_control.pdf

[12]   Lonnerdal, B. (2002) Phytic Acid-Trace Element (Zn, Cu, Mn) Interactions. International Journal of Food Science and Technology, 37, 749-758.
http://dx.doi.org/10.1046/j.1365-2621.2002.00640.x

[13]   WHO (2010) Parasitic Diseases. World Health Organization.
http://www.who.int/zoonoses/institutions/Parasitic/en/

[14]   Solomons, N.W. and Keusch, G.T. (1981) Nutritional Implications of Parasitic Infections. Nutrition Reviews, 39, 149161.
http://dx.doi.org/10.1111/j.1753-4887.1981.tb06762.x

[15]   WHO (1995) Physical Status: The Use and Interpretation of Anthropometry. Technical Report Series No. 8541995, World Health Organization, Geneva.
http://www.who.int/childgrowth/publications/physical_status/en/

[16]   WHO (2007) Growth Reference Data for 5 19 Years. World Health Organization.
http://www.who.int/growthref/en/

[17]   Lazarte, C., Encinas, M.E., Alegre, C. and Granfeldt, Y. (2012) Validation of Digital Photographs, as a Tool in 24-h Recall, for the Improvement of Dietary Assessment among Rural Populations in Developing Countries. Nutrition Journal, 11, 61.
http://dx.doi.org/10.1186/1475-2891-11-61

[18]   Lazarte, C.E., Carlsson, N.-G., Almgren, A., Sandberg, A.-S. and Granfeldt, Y. (2015) Phytate, Zinc, Iron and Calcium Content of Common Bolivian Food, and Implications for Mineral Bioavailability. Journal of Food Composition and Analysis, 39, 111-119.
http://dx.doi.org/10.1016/j.jfca.2014.11.015

[19]   FAO/WHO/UNU, Food and Agricultural Organization, World Health Organization, United Nations University (1985) Energy and Protein Requirements. WHO Technical Report Series 724, World Health Organization, Geneva.

[20]   Gibson RS (2005) Principles of Nutritional Assessment. Oxford University Press, New York.

[21]   WHO and FAO (2003) Dietary Recommendations in the Report of a Joint WHO/FAO Expert Consultation on Diet, Nutrition and the Prevention of Chronic Diseases. WHO Technical Report Series 916, World Health Organization, Geneva.

[22]   WHO (1996) Trace Elements in Human and Health Nutrition. World Health Organization, Geneva.
http://whqlibdoc.who.int/publications/1996/9241561734_eng.pdf?ua=1

[23]   Hurrell, R.F. (2004) Phytic Acid Degradation as a Means of Improving Iron Absorption. International Journal for Vitamin and Nutrition Research, 74, 445-452.
http://dx.doi.org/10.1024/0300-9831.74.6.445

[24]   Stenzel, D.J. and Boreham, P.F. (1996) Blastocystis hominis Revisited. Clinical Microbiology Reviews, 9, 563-584.

[25]   Hotz, C. and Brown, K.H. (2004) International Zinc Nutrition Consultative Group (IZiNCG) Technical Document No. 1. Assessment of the Risk of Zinc Deficiency in Populations and Options for Its Control. Food and Nutrition Bulletin, 25, S94-S203.

[26]   Taylor, A. (1997) Measurement of Zinc in Clinical Samples. Annals of Clinical Biochemistry, 34, 142-150.
http://dx.doi.org/10.1177/000456329703400202

[27]   Gibson, R.S. and Hotz, C. (2001) Dietary Diversification/Modification Strategies to Enhance Micronutrient Content and Bioavailability of Diets in Developing Countries. British Journal of Nutrition, 85, S159-S166.
http://dx.doi.org/10.1079/BJN2001309

[28]   Abebe, Y., Bogale, A., Hambidge, K.M., Stoecker, B.J., Bailey, K. and Gibson, R.S. (2007) Phytate, Zinc, Iron and Calcium Content of Selected Raw and Prepared Foods Consumed in Rural Sidama, Southern Ethiopia, and Implications for Bioavailability. Journal of Food Composition and Analysis, 20, 161-168.
http://dx.doi.org/10.1016/j.jfca.2006.09.003

[29]   Lazarte, C., Alegre, C., Rojas, E. and Granfeldt, Y. (2013) Nutritional Status of Patients with Cutaneous Leishmaniasis from a Tropical Area from Bolivia, and Implications for Zinc Bioavailability. Food and Nutrition Sciences, 4, 49-60.
http://dx.doi.org/10.4236/fns.2013.410A009

[30]   Mazariegos, M., Hambidge, K.M., Westcott, J.E., Solomons, N.W., Raboy, V., Das, A., et al. (2010) Neither a Zinc Supplement nor Phytate-Reduced Maize nor Their Combination Enhance Growth of 6to 12-Month-Old Guatemalan Infants. The Journal of Nutrition, 140, 1041-1048.
http://dx.doi.org/10.3945/jn.109.115154

[31]   Chan, S.S.L., Ferguson, E.L., Bailey, K., Fahmida, U., Harper, T.B. and Gibson, R.S. (2007) The Concentrations of Iron, Calcium, Zinc and Phytate in Cereals and Legumes Habitually Consumed by Infants Living in East Lombok, Indonesia. Journal of Food Composition and Analysis, 20, 609-617.
http://dx.doi.org/10.1016/j.jfca.2007.03.003

[32]   Gibson, R.S., Bailey, K.B., Gibbs, M. and Ferguson, E.L. (2010) A Review of Phytate, Iron, Zinc, and Calcium Concentrations in Plant-Based Complementary Foods Used in Low-Income Countries and Implications for Bioavailability. Food & Nutrition Bulletin, 31, 134-146.

[33]   Roohani, N., Hurrell, R., Wegmueller, R. and Schulin, R. (2012) Zinc and Phytic Acid in Major Foods Consumed by a Rural and a Suburban Population in Central Iran. Journal of Food Composition and Analysis, 28, 8-15.
http://dx.doi.org/10.1016/j.jfca.2012.07.005

[34]   Gibson, R.S., Heath, A.L.M., Limbaga, M.L.S., Prosser, N. and Skeaff, C. (2001) Are Changes in Food Consumption Patterns Associated with Lower Biochemical Zinc Status among Women from Dunedin, New Zealand? British Journal of Nutrition, 86, 71-80.
http://dx.doi.org/10.1079/BJN2001370

[35]   Donovan, U.M. and Gibson, R.S. (1995) Iron and Zinc Status of Young-Women Aged 14 to 19 Years Consuming Vegetarian and Omnivorous Diets. Journal of the American College of Nutrition, 14, 463-472.
http://dx.doi.org/10.1080/07315724.1995.10718537

[36]   Manary, M.J., Hotz, C., Krebs, N.F., Gibson, R.S., Westcott, J.E., Broadhead, R.L. and Hambidge, K.M. (2002) Zinc Homeostasis in Malawian Children Consuming a High-Phytate, Maize-Based Diet. The American Journal of Clinical Nutrition, 75, 1057-1061.

[37]   Mollinedo, S. and Prieto, C. (2006) Enteroparasitología en Bolivia. Ministerio de Salud y Deportes, La Paz. (Document in Spanish).

[38]   Tanner, S., Leonard, W.R., McDade, T.W., Reyes-Garcia, V., Godoy, R., et al. (2009) Influence of Helminth Infections on Childhood Nutritional Status in Lowland Bolivia. American Journal of Human Biology, 21, 651-656.
http://dx.doi.org/10.1002/ajhb.20944

[39]   Hurtado, A.M., Lambourne, C.A., James, P., Hill, K., Cheman, K., et al. (2005) Human Rights, Biomedical, Science, and Infectious Diseases among South American Indigenous Groups. Annual Review of Anthropology, 34, 639-665.
http://dx.doi.org/10.1146/annurev.anthro.32.061002.093406

[40]   Abou-Shady, O., El Raziky, M., Zaki, M. and Mohamed, R. (2011) Impact of Giardia lamblia on Growth, Serum Levels of Zinc, Copper, and Iron in Egyptian Children. Biological Trace Element Research, 140, 1-6.
http://dx.doi.org/10.1007/s12011-010-8673-6

[41]   Culha, G. and Sangün, M. (2007) Serum Levels of Zinc, Copper, Iron, Cobalt, Magnesium, and Selenium Elements in Children Diagnosed with Giardia intestinalis and Enterobiosis vermicularis in Hatay, Turkey. Biological Trace Element Research, 118, 21-26.
http://dx.doi.org/10.1007/s12011-007-0017-9

[42]   Ertan, P., Yereli, K., Kurt, O., BalcioGlu, I.C. and OnaG, A. (2002) Serological Levels of Zinc, Copper and Iron Elements among Giardia lamblia Infected Children in Turkey. Pediatrics International, 44, 286-288.
http://dx.doi.org/10.1046/j.1442-200X.2002.01550.x

[43]   Karakas, Z., Demirel, N., Tarakcioglu, M. and Mete, N. (2001) Serum Zinc and Copper Levels in Southeastern Turkish Children with Giardiasis or Amebiasis. Biological Trace Element Research, 84, 11-18.
http://dx.doi.org/10.1385/BTER:84:1-3:011

[44]   Singh, A., Smoak, B.L., Patterson, K.Y., Lemay, L.G., Veillon, C., et al. (1991) Biochemnical Indexes of Selected Trace Minerals in Men-Effect of Stress. American Journal of Clinical Nutrition, 53, 126-131.

[45]   Schroeder, J.J. and Cousins, R.J. (1990) Interleukin 6 Regulates Metallothionein Gene Expression and Zinc Metabolism in Hepatocyte Monolayer Cultures. Proceedings of the National Academy of Sciences, 87, 3137-3141.
http://dx.doi.org/10.1073/pnas.87.8.3137

[46]   CelIksoz, A., Acioz, M., DeGerlI, S., Cinar, Z., Elaldi, N., et al. (2005) Effects of Giardiasis on School Success, Weight and Height Indices of Primary School Children in Turkey. Pediatrics International, 47, 567-571.
http://dx.doi.org/10.1111/j.1442-200x.2005.02110.x

[47]   Goto, R., Panter-Brick, C., Northrop-Clewes, C.A., Manahdhar, R. and Tuladhar, N.R. (2002) Poor Intestinal Permeability in Mildly Stunted Nepali Children: Associations with Weaning Practices and Giardia lamblia Infection. British Journal of Nutrition, 88, 141-149.
http://dx.doi.org/10.1079/BJN2002599

[48]   Marini, E., Maldonado-Contreras, A.L., Cabras, S., Hidalgo, G., Buffa, R., et al. (2007) Helicobacter Pylori and Intestinal Parasites Are Not Detrimental to the Nutritional Status of Amerindians. American Journal of Tropical Medicine and Hygiene, 76, 534-540.

[49]   Berti, P.R., Jones, A.D., Cruz, Y., Larrea, S., Borja, R., et al. (2010) Assessment and Characterization of the Diet of an Isolated Population in the Bolivian Andes. American Journal of Human Biology, 22, 741-749.
http://dx.doi.org/10.1002/ajhb.21075

[50]   Stoltzfus, R.J., Chwaya, H.M., Tielsch, J.M., Schulze, K.J., Albonico, M., et al. (1997) Epidemiology of Iron Deficiency Anemia in Zanzibari Schoolchildren: The Importance of Hookworms. The American Journal of Clinical Nutrition, 65, 153-159.

[51]   Earley, A., Valman, H.B., Altman, D.G. and Pippard, M.J. (1990) Microcytosis, Iron Deficiency, and Thalassaemia in Preschool Children. Archives of Disease in Childhood, 65, 610-614.
http://dx.doi.org/10.1136/adc.65.6.610

[52]   Stoltzfus, R.J., Dreyfuss, M.L., Chwaya, H.M. and Albonico, M. (1997) Hookworm Control as a Strategy to Prevent Iron Deficiency. Nutrition Reviews, 55, 223-232.
http://dx.doi.org/10.1111/j.1753-4887.1997.tb01609.x

[53]   Kalkofen, U.P. (1970) Attachment and Feeding Behavior of Ancylostoma caninum. Zeitschrift Fur Parasitenkunde, 33, 339-354.
http://dx.doi.org/10.1007/BF00331470

[54]   Feng, C.G., Collazo-Custodio, C.M., Eckhaus, M., Hieny, S., Belkaid, Y., et al. (2004) Mice Deficient in LRG-47 Display Increased Susceptibility to Mycobacterial Infection Associated with the Induction of Lymphopenia. The Journal of Immunology, 172, 1163-1168.
http://dx.doi.org/10.4049/jimmunol.172.2.1163

[55]   Klion, A.D. and Nutman, T.B. (2004) The Role of Eosinophils in Host Defense against Helminth Parasites. Journal of Allergy and Clinical Immunology, 113, 30-37.
http://dx.doi.org/10.1016/j.jaci.2003.10.050