Nutritional Status of Patients with Cutaneous Leishmaniasis from a Tropical Area of Bolivia, and Implications for Zinc Bioavailability


Macro and micronutrient deficiencies are a significant problem among people in rural areas in developing countries. Deficiencies may lead to an impaired immune system making the organism vulnerable to infections and diseases. In this paper, the dietary intake, anthropometric measurements, zinc and copper levels in serum, of patients with cutaneous leishmaniasis (CL) are compared with a group of healthy controls and reference values. Results showed no significant differences in most nutrient intake or anthropometrics between patients and controls. However, serum zinc level of patients (80 μg/dl) was significantly lower (P < 0.001) than in controls (85 μg/dl), likely explained by the presence of leishmaniasis. The median serum zinc level in both groups was below the reference values, even though their median zinc intake met the zinc recommendations from WHO. Consequently, besides the presence of leishmaniasis, serum zinc levels may be compromised by inhibitory components in their diet, such as phytates, as it is shown by the molar ratio phytate:zinc (Phy:Zn) that was between 11 and 19, while 15 is the level said to compromise zinc status. There were significant (P < 0.05) negative correlations between serum zinc and Phy:Zn, for patients (r = - 0.413) and controls (r = - 0.410). In conclusion this study shows that patients with CL in Chapare, Bolivia had low serum zinc levels due to the leishmaniasis per se and the decreased zinc bioavailability in their diet. CL infection was not in direct association with the nutritional status indicated by the anthropometric or dietary assessments. However, dietary intake showed 5 essential nutrients below the nutrient recommendation in both groups.

Share and Cite:

C. Lazarte, C. Alegre, E. Rojas and Y. Granfeldt, "Nutritional Status of Patients with Cutaneous Leishmaniasis from a Tropical Area of Bolivia, and Implications for Zinc Bioavailability," Food and Nutrition Sciences, Vol. 4 No. 10A, 2013, pp. 49-60. doi: 10.4236/fns.2013.410A009.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] R. K. Chandra, “Nutrition and the Immune System: An Introduction,” The American Journal of Clinical Nutrition, Vol. 62, No. 2, 1997, pp. 460S-463S.
[2] R. W. Ashford, P. Desjeux and P. Deraadt, “Estimation of Population at Risk of Infection and Number of Cases of Leishmaniasis,” Parasitology Today, Vol. 8, No. 3, 1992, pp. 104-105.
[3] R. Reithinger, et al., “Cutaneous Leishmaniasis,” The Lancet Infectious Diseases, Vol. 7, No. 9, 2007, pp. 581-596.
[4] A. L. García, et al., “Leishmaniases in Bolivia: Comprehensive Review and Current Status,” The American Journal of Tropical Medicine and Hygiene, Vol. 80, No. 5, 2009, pp. 704-711.
[5] E. Rojas, et al., ”Leishmaniasis in Chaparé, Bolivia,” Emerging Infectious Diseases, Vol. 15, No. 4, 2009, pp. 678-680.
[6] L. Soong, C. A. Henard and P. C. Melby, “Immunopathogenesis of Non-Healing American Cutaneous Leishmaniasis and Progressive Visceral Leishmaniasis,” Seminars in Immunopathology, Vol. 34, No. 6, 2012, pp. 735751.
[7] A. J. M. Caldas, et al., “Leishmania (Leishmania) Chagasi Infection in Children from an Endemic Area of American Visceral Leishmaniasis on Sao Luis Island, Maranhao, Brazil,” Revista da Sociedade Brasileira de Medicina Tropical, Vol. 34, No. 5, 2001, pp. 445-451.
[8] D. F. D. Cunha, et al., “Retardo do Crescimento em Criancas com Reacao Intradérmica Positiva para Leishmaniose: Resultados Preliminares,” Revista da Sociedade Brasileira de Medicina Tropical, Vol. 34, No. 1, 2001, pp. 25-27.
[9] M. M. Weigel, et al., “Nutritional Status and Cutaneous Leishmaniasis in Rural Ecuadorian Children,” Journal of Tropical Pediatrics, Vol. 41, No. 1, 1995, pp. 22-28.
[10] B. L. L. Maciel, et al., “Association of Nutritional Status with the Response to Infection with Leishmania chagasi,” The American Journal of Tropical Medicine and Hygiene, Vol. 79, No. 4, 2008, pp. 591-598.
[11] H. Perez, I. Malave and B. Arredondo, “Effects of Protein-Malnutrition on the Course of Leishmania-Mexicana Infection in C57B1-6 Mice-Nutrition and Susceptibility to Leishmaniasis,” Clinical and Experimental Immunology, Vol. 38, No. 3, 1979, pp. 453-460.
[12] G. Malafaia, “Protein-Energy Malnutrition as a Risk Factor for Visceral Leishmaniasis: A Review,” Parasite Immunology, Vol. 31, No. 10, 2009, pp. 587-596.
[13] R. S. Gibson, “Principles of Nutritional Assessment,” 2nd Edition, Oxford University Press, New York, 2005.
[14] WHO, “Physical Status: The Use and Interpretation of Anthropometry in Technical Report Series No.8541995,” World Health Organization, Geneva.
[15] C. Lazarte, et al., “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, Vol. 11, No. 1, 2012, p. 61.
[16] R. S. Gibson, et al., “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, Vol. 31, No. S2, 2010, pp. 134-146.
[17] R. S. Gibson and C. Hotz, “Dietary Diversification/Modification Strategies to Enhance Micronutrient Content and Bioavailability of Diets in Developing Countries,” British Journal of Nutrition, Vol. 85, 2001, pp. S159-S166.
[18] B. Lonnerdal, “Dietary Factors Influencing Zinc Absorption,” The Journal of Nutrition, Vol. 130, No. 5, 2000, pp. 1378S-1383S.
[19] B. Sandstrom, “Bioavailability of Zinc,” European Journal of Clinical Nutrition, Vol. 51, 1997, pp. S17-S19.
[20] E. L. Ferguson, et al., “Dietary Calcium, Phytate and Zinc Intakes and the Calcium, Phytate and Zinc Molar Ratios of the Diets of a Selected Group of East-African Children,” American Journal of Clinical Nutrition, Vol. 50, No. 6, 1989, pp. 1450-1456.
[21] C. Hotz and K. H. Brown, “International Zinc Nutrition Consultative Group (IZiNCG) Technical Document #1. Assessment of the Risk of Zinc Deficiency in Populations and Options for Its Control,” Food and Nutrition Bulletin, Vol. 25, No. 1, 2004, pp. S94-S203.
[22] C., Hotz, et al., “Assessment of the Trace Element Status of Individuals and Populations: The Example of Zinc and Copper,” The Journal of Nutrition, Vol. 133, No. 5, 2003, pp. 1563S-1568S.
[23] A. S. Prasad, “Effects of Zinc Deficiency on Immune Functions,” Journal of Trace Elements in Experimental Medicine, Vol. 13, No. 1, 2000, pp. 1-20.<1::AID-JTRA3>3.0.CO;2-2
[24] P. Shetty, “Zinc Deficiency and Infections. Nutrition, Immunity and Infection,” Cabi Publishing, Wallingford, 2010, pp. 101-113.
[25] A. Kocyigit, et al., “Alterations of Serum Selenium, Zinc, Copper, and Iron Concentrations and Some Related Antioxidant Enzyme Activities in Patients with Cutaneous Leishmaniasis,” Biological Trace Element Research, Vol. 65, No. 3, 1998, pp. 271-281.
[26] M. Faryadi and M. Mohebali, “Alterations of Serum Zinc, Copper and Iron Concentrations in Patients with Acute and Chronic Cutaneous Leishmaniasis,” Iranian Journal of Public Health, Vol. 4, 2003, p. 53.
[27] M. F. Zubieta Durán and M. C. Torrico Rojas, “Manual de Normas y Procedimientos Técnicos de Laboratorio (para Leishmaniasis 2010: Ministerio de Salud y Deportes Bolivia,”, 2010.
[28] A. R. Frisancho, “Triceps Skin Fold and Upper Arm Muscle Size Norms for Assessment of Nutritional Status,” The American Journal of Clinical Nutrition, Vol. 27, No. 10, 1974, pp. 1052-1058.
[29] USDA, “USDA National Nutrient Database for Standard Reference,” 2001.
[30] INLASA, ”Tabla de Composicion de Alimentos Bolivianos,” C. Edicion, Ed., Ministerio de Salud y Deportes, La Paz, 2005.
[31] WHO and FAO, “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), 2003.
[32] N. R. Reddy, “Occurrence, Distribution, Content, and Dietary Intake of Phytate,” Food Phytates, CRC Press, 2001.
[33] R. M. Garc??a-Estepa, E. Guerra-Hernández and B. Garc??a-Villanova, “Phytic Acid Content in Milled Cereal Products and Breads,” Food Research International, Vol. 32, No. 3, 1999, pp. 217-221.
[34] B. Q. Phillippy, M. Lin and B. Rasco, “Analysis of Phytate in Raw and Cooked Potatoes,” Journal of Food Composition and Analysis, Vol. 17, No. 2, 2004, pp. 217-226.
[35] J. Ruales and B. M. Nair, “Saponins, Phytic Acid, Tannins and Protease Inhibitors in Quinoa (Chenopodium Quinoa, Willd) Seeds,” Food Chemistry, Vol. 48, No. 2, 1993, pp. 137-143.
[36] A. Taylor, “Measurement of Zinc in Clinical Samples,” Annals of Clinical Biochemistry, Vol. 34, No. 2, 1997, pp. 142-150.
[37] G. R. Goldberg, et al., “Critical-Evaluation of EnergyIntake Data Using Fundamental Principles of Energy Physiology. Derivation of Cutoff Limits to Identify Under-Recording,” European Journal of Clinical Nutrition, Vol. 45, No. 12, 1991, pp. 569-581.
[38] C. Hotz, J. M. Peerson and K. H. Brown, “Suggested Lower Cutoffs of Serum Zinc Concentrations for Assessing Zinc Status: Reanalysis of the Second National Health and Nutrition Examination Survey Data (1976-1980),” The American Journal of Clinical Nutrition, Vol. 78, No. 4, 2003, pp. 756-764.
[39] M. A. Knovich, et al., “The Association between Serum Copper and Anaemia in the Adult Second National Health and Nutrition Examination Survey (NHANES II) Population,” British Journal of Nutrition, Vol. 99, No. 6, 2008, pp. 1226-1229.
[40] WHO, “Trace Elements in Human and Health Nutrition,” 1996.
[41] J. Van Weyenbergh, et al., “Zinc/Copper Imbalance Reflects Immune Dysfunction in Human Leishmaniasis: An ex Vivo and in Vitro Study,” BMC Infectious Diseases, Vol. 4, No. 1, 2004, p. 50.
[42] J. Mishra, S. Carpenter and S. Singh, “Low Serum Zinc Levels in an Endemic Area of Visceral Leishmaniasis in Bihar,” Indian Journal of Medical Research, Vol. 131, No. 6, 2010, pp. 793-798.
[43] J. J. Schroeder and R. J. Cousins, “Interleukin 6 Regulates Metallothionein Gene Expression and Zinc Metabolism in Hepatocyte Monolayer Cultures,” Proceedings of the National Academy of Sciences, Vol. 87, No. 8, 1990, pp. 3137-3141.
[44] J. P. Liuzzi, et al., “Interleukin-6 Regulates the Zinc Transporter Zip14 in Liver and Contributes to the Hypozincemia of the Acute-Phase Response,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 102, No. 19, 2005, pp. 6843-6848.
[45] K. E. Sharquie, et al., “Oral Zinc Sulphate in the Treatment of Acute Cutaneous Leishmaniasis,” Clinical and Experimental Dermatology, Vol. 26, No. 1, 2001, pp. 2126.
[46] G. Culha, E. Yalin and K. Sanguen, “Alterations in Serum Levels of Trace Elements in Cutaneous Leishmaniasis Patients in Endemic Region of Hatay (Antioch),” Asian Journal of Chemistry, Vol. 20, No. 4, 2008, pp. 3104-3108.
[47] I. M. Goldstein, et al., “Ceruloplasmin: A Scavenger of Superoxide Anion Radicals,” Journal of Biological Chemistry, Vol. 254, No. 10, 1979, pp. 4040-4045.
[48] C. A. Dinarello, “Interleukin-1 and the Pathogenesis of the Acute-Phase Response,” New England Journal of Medicine, Vol. 311, No. 22, 1984, pp. 1413-1418.
[49] M. Panemangalore and F. N. Bebe, “Effect of High Dietary Zinc on Plasma Ceruloplasmin and Erythrocyte Superoxide Dismutase Activities in Copper-Depleted and Repleted Rats,” Biological Trace Element Research, Vol. 55, No. 1-2, 1996, pp. 111-126.
[50] Y. Abebe, et al., “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, Vol. 20, No. 3-4, 2007, pp. 161-168.
[51] E. I. Adeyeye, et al., “Calcium, Zinc and Phytate Interrelationships in Some Foods of Major Consumption in Nigeria,” Food Chemistry, Vol. 71, No. 4, 2000, pp. 435441.
[52] K. C. Menon, et al., “Concurrent Micronutrient Deficiencies Are Prevalent in Nonpregnant Rural and Tribal Women from CENTRAL INDIA,” Nutrition, Vol. 27, No. 4, 2011, pp. 496-502.
[53] R. F. Hurrell, “Phytic Acid Degradation as a Means of Improving Iron Absorption,” International Journal for Vitamin and Nutrition Research, Vol. 74, No. 6, 2004, pp. 445-452.
[54] M. Umeta, C. E. West and H. Fufa, “Content of Zinc, Iron, Calcium and Their Absorption Inhibitors in Foods Commonly Consumed in Ethiopia,” Journal of Food Composition and Analysis, Vol. 18, No. 8, 2005, pp. 803817.
[55] K. H. Brown, “Effect of Infections on Plasma Zinc Concentration and Implications for Zinc Status Assessment in Low-Income Countries,” American Journal of Clinical Nutrition, Vol. 68, No. 2, 1998, pp. 425S-429S.
[56] S. Y. Hess, et al., “Use of Serum Zinc Concentration as an Indicator of Population Zinc Status,” Food & Nutrition Bulletin, Vol. 28, No. 3, 2007, pp. 403S-429S.
[57] U. M. Donovan and R. S. Gibson, “Iron and Zinc Status of Young-Women Aged 14 to 19 Years Consuming Vegetarian and Omnivorous Diets,” Journal of the American College of Nutrition, Vol. 14, No. 5, 1995, pp. 463-472.
[58] R. S. Gibson, et al., “Are Changes in Food Consumption Patterns Associated with Lower Biochemical Zinc Status among Women from Dunedin, New Zealand?” British Journal of Nutrition, Vol. 86, No. 1, 2001, pp. 71-80.
[59] D. B. Milne and P. E. Johnson, “Assessment of Copper Status: Effect of Age and Gender on Reference Ranges in Healthy Adults,” Clinical Chemistry, Vol. 39, No. 5, 1993, pp. 883-887.
[60] D. F. Cunha, et al., “Is an Increased Body Mass Index Associated with a Risk of Cutaneous Leishmaniasis?” Revista da Sociedade Brasileira de Medicina Tropical, Vol. 42, No. 5, 2009, pp. 494-495.
[61] B. S. Kumari and R. K. Chandra, “Overnutrition and Immune-Responses,” Nutrition Research, Vol. 13, No. 1, 1993, S3-S18.
[62] S. Samartin and R. K. Chandra, “Obesity, Overnutrition and the Immune System,” Nutrition Research, Vol. 21, No. 1-2, 2001, pp. 243-262.
[63] O. I. Bermudez and K. L. Tucker, “Trends in Dietary Patterns of Latin American Populations,” Cadernos de Saúde Pública, Vol. 19, No. 1, 2003, pp. S87-S99.
[64] M. N. Bassett, D. Romaguera and N. Samman, “Nutritional Status and Dietary Habits of the Population of the Calchaqui Valleys of Tucuman, Argentina,” Nutrition, Vol. 27, No. 11-12, 2010, pp. 1130-1135.
[65] M. Gibbs, et al., “The Adequacy of Micronutrient Concentrations in Manufactured Complementary Foods from Low-Income Countries,” Journal of Food Composition and Analysis, Vol. 24, No. 3, 2011, pp. 418-426.
[66] IOM, “Prevention of Micronutrient Deficiencies: Tools for Policymakers and Public Health Workers,” The National Academies Press, Washington DC, 1998.
[67] G. L. L. Machado-Coelho, et al., “Risk Factors for Mucosal Manifestation of American Cutaneous Leishmaniasis,” Transactions of the Royal Society of Tropical Medicine and Hygiene, Vol. 99, No. 1, 2005, pp. 55-61.

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.