1887

Access Microbiology open research platform logo

Volume 6, Issue 11

A systematic review and meta-analysis of the association between neglected tropical diseases and malnutrition: more research needed on diseases other than intestinal parasites, leishmaniasis and leprosy Open Access

Abstract

According to the World Health Organization, neglected tropical diseases (NTDs) affect over two billion people worldwide. While the links between nutrition and many diseases have become clear over recent decades, NTDs have lagged behind and the linkage with nutrition is largely unknown. We conducted this systematic review with meta-analysis to determine the current knowledge on the association between NTDs and malnutrition.

PubMed, Embase, Scopus and African Journals Online databases were searched using predefined search terms. We included all original articles with a case–control design and at least one NTD. The studies had to compare nutritional parameters between infected cases and control participants. Articles that did not report original data were excluded. The quality of the studies was assessed using the Newcastle–Ottawa scale. Pooled estimates were conducted using the random effect model. The publication bias of the studies was determined by funnel plots. and statistics were used to assess the heterogeneity of the studies.

After screening 1294 articles, only 16 qualified for the systematic review and 12 for meta-analysis. These predominately had a focus on soil-transmitted helminthiasis (ascariasis, hookworm diseases and trichuriasis) and schistosomiasis, with a minority concerning leishmaniasis and leprosy. Pooled estimates showed an association between intestinal parasites and stunting in children [odds ratio (OR) = 1.38, 95% confidence interval (CI): 1.14–1.66, = 0%, tau = 0]. We also identified a moderate association established between serum iron deficiency (OR = 4.67, 95% CI: 1.91–11.44, tau = 0) and intestinal parasites.

Of the 20 NTDs, the links between diet and disease have been explored for only 4. There is a paucity of data from low- and middle-income countries and least-developed countries where the NTD burden is high. Therefore, more research into the role of malnutrition in NTDs other than intestinal parasites, leishmaniasis and leprosy is needed.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): meta-analysis , NTDs , nutrition and systematic review
Funding
This study was supported by the:
  • University of Surrey Faculty of Health and Medical Sciences (Award N/A)
    • Principle Award Recipient: AloysiusLoglo
  • Wellcome Trust (Award 202843/Z/16/Z)
    • Principle Award Recipient: RachelE Simmonds
© 2024 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/acmi/10.1099/acmi.0.000800.v3
2024-11-13
2024-12-02
Loading full text...

Full text loading...

/deliver/fulltext/acmi/6/11/acmi000800.v3.html?itemId=/content/journal/acmi/10.1099/acmi.0.000800.v3&mimeType=html&fmt=ahah

References

  1. Reed SL, McKerrow JH. Why funding for neglected tropical diseases should be a global priority. Clin Infect Dis 2018; 67:323–326 [View Article] [PubMed]
     [Google Scholar]
  2. King CH, Bertino A-M. Asymmetries of poverty: why global burden of disease valuations underestimate the burden of neglected tropical diseases. PLoS Neglected Tropical Dis 2008; 2:e209 [View Article]
     [Google Scholar]
  3. Engels D, Zhou X-N. Neglected tropical diseases: an effective global response to local poverty-related disease priorities. Infect Dis Poverty 2020; 9:10 [View Article] [PubMed]
     [Google Scholar]
  4. Fürst T, Salari P, Llamas LM, Steinmann P, Fitzpatrick C et al. Global health policy and neglected tropical diseases: then, now, and in the years to come. PLoS Negl Trop Dis 2017; 11:e0005759 [View Article]
     [Google Scholar]
  5. Balakrishnan VS. WHO’s 2021–30 roadmap for neglected tropical diseases. Lancet Microbe 2021; 2:e11 [View Article]
     [Google Scholar]
  6. Hotez PJ, Aksoy S, Brindley PJ, Kamhawi S. What constitutes a neglected tropical disease?. PLoS Negl Trop Dis 2020; 14:e0008001 [View Article]
     [Google Scholar]
  7. Brooker S, Hotez PJ, Bundy DAP. The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Negl Trop Dis 2010; 4:e779 [View Article]
     [Google Scholar]
  8. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ et al. Helminth infections: the great neglected tropical diseases. J Clin Invest 2008; 118:1311–1321 [View Article] [PubMed]
     [Google Scholar]
  9. Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL et al. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 2012; 142:w13727 [View Article] [PubMed]
     [Google Scholar]
  10. WHO Malnutrition geneva. WHO; 2022 https://www.who.int/news-room/questions-and-answers/item/malnutrition accessed 15 April 2020
  11. Hailegebriel T. Prevalence and determinants of stunting and thinness/wasting among schoolchildren of Ethiopia: a systematic review and meta-analysis. Food Nutr Bull 2020; 41:474–493 [View Article] [PubMed]
     [Google Scholar]
  12. Rousham EK, Pradeilles R, Akparibo R, Aryeetey R, Bash K et al. Dietary behaviours in the context of nutrition transition: a systematic review and meta-analyses in two African countries. Public Health Nutr 2020; 23:1948–1964 [View Article] [PubMed]
     [Google Scholar]
  13. Bosu WK. An overview of the nutrition transition in West Africa: implications for non-communicable diseases. Proc Nutr Soc 2015; 74:466–477 [View Article] [PubMed]
     [Google Scholar]
  14. Scrimshaw NS, Taylor CE, Gordon JE. WHO. Interactions of nutrition and infection World Health Organization monograph series ; no. 57. Geneva: World Health Organization; 1968
  15. Palmer AC, Bedsaul-Fryer JR, Stephensen CB. Interactions of nutrition and infection: the role of micronutrient deficiencies in the immune response to pathogens and implications for child health. Annu Rev Nutr 2024; 44:99–124 [View Article] [PubMed]
     [Google Scholar]
  16. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021; 372:n71 [View Article] [PubMed]
     [Google Scholar]
  17. Dobrescu AI, Nussbaumer-Streit B, Klerings I, Wagner G, Persad E et al. Restricting evidence syntheses of interventions to English-language publications is a viable methodological shortcut for most medical topics: a systematic review. J Clin Epidemiol 2021; 137:209–217 [View Article] [PubMed]
     [Google Scholar]
  18. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010; 25:603–605 [View Article] [PubMed]
     [Google Scholar]
  19. WHO WHO AnthroPlus software: software for assessing growth and development of the world’s children; 2007 https://www.who.int/tools/growth-reference-data-for-5to19-years/application-tools
  20. WHO WHO AnthroPlus for personal computers Manual: software for assessing growth of the world’s children and adolescents. Geneva: WHO; 2009 http://www.who.int/growthref/tools/en/
  21. Amare B, Ali J, Moges B, Yismaw G, Belyhun Y et al. Nutritional status, intestinal parasite infection and allergy among school children in Northwest Ethiopia. BMC Pediatr 2013; 13:1–9 [View Article]
     [Google Scholar]
  22. de Gier B, Nga TT, Winichagoon P, Dijkhuizen MA, Khan NC et al. Species-specific associations between soil-transmitted helminths and micronutrients in Vietnamese schoolchildren. Am J Trop Med Hyg 2016; 95:77–82 [View Article] [PubMed]
     [Google Scholar]
  23. Humphries D, Simms BT, Davey D, Otchere J, Quagraine J et al. Hookworm infection among school age children in kintampo north municipality, Ghana: nutritional risk factors and response to albendazole treatment. Am J Trop Med Hyg 2013; 89:540–548 [View Article]
     [Google Scholar]
  24. Kuong K, Fiorentino M, Perignon M, Chamnan C, Berger J et al. Cognitive performance and iron status are negatively associated with hookworm infection in Cambodian schoolchildren. Am J Trop Med Hyg 2016; 95:856–863 [View Article] [PubMed]
     [Google Scholar]
  25. Lwanga F, Kirunda BE, Orach CG. Intestinal helminth infections and nutritional status of children attending primary schools in Wakiso District, Central Uganda. Int J Environ Res Public Health 2012; 9:2910–2921 [View Article] [PubMed]
     [Google Scholar]
  26. Ross AG, Papier K, Luceres-Catubig R, Chau TN, Inobaya MT et al. Poverty, dietary intake, intestinal parasites, and nutritional status among school-age children in the rural Philippines. Trop Med Infect Dis 2017; 2:49 [View Article] [PubMed]
     [Google Scholar]
  27. Atukorala TS, Lanerolle P. Soil transmitted helminthic infection and its effect on nutritional status of adolescent schoolgirls of low socioeconomic status in Sri Lanka. J Trop Pediatr 1999; 45:18–22 [View Article]
     [Google Scholar]
  28. Quihui-Cota L, Morales-Figueroa GG, Esparza-Romero J, Valencia ME, Astiazarán-García H et al. Trichuriasis and low-iron status in schoolchildren from Northwest Mexico. Eur J Clin Nutr 2010; 64:1108–1115 [View Article] [PubMed]
     [Google Scholar]
  29. Zavala GA, Rosado JL, Doak CM, Caamaño MDC, Campos-Ponce M et al. Energy and food intake are associated with specific intestinal parasitic infections in children of rural Mexico. Parasitol Int 2017; 66:831–836 [View Article] [PubMed]
     [Google Scholar]
  30. Gomes CMC, Giannella-Neto D, Gama MEA, Pereira JCR, Campos MB et al. Correlation between the components of the insulin-like growth factor I system, nutritional status and visceral leishmaniasis. Trans R Soc Trop Med Hyg 2007; 101:660–667 [View Article] [PubMed]
     [Google Scholar]
  31. Kahvaz MS, Soltani S, Soltani S, Carvalheiro MC, Foroutan M. Low serum levels of selenium, zinc, iron, and zinc/copper ratio in an endemic region of cutaneous leishmaniasis in Southwest Iran. Biol Trace Elem Res 2021; 199:1291–1296 [View Article] [PubMed]
     [Google Scholar]
  32. Kocyigit A, Gur S, Erel O, Gurel MS. Associations among plasma selenium, zinc, copper, and iron concentrations and immunoregulatory cytokine levels in patients with cutaneous leishmaniasis. Biol Trace Elem Res 2002; 90:47–55
     [Google Scholar]
  33. Lal CS, Kumar S, Ranjan A, Rabidas VN, Verma N et al. Comparative analysis of serum zinc, copper, magnesium, calcium and iron level in acute and chronic patients of visceral leishmaniasis. J Trace Elem Med Biol 2013; 27:98–102
     [Google Scholar]
  34. Goyonlo VM, Norouzy A, Nemati M, Layegh P, Akhlaghi S et al. Nutritional intake and chronicity associated with the old world cutaneous leishmaniasis: role of vitamin A. Iran J Public Health 2020; 49:167 [View Article]
     [Google Scholar]
  35. Grossi de Oliveira AL, Chaves AT, Santos Cardoso M, Gomide Pinheiro GR, Parreiras de Jesus AC et al. Hypovitaminosis D and reduced cathelicidin are strongly correlated during the multidrug therapy against leprosy. Microb Pathog 2020; 147:104373 [View Article]
     [Google Scholar]
  36. Dennison CL, de Oliveira LB, Fraga LA de O, E Lima RS, Ferreira JA et al. Mycobacterium leprae-helminth co-infections and vitamin D deficiency as potential risk factors for leprosy: a case-control study in south-eastern Brazil. Int J Infect Dis 2021; 105:261–266 [View Article] [PubMed]
     [Google Scholar]
  37. WHO Physical status: the use of and interpretation of anthropometry, report of a WHO expert committee. Geneva: WHO; 1995
  38. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD et al. Helminth parasites--masters of regulation. Immunol Rev 2004; 201:89–116 [View Article] [PubMed]
     [Google Scholar]
  39. Crompton DW, Nesheim MC. Nutritional impact of intestinal helminthiasis during the human life cycle. Ann Rev Nutr 2002; 22:35–59 [View Article]
     [Google Scholar]
  40. de Gier B, Campos Ponce M, van de Bor M, Doak CM, Polman K. Helminth infections and micronutrients in school-age children: a systematic review and meta-analysis. Am J Clin Nutr 2014; 99:1499–1509 [View Article] [PubMed]
     [Google Scholar]
  41. WHO Leishmaniasis [Fact sheet]. Geneva: WHO; 2022 https://www.who.int/news-room/fact-sheets/detail/leishmaniasis
  42. Ikeogu NM, Akaluka GN, Edechi CA, Salako ES, Onyilagha C et al. Leishmania immunity: advancing immunotherapy and vaccine development. Microorganisms 2020; 8:1201 [View Article] [PubMed]
     [Google Scholar]
  43. Farias Amorim C, O. Novais F, Nguyen BT, Nascimento MT, Lago J et al. Localized skin inflammation during cutaneous leishmaniasis drives a chronic, systemic IFN-γ signature. PLoS Negl Trop Dis 2021; 15:e0009321 [View Article]
     [Google Scholar]
  44. Nahidi Y, Mashayekhi Goyonlo V, Layegh P, Marhamati H, Najaf Najafi M. Comparison of serum zinc level in acute improved and chronic cutaneous leishmaniasis. Iran J Dermatol 2021; 24:40–45
     [Google Scholar]
  45. Taghipour A, Abdoli A, Ramezani A, Abolghazi A, Mofazzal Jahromi MA et al. Leishmaniasis and trace element alterations: a systematic review. Biol Trace Elem Res 2021; 199:3918–3938 [View Article] [PubMed]
     [Google Scholar]
  46. Serrano-Coll H, Wan EL, Restrepo-Rivera L, Cardona-Castro N. Leprosy reactions: unraveling immunological mechanisms underlying tissue damage in leprosy patients. Pathog Dis 2024; 82:ftae013 [View Article] [PubMed]
     [Google Scholar]
  47. WHO Leprosy (Hansen’s disease). Geneva, Switzerland: WHO; 2022 https://www.who.int/data/gho/data/themes/topics/leprosy-hansens-disease
  48. Dwivedi VP, Banerjee A, Das I, Saha A, Dutta M et al. Diet and nutrition: an important risk factor in leprosy. Microb Pathog 2019; 137:103714 [View Article] [PubMed]
     [Google Scholar]
  49. Shaik-Dasthagirisaheb YB, Varvara G, Murmura G, Saggini A, Caraffa A et al. Role of vitamins D, E and C in immunity and inflammation. J Biol Regul Homeost Agents 2013; 27:291–295 [PubMed]
     [Google Scholar]
  50. Rivas-Santiago B, Hernandez-Pando R, Carranza C, Juarez E, Contreras JL et al. Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect Immun 2008; 76:935–941 [View Article] [PubMed]
     [Google Scholar]
  51. Liu PT, Stenger S, Li H, Wenzel L, Tan BH et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006; 311:1770–1773 [View Article] [PubMed]
     [Google Scholar]
  52. Singh I, Lavania M, Pathak VK, Ahuja M, Turankar RP et al. VDR polymorphism, gene expression and vitamin D levels in leprosy patients from North Indian population. PLoS Negl Trop Dis 2018; 12:e0006823 [View Article]
     [Google Scholar]
  53. McMillan DC, Maguire D, Talwar D. Relationship between nutritional status and the systemic inflammatory response: micronutrients. Proc Nutr Soc 2019; 78:56–67 [View Article] [PubMed]
     [Google Scholar]
  54. Galloway SP, McMillan DC, Sattar N. Effect of the inflammatory response on trace element and vitamin status. Ann Clin Biochem 2000; 37:289–297 [View Article]
     [Google Scholar]
  55. Phillips RO, Sarfo FS, Landier J, Oldenburg R, Frimpong M et al. Combined inflammatory and metabolic defects reflected by reduced serum protein levels in patients with Buruli ulcer disease. PLoS Negl Trop Dis 2014; 8:e2786 [View Article] [PubMed]
     [Google Scholar]
  56. de Gier B, Pita-Rodríguez GM, Campos-Ponce M, van de Bor M, Chamnan C et al. Soil-transmitted helminth infections and intestinal and systemic inflammation in schoolchildren. Acta Tropica 2018; 182:124–127 [View Article]
     [Google Scholar]
  57. Suchdev PS, Namaste SML, Aaron GJ, Raiten DJ, Brown KH et al. Overview of the Biomarkers Reflecting Inflammation and Nutritional Determinants of Anemia (BRINDA) project. Adv Nutr 2016; 7:349–356 [View Article] [PubMed]
     [Google Scholar]
  58. Luo H, Geng J, Zeiler M, Nieckula E, Sandalinas F et al. A practical guide to adjust micronutrient biomarkers for inflammation using the BRINDA method. J Nutr 2023; 153:1265–1272 [View Article] [PubMed]
     [Google Scholar]
  59. D’Oliveira A Jr, Machado P, Bacellar O, Cheng LH, Almeida RP et al. Evaluation of IFN-gamma and TNF-alpha as immunological markers of clinical outcome in cutaneous leishmaniasis. Rev Soc Bras Med Trop 2002; 35:7–10 [View Article] [PubMed]
     [Google Scholar]
  60. Wasunna KM, Raynes JG, Were JB, Muigai R, Sherwood J et al. Acute phase protein concentrations predict parasite clearance rate during therapy for visceral leishmaniasis. Trans R Soc Trop Med Hyg 1995; 89:678–681 [View Article] [PubMed]
     [Google Scholar]
  61. Singh UK, Patwari AK, Sinha RK, Kumar R. Prognostic value of serum C-reactive protein in kala-azar. J Trop Pediatr 1999; 45:226–228 [View Article] [PubMed]
     [Google Scholar]
  62. Budge S, Parker AH, Hutchings PT, Garbutt C. Environmental enteric dysfunction and child stunting. Nutr Rev 2019; 77:240–253 [View Article] [PubMed]
     [Google Scholar]
  63. Yotsu RR, Fuller LC, Murdoch ME, van Brakel WH, Revankar C et al. A global call for action to tackle skin-related neglected tropical diseases (skin NTDs) through integration: an ambitious step change. PLoS Negl Trop Dis 2023; 17:e0011357 [View Article]
     [Google Scholar]
  64. Cook JD, Flowers CH, Skikne BS. The quantitative assessment of body iron. Blood 2003; 101:3359–3364 [View Article] [PubMed]
     [Google Scholar]
/content/journal/acmi/10.1099/acmi.0.000800.v3
Loading
A systematic review and meta-analysis of the association between neglected tropical diseases and malnutrition: more research needed on diseases other than intestinal parasites, leishmaniasis and leprosy
Access Microbiology 6, 000800.v3 (2024); https://doi.org/10.1099/acmi.0.000800.v3
/content/journal/acmi/10.1099/acmi.0.000800.v3
/content/journal/acmi/10.1099/acmi.0.000800.v3
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error