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Association Between Food Insecurity and HIV Viral Suppression: A Systematic Review and Meta-Analysis

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Abstract

Although an increasing number of HIV infected people are accessing antiretroviral treatment, many do not achieve complete HIV viral suppression and remain at risk for AIDS and capable of HIV transmission. Food insecurity has been identified as a potential risk factor for poor virologic response, but the association between these factors has been inconsistently documented in the literature. We systematically searched five electronic databases and bibliographies of relevant studies through April 2015 and retrieved 11 studies that met our inclusion criteria, of which nine studies were conducted in North America and the remaining two studies were in Brazil and Uganda respectively. Meta-analyzed results indicated that experiencing food insecurity resulted in 29% lower odds of achieving complete HIV viral suppression (OR = 0.71, 95% CI 0.61–0.82) and this significant inverse association was consistently found regardless of study design, exposure measurement, and confounder adjustment methods. These findings suggest that food insecurity is a potential risk factor for incomplete HIV viral suppression in people living with HIV.

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References

  1. Joint United Nations Programme on HIV/AIDS (UNAIDS). Global AIDS Update 2016. http://www.unaids.org/sites/default/files/media_asset/global-AIDS-update-2016_en.pdf. Accessed 28 Jun 2016.

  2. Boender TS, Sigaloff KC, McMahon JH, et al. Long-term virological outcomes of first-line antiretroviral therapy for HIV-1 in low- and middle-income countries: a systematic review and meta-analysis. Clin Infect Dis. 2015;61(9):1453–61.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Heath K, Samji H, Nosyk B, et al. Cohort profile: seek and treat for the optimal prevention of HIV/AIDS in British Columbia (STOP HIV/AIDS BC). Int J Epidemiol. 2014;43(4):1073–81.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Shuter J, Sarlo JA, Kanmaz TJ, Rode RA, Zingman BS. HIV-infected patients receiving lopinavir/ritonavir-based antiretroviral therapy achieve high rates of virologic suppression despite adherence rates less than 95%. J Acquir Immune Defic Syndr. 2007;45(1):4–8.

    Article  CAS  PubMed  Google Scholar 

  5. Chakraborty H, Sen PK, Helms RW, et al. Viral burden in genital secretions determines male-to-female sexual transmission of HIV-1: a probabilistic empiric model. Aids. 2001;15(5):621–7.

    Article  CAS  PubMed  Google Scholar 

  6. Garcia PM, Kalish LA, Pitt J, et al. Maternal levels of plasma human immunodeficiency virus type 1 RNA and the risk of perinatal transmission. Women and Infants Transmission Study Group. N Engl J Med. 1999;341(6):394–402.

    Article  CAS  PubMed  Google Scholar 

  7. Wang EA, McGinnis KA, Fiellin DA, et al. Food insecurity is associated with poor virologic response among HIV-infected patients receiving antiretroviral medications. J Gen Intern Med. 2011;26(9):1012–8.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Weiser SD, Frongillo EA, Ragland K, Hogg RS, Riley ED, Bangsberg DR. Food insecurity is associated with incomplete HIV RNA suppression among homeless and marginally housed HIV-infected individuals in San Francisco. J Gen Intern Med. 2009;24(1):14–20.

    Article  PubMed  Google Scholar 

  9. Anderson SA. Core indicators of nutritional state for difficult-to-sample populations. J Nutr. 1990;120(Suppl 11):1559–600.

    Google Scholar 

  10. Bickel G, Nord M, Price C, Hamilton W, Cook J. Guide to Measuring Household Food Security, Revised 2000. Alexandria: US Department of Agriculture, Food and Nutrition Service, March 2000. http://www.fns.usda.gov/sites/default/files/FSGuide.pdf. Accessed 23 Jun 2016.

  11. Coates J, Swindale A, Bilinsky P. Household Food Insecurity Access Scale (HFIAS) for Measurement of Food Access: Indicator Guide (v. 3). Washington, D.C : Food and Nutrition Technical Assistance Project, Academy for Educational Development, August 2007. http://www.fao.org/fileadmin/user_upload/eufao-fsi4dm/doc-training/hfias.pdf. Accessed 30 Jun 2016.

  12. Radimer KL, Olson CM, Campbell CC. Development of indicators to assess hunger. J Nutr. 1990;120(Suppl 11):1544–8.

    PubMed  Google Scholar 

  13. Anema A, Weiser SD, Fernandes KA, et al. High prevalence of food insecurity among HIV-infected individuals receiving HAART in a resource-rich setting. AIDS Care. 2011;23(2):221–30.

    Article  CAS  PubMed  Google Scholar 

  14. Weiser SD, Bangsberg DR, Kegeles S, Ragland K, Kushel MB, Frongillo EA. Food insecurity among homeless and marginally housed individuals living with HIV/AIDS in San Francisco. AIDS Behav. 2009;13(5):841–8.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Chen Y, Kalichman SC. Synergistic effects of food insecurity and drug use on medication adherence among people living with HIV infection. J Behav Med. 2015;38(3):397–406.

    Article  PubMed  Google Scholar 

  16. Hong SY, Fanelli TJ, Jonas A, et al. Household food insecurity associated with antiretroviral therapy adherence among HIV-infected patients in Windhoek, Namibia. J Acquir Immune Defic Syndr. 2014;67(4):e115–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Kalichman SC, Grebler T, Amaral CM, et al. Food insecurity and antiretroviral adherence among HIV positive adults who drink alcohol. J Behav Med. 2014;37(5):1009–18.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Weiser SD, Palar K, Frongillo EA, et al. Longitudinal assessment of associations between food insecurity, antiretroviral adherence and HIV treatment outcomes in rural Uganda. AIDS. 2014;28(1):115–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Kalichman SC, Washington C, Grebler T. Medication adherence and health outcomes of people living with HIV who are food insecure and prescribed antiretrovirals that should be taken with food. Infect Dis Ther. 2015;. doi:10.1007/s40121-015-0057-y.

    PubMed  PubMed Central  Google Scholar 

  20. Singer AW, Weiser SD, McCoy SI. Does food insecurity undermine adherence to antiretroviral therapy? A systematic review. AIDS Behav. 2015;19(8):1510–26.

    Article  PubMed  Google Scholar 

  21. Kiehne E, Mendoza NS. Migrant and seasonal farmworker food insecurity: prevalence, impact, risk factors, and coping strategies. Soc Work Public Health. 2015;30(5):397–409.

    Article  PubMed  Google Scholar 

  22. Leung CW, Epel ES, Ritchie LD, Crawford PB, Laraia BA. Food insecurity is inversely associated with diet quality of lower-income adults. J Acad Nutr Diet. 2014;114(12):1943–53.

    Article  PubMed  Google Scholar 

  23. McIntyre L, Bartoo AC, Pow J, Potestio ML. Coping with child hunger in Canada: have household strategies changed over a decade? Can J Public Health. 2012;103(6):e428–32.

    PubMed  Google Scholar 

  24. Kirkpatrick SI, Tarasuk V. Food insecurity is associated with nutrient inadequacies among Canadian adults and adolescents. J Nutr. 2008;138(3):604–12.

    CAS  PubMed  Google Scholar 

  25. Cunningham-Rundles S, McNeeley DF, Moon A. Mechanisms of nutrient modulation of the immune response. J Allergy Clin Immunol. 2005;115(6):1119–28 quiz 29.

    Article  CAS  PubMed  Google Scholar 

  26. Drain PK, Kupka R, Mugusi F, Fawzi WW. Micronutrients in HIV-positive persons receiving highly active antiretroviral therapy. Am J Clin Nutr. 2007;85(2):333–45.

    CAS  PubMed  Google Scholar 

  27. Anema A, Kerr T, Milloy MJ, Feng C, Montaner JSG, Wood E. Relationship between hunger, adherence to antiretroviral therapy and plasma HIV RNA suppression among HIV-positive illicit drug users in a Canadian setting. AIDS Care. 2014;26(4):459–65.

    Article  PubMed  Google Scholar 

  28. Weiser SD, Yuan C, Guzman D, et al. Food insecurity and HIV clinical outcomes in a longitudinal study of urban homeless and marginally housed HIV-infected individuals. AIDS. 2013;27(18):2953–8.

    Article  PubMed  Google Scholar 

  29. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9 w64.

    Article  PubMed  Google Scholar 

  30. Wells GA, Shea B, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non randomised studies in meta-analyses. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp. Accessed 28 Jun 2016.

  31. Herzog R, Alvarez-Pasquin MJ, Diaz C, Del Barrio JL, Estrada JM, Gil A. Are healthcare workers’ intentions to vaccinate related to their knowledge, beliefs and attitudes? a systematic review. BMC Public Health. 2013;13:154.

    Article  PubMed  PubMed Central  Google Scholar 

  32. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.

    Article  CAS  PubMed  Google Scholar 

  33. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–58.

    Article  PubMed  Google Scholar 

  34. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Charao AP, Batista MH, Ferreira LB. Food insecurity of HIV/AIDS patients at a unit of outpatient healthcare system in Brasilia, Federal District, Brazil. Rev Soc Bras Med Trop. 2012;45(6):751–3.

    Article  PubMed  Google Scholar 

  36. Kalichman SC, Cherry C, Amaral C, et al. Health and treatment implications of food insufficiency among people living with HIV/AIDS, Atlanta, Georgia. J Urban Health. 2010;87(4):631–41.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Kalichman SC, Washington C, Grebler T, et al. Treatment outcomes among people living with HIV who are food insecure and prescribed antiretrovirals taken with food. J Prim Care Community Health. 2015;6(1):35–40.

    Article  PubMed  Google Scholar 

  38. Feldman MB, Alexy ER, Thomas JA, Gambone GF, Irvine MK. The Association between food insufficiency and HIV treatment outcomes in a longitudinal analysis of HIV-infected individuals in New York City. J Acquir Immune Defic Syndr. 2015;69(3):329–37.

    Article  PubMed  Google Scholar 

  39. Shannon K, Kerr T, Milloy MJ, et al. Severe food insecurity is associated with elevated unprotected sex among HIV-seropositive injection drug users independent of HAART use. AIDS. 2011;25(16):2037–42.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Duval S, Tweedie R. A Nonparametric, “Trim and Fill” Method of Accounting for Publication Bias in Meta-Analysis. J Am Stat Assoc. 2000;95(449):89–98.

    Google Scholar 

  41. Hill AB. The environment and disease: association or causation? Proc R Soc Med. 1965;58(5):295–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Robins JM. Marginal structural models. In: 1997 Proceedings of the Section on Bayesian Statistical Science. American Statistical Association. 1998:1–10

  43. Robins JM. Marginal structural models versus structural nested models as tools for causal inference. In: Halloran ME, Berry D, editors. Statistical models in epidemiology, the environment, and clinical trials. New York: Springer; 2000. p. 95–134.

    Chapter  Google Scholar 

  44. Szklo M, Nieto FJ. Epidemiology: beyond the basics. Sudbury : Jones and Bartlett Publishers; 2007.

    Google Scholar 

  45. Low-Beer S, Yip B, O’Shaughnessy MV, Hogg RS, Montaner JS. Adherence to triple therapy and viral load response. J Acquir Immune Defic Syndr. 2000;23(4):360–1.

    Article  CAS  PubMed  Google Scholar 

  46. Maher K, Klimas N, Fletcher MA, et al. Disease progression, adherence, and response to protease inhibitor therapy for HIV infection in an Urban Veterans Affairs Medical Center. J Acquir Immune Defic Syndr. 1999;22(4):358–63.

    Article  CAS  PubMed  Google Scholar 

  47. Schisterman EF, Cole SR, Platt RW. Overadjustment bias and unnecessary adjustment in epidemiologic studies. Epidemiology. 2009;20(4):488–95.

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

Supported in part by the Food Security & HIV-HCV Study of the Canadian Co-infection Cohort, which is funded by the Canadian Institutes of Health Research (CIHR) and the CIHR Canadian HIV Trials Network (CTN 264).

Author information

Authors and Affiliations

  1. Department of Epidemiology, Biostatistics and Occupational Health, McGill University, Montreal, QC, Canada

    Wusiman Aibibula, Joseph Cox, Anne-Marie Hamelin, Taylor McLinden, Marina B. Klein & Paul Brassard

  2. Public Health Department, CIUSSS du Centre-Est-de-l ‘Ile-de-Montréal, Montréal, QC, Canada

    Joseph Cox

  3. Department of Medicine, McGill University, Montreal, QC, Canada

    Marina B. Klein & Paul Brassard

  4. Division of Clinical Epidemiology, McGill University Health Centre, Montreal, QC, Canada

    Paul Brassard

  5. Centre for Clinical Epidemiology, Jewish General Hospital, 3755 Cote Sainte-Catherine, Pavilion H 424.1, Montreal, QC, H3T 1E2, Canada

    Paul Brassard

Authors
  1. Wusiman Aibibula
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  2. Joseph Cox
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  3. Anne-Marie Hamelin
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  4. Taylor McLinden
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  6. Paul Brassard
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Corresponding author

Correspondence to Paul Brassard.

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Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants performed by any of the authors.

Appendices

Appendix A

PubMed

  1. 1.

    (Human immunodeficiency viruses[MeSH Terms] OR hiv[Title/Abstract] OR aids[Title/Abstract] OR human immunodeficiency virus[Title/Abstract] OR human immuno deficiency virus[Title/Abstract] OR human immuno-deficiency virus[Title/Abstract] OR human immunodeficiency viruses[Title/Abstract] OR human immuno deficiency viruses[Title/Abstract] OR human immuno-deficiency viruses[Title/Abstract] OR acquired immunodeficiency syndrome[Title/Abstract] OR acquired immuno deficiency syndrome[Title/Abstract] OR acquired immuno-deficiency syndrome[Title/Abstract] OR acquired immunodeficiency syndromes[Title/Abstract] OR acquired immuno deficiency syndromes[Title/Abstract] OR acquired immuno-deficiency syndromes[Title/Abstract]).

  2. 2.

    (Food security[MeSH Terms] OR hunger[MeSH Terms] OR malnutrition[MeSH Terms] OR food security[Title/Abstract] OR malnutrition[Title/Abstract] OR hunger[Title/Abstract] OR food insufficienc*[Title/Abstract]).

  3. 3.

    (Viral load[MeSH Terms] OR viral rna[MeSH Terms] OR viral load[Title/Abstract] OR viral rna[Title/Abstract] OR virus load[Title/Abstract] OR virus rna[Title/Abstract]).

1 AND 2 AND 3.

101 citations as of April 15th, 2015.

Web of Science

TS = (hiv OR human immunodeficiency virus* OR human immuno deficiency virus* OR human immuno-deficiency virus* OR aids OR acquired immunodeficiency syndrome* OR acquired immuno deficiency syndrome* OR acquired immuno-deficiency syndrome*).

TS = (food security* OR food insecurity* OR nutrition* OR hunger* OR food insufficiency*).

TS = (viral load* OR viral rna* OR virus load OR virus rna).

1 AND 2 AND 3.

223 citations as of April 15th, 2015.

ProQuest ABI/INFORM Complete

(Hiv OR human immunodeficiency virus* OR human immuno deficiency virus* OR human immunodeficiency virus* OR aids OR acquired immunodeficiency syndrome* OR acquired immuno deficiency syndrome* OR acquired immunodeficiency syndrome*) AND (food security* OR food insecurity* OR hunger* OR food insufficient*) AND (viral load* OR viral rna* OR virus rna*).

Source type: Conference Papers & Proceedings, Dissertations & Theses, Scholarly Journals.

342 citations as of April 15th, 2015.

Ovid MEDLINE(R) In-Process & Other Non-Indexed Citations, Ovid MEDLINE(R) Daily, Ovid MEDLINE(R) and Ovid OLDMEDLINE(R) 1946 to Present

  1. 1.

    HIV Antigen/or HIV Infection/or HIV Seropositivity/or HIV/or HIV Antibody/.

  2. 2.

    Acquired Immunodeficiency Syndrome/bl, cf, di, me, mo, nu [Blood, Cerebrospinal Fluid, Diagnosis, Metabolism, Mortality, Nursing].

  3. 3.

    1 OR 2.

  4. 4.

    Food insecurity.mp.

  5. 5.

    Food insufficiency.mp.

  6. 6.

    Exp Malnutrition/or exp Hunger/or exp Food Supply/or exp Poverty/.

  7. 7.

    4 OR 5 OR 6.

  8. 8.

    Exp HIV/or exp Viral Load/.

  9. 9.

    Exp RNA, Viral/an, bl, du, de, im, ip, tu [Analysis, Blood, Diagnostic Use, Drug Effects, Immunology, Isolation & Purification, Therapeutic Use].

  10. 10.

    8 OR 9.

  11. 11.

    3 AND 7 AND 10.

270 Citations as of April 15th, 2015.

Embase classic + Embase

  1. 1.

    Hiv.mp. or exp Human immunodeficiency virus/.

  2. 2.

    Exp acquired immune deficiency syndrome/di, dm, dr, dt, ep, et, pc [Diagnosis, Disease Management, Drug Resistance, Drug Therapy, Epidemiology, Etiology, Prevention].

  3. 3.

    1 OR 2.

  4. 4.

    Exp malnutrition/or exp hunger/or exp food insecurity/or exp starvation/or exp socioeconomics/or exp nutritional status/or exp food intake/or food insufficiency.mp.

  5. 5.

    Viral load.mp. or exp virus load/.

  6. 6.

    Viral rna.mp. or exp virus RNA/.

  7. 7.

    5 OR 6.

  8. 8.

    3 AND 4 AND 7.

1198 citations as of April 15th, 2015.

Appendix B

Adapted version of Newcastle Ottawa Scale (NOS) for assessing cross sectional study quality (Adaptation was based on work by Herzog et al. [31] with slight modification)

Selection: (Maximum 4 stars)

  1. 1)

    Representativeness of the sample:

    1. a

      Truly representative of the average in the target population. * (all subjects or random sampling).

    2. b

      Somewhat representative of the average in the target population. * (non-random sampling).

    3. c

      Selected group of users.

    4. d

      No description of the sampling strategy.

  2. 2)

    Sample size:

    1. a.

      Justified and satisfactory. *

    2. b.

      Not justified.

  3. 3)

    Non-respondents:

    1. a.

      Comparability between respondents and non-respondents characteristics is established, and the response rate is satisfactory. *

    2. b.

      The comparability between respondents and non-respondents is unsatisfactory.

    3. c.

      No description of the response rate or the characteristics of the responders and the non-responders.

    4. d.

      No description of respondents and non-respondents regarding important confounders.

  4. 4)

    Ascertainment of the exposure (risk factor):

    1. a.

      Validated measurement tool or the tool is available or described. *

    2. b.

      No description of the measurement tool.

Comparability: (Maximum 2 stars)

  1. 1)

    Comparability of different exposure groups except that exposure variable on the basis of the design or analysis:

    1. a.

      The study controls for the most important factor through regression or matching.*

    2. b.

      The study control for any additional factor. *

Outcome: (Maximum 3 stars)

  1. 1)

    Assessment of outcome.

    1. a.

      Independent blind assessment. **

    2. b.

      Record linkage. **

    3. c.

      Self-report. *

    4. d.

      No description.

  2. 2)

    Statistical test:

    1. a.

      The statistical test used to analyze the data is clearly described and appropriate, and the measurement of the association is presented, including confidence intervals and the probability level (p value). *

    2. b.

      The statistical test is not appropriate, not described or incomplete.

Appendix C

See Table 3.

Table 3 Scoring details for each included studies
Full size table

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Aibibula, W., Cox, J., Hamelin, AM. et al. Association Between Food Insecurity and HIV Viral Suppression: A Systematic Review and Meta-Analysis. AIDS Behav 21, 754–765 (2017). https://doi.org/10.1007/s10461-016-1605-5

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  • DOI: https://doi.org/10.1007/s10461-016-1605-5

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