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Sarcopenia in people living with the Human Immunodeficiency Virus: a systematic review and meta-analysis

European Journal of Clinical Nutrition volume 74, pages 1009–1021 (2020)Cite this article

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Abstract

People living with HIV (PLHIV) experience greater loss of muscle mass and function than people without HIV. However, HIV is not routinely recognized as a sarcopenia risk factor outside of HIV literature. The purposes of this study were to establish the prevalence and predictors of sarcopenia among PLHIV, and to compare the prevalence of sarcopenia among PLHIV and people without HIV. A systematic literature search of the PubMed, Embase, Cinahl, and Scielo databases was performed following PRISMA and MOOSE guidelines. Identified articles were included if they evaluated sarcopenia among PLHIV using either the presence of low muscle mass only or low muscle mass in association with low muscle function. The pooled prevalence of sarcopenia among PLHIV and the odds ratio for sarcopenia in PLHIV compared with controls were calculated. From 13 studies and 2267 participants, the prevalence of sarcopenia among PLHIV was 24.1% (95% CI = 17.8–31.0%). PLHIV presented 6.1 greater odds (95% CI = 1.1–33.5) of sarcopenia compared with people without HIV, matched by age, sex, BMI, and ethnicity. Longer exposure to specific HIV drugs, tobacco and alcohol, lower education and employment rates, and greater HIV duration were associated with sarcopenia. In conclusion, PLHIV had a high prevalence of sarcopenia, related to both HIV and non-HIV risk factors. HIV should be considered a risk factor for sarcopenia in the general population. CRD42019131449.

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Fig. 1
Fig. 2
Fig. 3: Odds of having sarcopenia between people living with HIV (PLHIV) and people without HIV (control).
Fig. 4

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References

  1. Roubenoff R. Acquired immunodeficiency syndrome wasting, functional performance, and quality of life. Am J Manag Care. 2000;6:1003–16.

    CAS  PubMed  Google Scholar 

  2. Wanke CA, Silva M, Knox TA, Forrester J, Speigelman D, Gorbach SL. Weight loss and wasting remain common complications in individuals infected with human immunodeficiency virus in the era of highly active antiretroviral therapy. Clin Infect Dis. 2000;31:803–5.

    CAS  PubMed  Google Scholar 

  3. Dudgeon W, Phillips K, Carson J, Brewer R, Durstine J, Hand G. Counteracting muscle wasting in HIV-infected individuals. HIV Med. 2006;7:299–310.

    CAS  PubMed  Google Scholar 

  4. Grant PM, Kitch D, McComsey GA, Collier AC, Bartali B, Koletar SL, et al. Long-term body composition changes in antiretroviral-treated HIV-infected individuals. Aids. 2016;30:2805–13.

    CAS  PubMed  Google Scholar 

  5. Richert L, Dehail P, Mercié P, Dauchy F-A, Bruyand M, Greib C, et al. High frequency of poor locomotor performance in HIV-infected patients. AIDS. 2011;25:797–805.

    PubMed  Google Scholar 

  6. Wasserman P, Segal-Maurer S, Rubin DS. High prevalence of low skeletal muscle mass associated with male gender in midlife and older HIV-infected persons despite CD4 cell reconstitution and viral suppression. J Int Assoc Provid AIDS Care. 2014;13:145–52.

    PubMed  Google Scholar 

  7. Gomes-Neto M, Rodriguez I, Lédo AP, Vieira JPB, Brites C. Muscle strength and aerobic capacity in HIV-infected patients. JAIDS J Acquir Immune Defic Syndr. 2018;79:491–500.

    PubMed  Google Scholar 

  8. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyère O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48:16–31.

    PubMed  Google Scholar 

  9. Abdul Aziz SA, Mcstea M, Bashah NSA, Chong ML, Ponnampalavanar S, Omar SFS, et al. Assessment of sarcopenia in virally suppressed HIV-infected Asians receiving treatment. AIDS. 2018;32:1.

    Google Scholar 

  10. Echeverría P, Bonjoch A, Puig J, Estany C, Ornelas A, Clotet B, et al. High prevalence of sarcopenia in HIV-infected individuals. Biomed Res Int. 2018;2018:1–5.

    Google Scholar 

  11. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis. Age Ageing. 2010;39:412–23.

    PubMed  PubMed Central  Google Scholar 

  12. Kim TN, Park MS, Yang SJ, Yoo HJ, Kang HJ, Song W, et al. Prevalence and determinant factors of sarcopenia in patients with type 2 diabetes: the Korean Sarcopenic Obesity Study (KSOS). Diabetes Care. 2010;33:1497–9.

    PubMed  PubMed Central  Google Scholar 

  13. Chindapasirt J. Sarcopenia in cancer patients. Asian Pac J Cancer Prev. 2016;16:8075–7.

    Google Scholar 

  14. Wang T, Feng X, Zhou J, Gong H, Xia S, Wei Q, et al. Type 2 diabetes mellitus is associated with increased risks of sarcopenia and pre-sarcopenia in Chinese elderly. Sci Rep. 2016;6:38937.

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Dovjak P. Sarcopenia in cases of chronic and acute illness. Z Gerontol Geriatr. 2016;49:100–6.

    PubMed  Google Scholar 

  16. Liu P, Hao Q, Hai S, Wang H, Cao L, Dong B. Sarcopenia as a predictor of all-cause mortality among community-dwelling older people: a systematic review and meta-analysis. Maturitas. 2017;103:16–22.

    PubMed  Google Scholar 

  17. Sousa AS, Guerra RS, Fonseca I, Pichel F, Ferreira S, Amaral TF. Financial impact of sarcopenia on hospitalization costs. Eur J Clin Nutr. 2016;70:1046–51.

    CAS  PubMed  Google Scholar 

  18. Anker SD, Morley JE, von Haehling S. Welcome to the ICD-10 code for sarcopenia. J Cachexia Sarcopenia Muscle. 2016;7:512–4.

    PubMed  PubMed Central  Google Scholar 

  19. Muscaritoli M, Anker SD, Argilés J, Aversa Z, Bauer JM, Biolo G, et al. Consensus definition of sarcopenia, cachexia and pre-cachexia: Joint document elaborated by Special Interest Groups (SIG) ‘cachexia-anorexia in chronic wasting diseases’ and ‘nutrition in geriatrics’. Clin Nutr. 2010;29:154–9.

    CAS  PubMed  Google Scholar 

  20. Fielding RA, Vellas B, Evans WJ, Bhasin S, Morley JE, Newman AB, et al. Sarcopenia: an Undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia. J Am Med Dir Assoc. 2011;12:249–56.

    PubMed  Google Scholar 

  21. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000;283:2008–12.

    CAS  PubMed  Google Scholar 

  22. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.

    PubMed  PubMed Central  Google Scholar 

  23. Dawson-Hughes B, Bischoff-Ferrari H. Considerations concerning the definition of sarcopenia. Osteoporos Int. 2016;27:3139–44.

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Baumgartner RN, Koehler KM, Gallagher D, Romero L, Heymsfield SB, Ross RR, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–63.

    CAS  PubMed  Google Scholar 

  25. Janssen I, Baumgartner RN, Ross R, Rosenberg IH, Roubenoff R. Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women. Am J Epidemiol. 2004;159:413–21.

    PubMed  Google Scholar 

  26. Oliveira VH, Wiechmann SL, Narciso AM, Webel AR, Deminice R. Muscle strength is impaired in men but not in women living with HIV taking antiretroviral therapy. Antivir Ther. 2017;23:11–19.

    Google Scholar 

  27. Bernard C, Dabis F, de Rekeneire N. Physical function, grip strength and frailty in people living with HIV in sub-Saharan Africa: systematic review. Trop Med Int Heal. 2017;22:516–25.

    Google Scholar 

  28. Loney PL, Chambers LW, Bennett KJ, Roberts JG, Stratford PW. Critical appraisal of the health research literature: prevalence or incidence of a health problem. Chronic Dis Can. 1998;19:170–6.

    CAS  PubMed  Google Scholar 

  29. Furuya-Kanamori L, Barendregt JJ, Doi SAR. A new improved graphical and quantitative method for detecting bias in meta-analysis. Int J Evid Based Health. 2018;16:195–203.

    Google Scholar 

  30. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses Testing for heterogeneity. BMJ. 2003;327:557–60.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67:974–8.

    PubMed  Google Scholar 

  32. Buehring B, Kirchner E, Sun Z, Calabrese L. The frequency of low muscle mass and its overlap with low bone mineral density and lipodistrophy in individuals with HIV—a pilot study using DXA total body composition analysis. J Clin Densitom. 2012;15:224–32.

    PubMed  Google Scholar 

  33. Dutta D, Sharma M, Bansal R, Sharma N, Garga UC, Anand A, et al. Low skeletal mass is an important predictor of osteoporosis in HIV infected men in India. Endokrynol Pol. 2017;66:469–72.

    Google Scholar 

  34. Dutta D, Garga U, Gadpayle A, Bansal R, Anand A, Gaurav K, et al. Occurrence and predictors of osteoporosis and impact of body composition alterations on bone mineral health in asymptomatic pre-menopausal women with HIV infection. Indian J Med Res. 2018;147:484.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Hawkins KL, Zhang L, Ng DK, Althoff KN, Palella FJ, Kingsley LA, et al. Abdominal obesity, sarcopenia, and osteoporosis are associated with frailty in men living with and without. Hiv Aids. 2018;32:1257–66.

    Google Scholar 

  36. Kruger HS, Havemann-Nel L, Ravyse C, Moss SJ, Tieland M. Physical activity energy expenditure and sarcopenia in black South African urban women. Orig Res J Phys Act Heal. 2016;13:296–302.

    Google Scholar 

  37. Mialich MS, dos Santos AP, da Silva BR, de Paula FJA, Jordão AA, Navarro AM. Relationship between adiposity indices, lipodystrophy, and sarcopenia in HIV-positive individuals with and without lipodystrophy. J Clin Densitom. 2017;20:73–81.

    PubMed  Google Scholar 

  38. Pinto Neto LF, da S, Sales MC, Scaramussa ES, da Paz CJC, Morelato RL. Human immunodeficiency virus infection and its association with sarcopenia. Braz J Infect Dis. 2016;20:99–102.

    PubMed  Google Scholar 

  39. Serrano-Villar S, Moreno S, Fuentes-Ferrer M, Sánchez-Marcos C, Ávila M, Sainz T, et al. The CD4: CD8 ratio is associated with markers of age-associated disease in virally suppressed HIV-infected patients with immunological recovery. HIV Med. 2014;15:40–49.

    CAS  PubMed  Google Scholar 

  40. Erlandson KM, Allshouse AA, Jankowski CM, MaWhinney S, Kohrt WM, Campbell TB. Functional impairment is associated with low bone and muscle mass among persons aging with HIV infection. JAIDS J Acquir Immune Defic Syndr. 2013;63:209–15.

    PubMed  Google Scholar 

  41. Debroy P, Lake JE, Malagoli A, Guaraldi G. Relationship between grip strength and nonalcoholic fatty liver disease in men living with HIV referred to a metabolic clinic. J frailty aging. 2019;8:150–3.

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Janssen IAN, Heymsfield SB, Baumgartner RN, Ross R, Richard N. Estimation of skeletal muscle mass by bioelectrical impedance analysis. J Appl Physiol. 2000;89:465–71.

    CAS  PubMed  Google Scholar 

  43. Shafiee G, Keshtkar A, Soltani A, Ahadi Z, Larijani B, Heshmat R. Prevalence of sarcopenia in the world: a systematic review and meta- analysis of general population studies. J Diabetes Metab Disord. 2017;16:21.

    PubMed  PubMed Central  Google Scholar 

  44. Diz JBM, Leopoldino AAO, Moreira B, de S, Henschke N, Dias RC, et al. Prevalence of sarcopenia in older Brazilians: a systematic review and meta-analysis. Geriatr Gerontol Int. 2017;17:5–16.

    PubMed  Google Scholar 

  45. Smith RL, de Boer R, Brul S, Budovskaya Y, van der Spek H. Premature and accelerated aging: HIV or HAART? Front Genet. 2013;3:1–10.

    Google Scholar 

  46. Pathai S, Bajillan H, Landay AL, High KP. A Is HIV a model of accelerated or accentuated aging?. J Gerontol Ser A Biol Sci Med Sci. 2014;69:833–42.

    Google Scholar 

  47. Deeks SG. HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med. 2011;62:141–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Capeau J. Premature aging and premature age-related comorbidities in HIV-infected patients: facts and hypotheses. Clin Infect Dis. 2011;53:1127–9.

    PubMed  Google Scholar 

  49. Murata Y, Kadoya Y, Yamada S, Sanke T. Sarcopenia in elderly patients with type 2 diabetes mellitus: prevalence and related clinical factors. Diabetol Int. 2018;9:136–42.

    PubMed  Google Scholar 

  50. Pereira RA, Cordeiro AC, Avesani CM, Carrero JJ, Lindholm B, Amparo FC, et al. Sarcopenia in chronic kidney disease on conservative therapy: prevalence and association with mortality. Nephrol Dial Transpl. 2015;30:1718–25.

    CAS  Google Scholar 

  51. Jones SE, Maddocks M, Kon SSC, Canavan JL, Nolan CM, Clark AL, et al. Sarcopenia in COPD: prevalence, clinical correlates and response to pulmonary rehabilitation. Thorax. 2015;70:213–8.

    PubMed  Google Scholar 

  52. Du K, Goates S, Arensberg MB, Pereira S, Gaillard T. Prevalence of sarcopenia and sarcopenic obesity vary with race/ethnicity and advancing age. Divers Equal Heal Care. 2018;15:175–83.

    Google Scholar 

  53. Kim G, Kang SH, Kim MY, Baik SK. Prognostic value of sarcopenia in patients with liver cirrhosis: a systematic review and meta-analysis. PLoS ONE. 2017;12:e0186990.

    PubMed  PubMed Central  Google Scholar 

  54. Ryom L, Lundgren JD, De Wit S, Kovari H, Reiss P, Law M, et al. Use of antiretroviral therapy and risk of end-stage liver disease and hepatocellular carcinoma in HIV-positive persons. AIDS. 2016;30:1731–43.

    CAS  PubMed  Google Scholar 

  55. Yarasheski KE, Scherzer R, Kotier DP, Dobs AS, Tien PC, Lewis CE, et al. Age-related skeletal muscle decline is similar in HIV-infected and uninfected individuals. J Gerontol Med Sci. 2011;66 A:332–40.

    Google Scholar 

  56. Grinspoon S, Corcoran C, Miller K, Biller BM, Askari H, Wang E, et al. Body composition and endocrine function in women with acquired immunodeficiency syndrome wasting. J Clin Endocrinol Metab. 1997;82:1332–7.

    CAS  PubMed  Google Scholar 

  57. Mulligan K, Tai VW, Schambelan M. Cross-sectional and longitudinal evaluation of body composition in men with HIV infection. J Acquir Immune Defic Syndr Hum Retrovirology. 1997;15:43–48.

    CAS  Google Scholar 

  58. Silva AM, Shen W, Heo M, Gallagher D, Wang Z, Sardinha LB, et al. Ethnicity-related skeletal muscle differences across the lifespan. Am J Hum Biol. 2010;22:76–82.

    PubMed  PubMed Central  Google Scholar 

  59. Legarth R, Omland LH, Kronborg G, Larsen CS, Pedersen C, Pedersen G, et al. Employment status in persons with and without HIV infection in Denmark. AIDS. 2014;28:1489–98.

    PubMed  Google Scholar 

  60. Thirumurthy H, Chamie G, Jain V, Kabami J, Kwarisiima D, Clark TD, et al. Improved employment and education outcomes in households of HIV-infected adults with high CD4 cell counts. AIDS. 2013;27:627–34.

    PubMed  Google Scholar 

  61. Zhang Y, Wilson TE, Adedimeji A, Merenstein D, Milam J, Cohen J, et al. The impact of substance use on ADherence to Antiretroviral Therapy Among HIV-infected women in the United States. AIDS Behav. 2018;22:896–908.

    PubMed  PubMed Central  Google Scholar 

  62. Gurung S, Ventuneac A, Cain D, Mirzayi C, Ferraris C, Rendina HJ, et al. Alcohol and substance use diagnoses among HIV-positive patients receiving care in NYC clinic settings. Drug Alcohol Depend. 2017;180:62–67.

    PubMed  PubMed Central  Google Scholar 

  63. Ahmad AN, Ahmad SN, Ahmad N. HIV infection and bone abnormalities. Open Orthop J. 2017;11:777–84.

    PubMed  PubMed Central  Google Scholar 

  64. Grinspoon S, Mulligan K. Weight loss and wasting in patients infected with human immunodeficiency virus. Clin Infect Dis. 2003;36:S69–S78.

    PubMed  Google Scholar 

  65. Filteau S, PrayGod G, Woodd SL, Friis H, Heimburger DC, Koethe JR, et al. Nutritional status is the major factor affecting grip strength of African HIV patients before and during antiretroviral treatment. Trop Med Int Heal. 2017;22:1302–13.

    CAS  Google Scholar 

  66. UNAIDS. UNAIDS data 2019. UNAIDS: Geneva, 2019.

  67. Naing L, Winn T, Rusli BN. Practical issues in calculating the sample size for prevalence. Stud Arch Orofac Sci. 2006;1:9–14.

    Google Scholar 

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Acknowledgements

VHFO was granted a Brazilian scholarship for a research internship at Dr. Webel’s (ARW) laboratory in Cleveland, USA (bolsista da Capes/Programa de Doutorado Sanduíche no Exterior/Processo no [88881.132132/2016-01]).

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Authors and Affiliations

  1. Department of Physical Education, State University of Londrina, Londrina, Paraná, Brazil

    Vitor H. F. Oliveira, Ana L. Borsari & Rafael Deminice

  2. Frances Payne Bolton School of Nursing, Case Western Reserve University, Cleveland, OH, USA

    Allison R. Webel

  3. University of Colorado, Anschutz Medical Campus, Aurora, CO, USA

    Kristine M. Erlandson

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  1. Vitor H. F. Oliveira
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Oliveira, V.H.F., Borsari, A.L., Webel, A.R. et al. Sarcopenia in people living with the Human Immunodeficiency Virus: a systematic review and meta-analysis. Eur J Clin Nutr 74, 1009–1021 (2020). https://doi.org/10.1038/s41430-020-0637-0

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