Journal of Neuroimmune Pharmacology

, Volume 8, Issue 5, pp 1114–1122

Identifying Risk Factors for HIV-Associated Neurocognitive Disorders Using the International HIV Dementia Scale

  • Sara Cross
  • Nur Önen
  • Amber Gase
  • Edgar Turner Overton
  • Beau M. Ances
BRIEF REPORT

Abstract

HIV-associated neurocognitive disorders (HAND) persist despite great advancements in combination antiretroviral therapy (cART). The gold standard for diagnosing cognitive impairment consists of a time-consuming neuropsychological battery of tests given by a trained neuropsychologist, however in the outpatient HIV clinic this is not feasible. The International HIV Dementia Scale (IHDS) was developed to help identify individuals with cognitive impairment in the outpatient setting. The IHDS is moderately sensitive for detecting more symptomatic forms of HAND but sensitivity has been shown to be poor in mild impairment. The IHDS has not been evaluated in developed countries in large cohort populations. We conducted a prospective cross-sectional study of only HIV+ individuals in an urban clinic and evaluated the prevalence of HAND and associated risk factors for cognitive impairment using the IHDS. A total of 507 HIV+ individuals participated in the study of which the majority were male (65 %) and African American (68 %); and 41 % had cognitive impairment. On multivariate analysis, African American race (p = 2.21), older age (p = 1.03), high school education or less (p = 2.03) and depression (p = 1.05) were associated with cognitive impairment. The high prevalence of HAND in this group suggests that more severe forms of HAND persist despite cART. Identified risk factors were non-HIV-related and suggest that environmental and sociodemographic factors have a significant impact on cognitive functioning and should be given more attention. The IHDS should be further evaluated in large cohort HIV+ and HIV- populations in the United States, as there remains a significant need to identify an effective brief screening tool for cognitive impairment.

Keywords

HIV International HIV Dementia Scale (IHDS) HIV associated neurocognitive disorders (HAND) 

References

  1. An Q, Prejean J, Hall HI (2012) Racial disparity in U.S. diagnoses of acquired immune deficiency syndrome, 2000–2009. Am J Prev Med 43:461–466. doi:10.1016/j.amepre.2012.07.040 PubMedCrossRefGoogle Scholar
  2. Ances BM, Ellis RJ (2007) Dementia and neurocognitive disorders due to HIV-1 infection. Semin Neurol 27:86–92. doi:10.1055/s-2006-956759 PubMedCrossRefGoogle Scholar
  3. Andel R, Vigen C, Mack WJ, Clark LJ, Gatz M (2006) The effect of education and occupational complexity on rate of cognitive decline in Alzheimer’s patients. J Int Neuropsychol Soc 12:147–152. doi:10.1017/S1355617706060206 PubMedGoogle Scholar
  4. Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslen M, Grant I, Heaton RK, Joseph J, Marder K, Marra CM, McArthur JC, Nunn M, Price RW, Pulliam L, Robertson KR, Sacktor N, Valcour V, Wojna VE (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799. doi:10.1212/01.WNL.0000287431.88658.8b PubMedCrossRefGoogle Scholar
  5. Basso MR, Bornstein RA (2000) Estimated premorbid intelligence mediates neurobehavioral change in individuals infected with HIV across 12 months. J Clin Exp Neuropsychol 22:208–218. doi:10.1076/1380-3395(200004)22:2;1-1 PubMedCrossRefGoogle Scholar
  6. Becker JT, Dew MA, Aizenstein HJ, Lopez OL, Morrow L, Saxton J (2011) Concurrent validity of a computer-based cognitive screening tool for use in adults with HIV disease. AIDS Patient Care STDS 25:351–357. doi:10.1089/apc.2011.0051 PubMedCrossRefPubMedCentralGoogle Scholar
  7. Centers for Disease Control and Prevention (2004) Indicators for chronic disease surveillance. MMWR 53:19–27Google Scholar
  8. Cherner M, Letendre S, Heaton RK, Durelle J, Marquie-Beck J, Gragg B, Grant I, HIV Neurobehavioral Research Center Group (2005) Hepatitis C augments cognitive deficits associated with HIV infection and methamphetamine. Neurology 64:1343–1347PubMedCrossRefGoogle Scholar
  9. Cysique LA, Deutsch R, Atkinson JH, Young C, Marcotte TD, Dawson L, Grant I, Heaton RK, HNRC Group (2007) Incident major depression does not affect neuropsychological functioning in HIV-infected men. J Int Neuropsychol Soc 1:1–11. doi:10.1017/S1355617707070026 Google Scholar
  10. Cysique LA, Vaida F, Letendre S, Gibson S, Cherner M, Woods SP, McCutchan JA, Heaton RK, Ellis RJ (2009) Dynamics of cognitive change in impaired HIV-positive patients initiating antiretroviral therapy. Neurology 73:342–348. doi:10.1212/WNL.0b013e3181ab2b3b PubMedCrossRefPubMedCentralGoogle Scholar
  11. Ellis RJ, Badiee J, Vaida F, Letendre S, Heaton RK, Clifford D, Collier AC, Gelman B, McArthur J, Morgello S, McCutchan JA, Grant I, CHARTER Group (2011) CD4 nadir is a predictor of HIV neurocognitive impairment in the era of combination antiretroviral therapy. AIDS 25:1747–1751. doi:10.1097/QAD.0b013e32834a40cd PubMedCrossRefGoogle Scholar
  12. Fabbiani M, Ciccarelli N, Tana M, Farina S, Baldonero E, Di Cristo V, Colafigli M, Tamburrini E, Cauda R, Silveri MC, Grima P, Di Giambenedetto S (2013) Cardiovascular risk factors and carotid intima-media thickness are associated with lower cognitive performance in HIV-infected patients. HIV Med 14:136–144. doi:10.1111/j.1468-1293.2012.01044 PubMedCrossRefGoogle Scholar
  13. Ford ES (2013) Trends in predicted 10-year risk of coronary heart disease and cardiovascular disease among U.S. adults from 1999 to 2010. J Am Coll Cardiol 61:2249–2252. doi:10.1016/j.jacc.2013.03.023 PubMedCrossRefGoogle Scholar
  14. Gelman BB, Lisinicchia JG, Morgello S, Masliah E, Commins D, Achim CL, Fox HS, Kolson DL, Grant I, Singer E, Yiannoutsos CT, Sherman S, Gensler G, Moore DJ, Chen T, Soukup VM (2013) Neurovirological correlation with HIV-associated neurocognitive disorders and encephalitis in a HAART-era cohort. J Acquir Immune Defic Syndr 62:487–495. doi:10.1097/QAI.0b013e31827f1bdb PubMedCrossRefGoogle Scholar
  15. Haddow LJ, Floyd S, Copas A, Gilson RJ (2013) A systematic review of the screening accuracy of the HIV Dementia Scale and International HIV Dementia Scale. PLoS ONE 8:e61826. doi:10.1371/journal.pone.0061826 PubMedCrossRefPubMedCentralGoogle Scholar
  16. Hawkins LA, Kilian S, Firek A, Kashner TM, Firek CJ, Silvet H (2012) Cognitive impairment and medication adherence in outpatients with heart failure. Heart Lung 41:572–582. doi:10.1016/j.hrtlng.2012.06.001 PubMedCrossRefGoogle Scholar
  17. Heaton RK, Velin RA, McCutchan JA, Gulevich SJ, Atkinson JH, Wallace MR, Godfrey HP, Kirson DA, Grant I (1994) Neuropsychological impairment in human immunodeficiency virus-infection: implications for employment. HNRC Group. HIV Neurobehavioral Research Center. Psychosom Med 56:8–17PubMedGoogle Scholar
  18. Heaton RK, Clifford DB, Franklin DR, Woods SB, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, CHARTER Group (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy. Neurology 75:2087–2096. doi:10.1212/WNL.0b013e318200d727 PubMedCrossRefPubMedCentralGoogle Scholar
  19. Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL et al (2011) HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: differences in rates, nature and predictors. J Neurovirol 17:3–16. doi:10.1007/s13365-010-0006-1 PubMedCrossRefPubMedCentralGoogle Scholar
  20. Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, Thrasher D, Goetz MB, Stefaniak M (2002) Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology 59:1944–1950PubMedCrossRefPubMedCentralGoogle Scholar
  21. Hinkin CH, Hardy DJ, Mason KI, Castellon SA, Durvasula RS, Lam MN, Stefaniak M (2004) Medication adherence in HIV-infected adults: effect of patient age, cognitive status, and substance abuse. AIDS 18(Suppl 1):S19–S25. doi:10.1097/01.aids.0000125980.64033.f PubMedPubMedCentralGoogle Scholar
  22. Hosmer DW, Hosmer T, Le Cessie S, Lemeshow S (1997) A comparison of goodness-of-fit tests for the logistic regression model. Stat Med 16:965–980. doi:10.1002/(SICI)1097-0258 PubMedCrossRefGoogle Scholar
  23. Jorm AF, Jolley D (1998) The incidence of dementia: a meta-analysis. Neurology 51:728–733PubMedCrossRefGoogle Scholar
  24. Joska JA, Westgarth-Taylor J, Hoare J, Thomas KG, Paul R, Myer L, Stein DJ (2011) Validity of the International HIV Dementia Scale in South Africa. AIDS Patient Care STDs 25:95–101. doi:10.1089/apc.2010.0292 PubMedCrossRefGoogle Scholar
  25. Kalechstein AD, Newton TF, van Gorp WG (2003) Neurocognitive functioning is associated with employment status: a quantitative review. J Clin Exp Neuropsychol 25:1186–1191. doi:10.1076/jcem.25.8.1186.16723 PubMedCrossRefGoogle Scholar
  26. Katz MJ, Lipton RB, Hall CB, Zimmerman ME, Sanders AE, Verghese J, Dickson DW, Derby CA (2012) Age-specific and sex-specific prevalence and incidence of mild cognitive impairment, dementia and Alzheimer dementia in blacks and whites: a report from the Einstein Aging Study. Alzheimer Dis Assoc Disord 26:335–343. doi:10.1097/WAD.0b013e31823dbcfc PubMedCrossRefPubMedCentralGoogle Scholar
  27. Kissel EC, Pukay-Martin ND, Borenstein RA (2005) The relationship between age and cognitive function in HIV-infected men. J Neuropsychiatry Clin Neurosci 17:180–184. doi:10.1176/appi.neuropsych.17.2.180 PubMedCrossRefGoogle Scholar
  28. Kroenke K, Spitzer RL, Williams JB (2001) The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med 16:606–613. doi:10.1046/j.1525-1497.2001.016009606.x, doi:10.1046%2Fj.1525-1497.2001.016009606.x#_blank PubMedCrossRefPubMedCentralGoogle Scholar
  29. Lescure FX, Omland LH, Engsig FN, Roed C, Gerstoft J, Pialoux G, Kronborg G, Larsen CS, Obel N (2011) Incidence and impact on mortality of severe neurocognitive disorders in persons with and without HIV infection: a Danish nationwide cohort study. Clin Infect Dis 52:235–243. doi:10.1093/cid/ciq041 PubMedCrossRefGoogle Scholar
  30. Letendre SL, Ellis RJ, Ances BM, McCutchan JA (2010) Neurologic complications of HIV disease and their treatment. Top HIV Med 18:45–55PubMedGoogle Scholar
  31. McCutchan JA, Marquie-Beck JA, Fitzsimons CA, Letendre SL, Ellis RJ, Heaton RK, Wolfson T, Rosario D, Alexander TJ, Marra C, Ances BM, Grant I, CHARTER Group (2012) Role of obesity, metabolic variables, and diabetes in HIV-associated neurocognitive disorder. Neurology 78:485–492. doi:10.1212/WNL.0b013e3182478d64 PubMedCrossRefPubMedCentralGoogle Scholar
  32. Morgan EE, Wood SP, Smith C, Weber E, Scott JC, Grant I, HIV Neurobehavioral Research Program (HNRP) Group (2012) Lower cognitive reserve among individuals with syndromic HIV-associated neurocognitive disorders (HAND). AIDS Behav 16:2279–2285. doi:10.1007/s10461-012-0229-7 PubMedCrossRefPubMedCentralGoogle Scholar
  33. Muniyandi K, Venkatesan J, Arutselvi T, Jayaseelan V (2012) Study to assess the prevalence, nature and extent of cognitive impairment in people living with AIDS. Indian J Psychiatry 54:149–153. doi:10.4103/0019-5545.99534 PubMedCrossRefPubMedCentralGoogle Scholar
  34. Needle R, Fisher DG, Weatherby N, Chitwood D, Brown B, Cesari H, Booth R, Williams ML, Watters J, Anderson M, Braunstein M (1995) Reliability of self-reported HIV risk behaviors of drug users. Psychol Addict Behav 9:242–250. doi:10.1037/0893-164X.9.4.242 CrossRefGoogle Scholar
  35. Njamnshi AK, Bissek AC, Ongolo-Zogo P, Tabah EN, Lekoubou AZ, Yepnjio FN, Fonsah JY, Kuate CT, Angwafor SA, Dema F, Njamnshi DM, Kouanfack C, Djientcheu Vde P, Muna WF, Kanmogne GD (2009) Risk factors for HIV-associated neurocognitive disorders (HAND) in Sub-Saharan Africa: the case of Yaoundé-Cameroon. J Neurol Sci 285:149–153. doi:10.1016/j.jns.2009.06.043 PubMedCrossRefGoogle Scholar
  36. Overton ET, Kauwe JS, Paul R, Tashima K, Tate DF, Patel P, Carpenter CC, Patty D, Brooks JT, Clifford DB (2011) Performances on the Cog State and standard neuropsychological batteries among HIV patients without dementia. AIDS Behav 15:1902–1909. doi:10.1007/s10461-011-0033-9 PubMedCrossRefPubMedCentralGoogle Scholar
  37. Overton ET, Azad TD, Parker N, Demarco Shaw D, Frain J, Spitz T, Westerhaus E, Paul R, Clifford DB, Ances BM (2013) The Alzheimer’s Disease-8 and Montreal Cognitive Assessment as screening tools for neurocognitive impairment in HIV-infected persons. J Neurovirol 19:109–116. doi:10.1007/s13365-012-0147-5 PubMedCrossRefGoogle Scholar
  38. Richardson MA, Morgan EE, Vielhauer MJ, Cuevas CA, Buondonno LM, Keane TM (2005) Utility of the HIV dementia scale in assessing risk for significant HIV-related cognitive-motor deficits in a high-risk urban adult sample. AIDS Care 17:1013–1021. doi:10.1080/09540120500100858 PubMedCrossRefGoogle Scholar
  39. Robertson KR, Smurzinski M, Parsons TD, Wu K, Bosch RJ, Wu J, McArthur JC, Collier AC, Evans SR, Ellis RJ (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21:1915–1921. doi:10.1097/QAD.0b013e32828e4e27 PubMedCrossRefGoogle Scholar
  40. Robinson-Papp J, Elliott KJ, Simpson DM (2009) HIV-related neurocognitive impairment in the HAART era. Curr HIV/AIDS Rep 6:146–152. doi:10.1007/s11904-009-0020-1 PubMedCrossRefGoogle Scholar
  41. Sacktor NC, Wong M, Nakasujja N, Skolasky RL, Selnes OA, Musisi S, Robertson K, McArthur JC, Ronald A, Katabira E (2005) The International HIV Dementia scale: a new rapid screening test for HIV dementia. AIDS 19:1367–1374PubMedGoogle Scholar
  42. Singh D, Sunpath H, John S, Eastham L, Gouden R (2008) The utility of a rapid screening tool for depression and HIV dementia amongst patients with low CD4 counts—a preliminary report. Afr J Psychiatry 11:282–286Google Scholar
  43. Stern R, Silva S, Chaisson N, Evans D (1996) Influence of cognitive reserve on neuropsychological functioning in asymptomatic human immunodeficiency virus-1 infection. Arch Neurol 53:148–153. doi:10.1001/archneur.1996.00550020052015 PubMedCrossRefGoogle Scholar
  44. Stern Y, McDermott MP, Albert S, Palumbo D, Selnes OA, McArthur J, Sacktor N, Schifitto G, Kieburtz K, Epstein L, Marder KS, Dana Consortium on the Therapy of HIV- Dementia and Related Cognitive Disorders (2001) Factors associated with incident human immunodeficiency virus-dementia. Arch Neurol 58:473–479. doi:10.1001/archneur.58.3.473 PubMedCrossRefGoogle Scholar
  45. The Mind Exchange Working Group (2013) Assessment, diagnosis and treatment of HIV-associated neurocognitive disorder: a consensus report of the Mind Exchange Program. Clin Infect Dis 56:1004–1017. doi:10.1093/cid/cis975 CrossRefGoogle Scholar
  46. Tozzi V, Balestra P, Galgani S, Murri R, Bellagamba R, Narciso P, Antinori A, Giulianelli M, Tosi G, Costa M, Sampaolesi A, Fantoni M, Noto P, Ippolito G, Wu AW (2003) Neurocognitive performance and quality of life in patients with HIV infection. AIDS Res Hum Retrovir 19:643–652. doi:10.1089/088922203322280856 PubMedCrossRefGoogle Scholar
  47. United States Department of Agriculture and United States Department of Health and Human Services (2005) Dietary guidelines for Americans. Chapter 9. Alcoholic Beverages. US Government Printing Office, Washington DC, pp 43–46Google Scholar
  48. Unverzagt FW, McClure LA, Wadley VG, Jenny NS, Go RC, Cushman M, Kissela BM, Kelley BJ, Kennedy R, Moy CS, Howard V, Howard G (2011) Vascular risk factors and cognitive impairment in a stroke-free cohort. Neurology 77:1729–1736. doi:10.1212/WNL.0b013e318236ef23 PubMedCrossRefPubMedCentralGoogle Scholar
  49. Valcour VG (2011) Evaluating cognitive impairment in the clinical setting: practical screening and assessment tools. Top Antivir Med 19:175–180PubMedGoogle Scholar
  50. Valcour V, Shikuma C, Shiramizu B, Watters M, Poff P, Selnes O, Holck P, Grove J, Sacktor N (2004) Higher frequency of dementia in older HIV-1 individuals: the Hawaii Aging with HIV-1 Cohort. Neurology 63:822–827PubMedCrossRefPubMedCentralGoogle Scholar
  51. Valcour V, Paul R, Neuhaus J, Shikuma C (2011) The effects of age and HIV on neuropsychological performance. J Int Neuropsychol Soc 17:190–195. doi:10.1017/S1355617710001438 PubMedCrossRefPubMedCentralGoogle Scholar
  52. van Gorp WG, Baerwald JP, Ferrando SJ, McElhiney MC, Rabkin JG (1999) The relationship between employment and neuropsychological impairment in HIV infection. J Int Neuropsychol Soc 5:534–539PubMedGoogle Scholar
  53. Zipursky AR, Gogolishvilli D, Rueda S, Brunetta J, Carvalhal A, McCombe JA, Gill MJ, Rachlis A, Rosenes R, Arbess G, Marcotte T, Rourke SB (2013) Evaluation of brief screening tools for neurocognitive impairment in HIV/AIDS: a systematic review of the literature. AIDS 27:2385–2401. doi:10.1097/QAD.0b013e328363bf56 PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Sara Cross
    • 1
  • Nur Önen
    • 1
  • Amber Gase
    • 1
  • Edgar Turner Overton
    • 2
  • Beau M. Ances
    • 3
    • 4
    • 5
  1. 1.Department of MedicineWashington University School of MedicineSt. LouisUSA
  2. 2.Department of MedicineUniversity of Alabama School of MedicineBirminghamUSA
  3. 3.Department of NeurologyWashington University School of MedicineSaint LouisUSA
  4. 4.Hope Center for Neurological DisordersWashington University School of MedicineSt. LouisUSA
  5. 5.Department of Bioengineering and RadiologyWashington University School of MedicineSt. LouisUSA

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