Abstract
HIV-associated neurocognitive disorders (HAND) occur in approximately 50% of HIV-infected individuals, yet available diagnostic criteria yield varying prevalence rates. This study examined the frequency, reliability, and sensitivity to everyday functioning problems of three HAND diagnostic criteria (DSM-5, Frascati, Gisslén). Participants included 361 adults with HIV disease and 199 seronegative adults. Neurocognitive status as defined by each of the three diagnostic systems was determined via a comprehensive neuropsychological battery. Everyday functioning was evaluated through self-report and clinician ratings. Results of logistic regressions revealed an association of HIV serostatus with Frascati-defined neurocognitive impairment (p = .027, OR = 1.7[1.1, 2.7]), but not DSM-5 or Gisslén-defined criteria (ps > .05). Frascati and DSM-5 criteria demonstrated agreement on 71% of observations, Frascati and Gisslén showed agreement on 80%, and DSM-5 and Gisslén criteria showed agreement on 46%, though reliability across the three criteria was poor. Only Frascati-defined neurocognitive impairment significantly predicted everyday functioning problems (p = .002, OR = 2.3[1.4, 3.8]). However, when both neurocognitive and complaint criteria were considered, the DSM-5 guidelines demonstrated significant relationships to everyday functioning, serostatus, and also increased reliability overtime compared to neurocognitive criteria alone (all ps < .05). A subset (n = 118) of the HIV+ group was assessed again after 14.0 (2.2) months. DSM-5 criteria evidenced significantly higher rates of incident neurocognitive disorder compared to both Frascati (p = .003) and Gisslén (p = .021) guidelines, while there were fewer remitting neurocognitive disorder diagnoses when Gisslén criteria were applied to the study sample compared to Frascati (p = .04). Future studies should aim to identify gold standard biological markers (e.g., neuropathology) and clinical outcomes associated with specific diagnostic criteria.
Similar content being viewed by others
References
Al-Khindi T, Zakzanis KK, Van Gorp WG (2011) Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. JINS 17(6):9–56
American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders, 5th edn. Author, Washington DC
Antinori A, Arendt G, Becker JT, Brew BJ, Byrd DA, Cherner M, Clifford DB, Cinque P, Epstein LG, Goodkin K, Gisslén 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
Army Individual Test Battery (1944) Manual of directions and scoring. War Department, Adjutant General’s Office, Washington, DC
Chan P, Brew BJ (2014) HIV associated neurocognitive disorders in the modern antiviral treatment era: prevalence, characteristics, biomarkers, and effects of treatment. Current HIV/AIDS Reports 1(3):317–324
Culbertson WC, Zillmer EA (1999) The tower of London, Drexel University, research version: examiner’s manual. Multi-Health Systems, North Tonawanda
Delis DC, Kramer JH, Kaplan E, Ober BA (2000) The California verbal learning test, 2nd edn. The Psychological Corporation, San Antonio
Gandhi NS, Skolasky RL, Peters KB, Moxley RT IV, Creighton J, Roosa HV et al (2011) A comparison of performance-based measures of function in HIV-associated neurocognitive disorders. J Neurovirol 17(2):159–165
Gisslén M, Price RW, Nilsson S (2011) The definition of HIV-associated neurocognitive disorders: are we overestimating the real prevalence? BMC Infect Dis 11:356
Grant I, Franklin DR, Deutsch R, Woods SP, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Collier AC, Marra CM, Clifford DB, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Smith DM, Heaton RK, CHARTER Group (2014) Asymptomatic HIV-associated neurocognitive impairment increases risk for symptomatic decline. Neurology 82:2055–2062. doi:10.1212/WNL.0000000000000492
Haziot MEJ, Junior SPB, Vidal JE, Oliveira FTM, Oliveira ACP (2015) Neuroimaging of HIV-associated neurocognitive disorders. Dement Neuropsychologia 9(4). doi:10.1590/1980-57642015DN94000380
Heaton RK, Marcotte TD, Mindt MR, Sadek J, Moore DJ, Bentley H, McCutchan JA, Reicks C, Grant I, HNRC Group (2004a) The impact of HIV-associated neuropsychological impairment on everyday functioning. J Int Neuropsychol Soc 10:317–331. doi:10.1017/S1355617704102130
Heaton RK, Miller SW, Taylor MJ, Grant I (2004b) Revised comprehensive norms for an expanded Halstead-Reitan battery: demographically adjusted neuropsychological norms for African American and Caucasian adults. Psychological Assessment Resources, Inc., Odessa, FL
Heaton RK, Clifford DB, Franklin DR, Woods SP, 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: CHARTER study. Neurology 75:2087–2096. doi:10.1212/WNL.0b013e318200d727
Heaton, RK, Franklin, DR, Ellis, RJ, McCutchan, JA, Letendre, SL, Leblanc, S, Corkran, SH, Duarte, NA, Clifford, DB, Woods, SP, Collier, AC, Marra, CM, Morgello, S, Mindt, MR, Taylor, MJ, Marcotte, TD, Atkinson, JH, Wolfson, T, Gelman, BB, McArthur, JC, Simpson, DM, Abramson, I, Gamst, A, Fennema-Notestine, C, Jernigan, TL, Wong, J, Grant I, CHARTER Group, HNRC Group (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.
Hinkin CH, Castellon SA, Durvasula RS, Hardy DJ, Lam MN, Mason KI, Stefaniak M (2002) Medication adherence among HIV+ adults: effects of cognitive dysfunction and regimen complexity. Neurology 59:1944–1950
Janssen RS, Cornblath DR, Epstein LG et al (1991) Nomenclature and research case definitions for neurological manifestations of human immunodeficiency virus type-1 (HIV-1) infection. Report of a working Group of the American Academy of neurology AIDS task force. Neurology 41:778–785
Kaplan E, Goodglass H, Weintraub S (1983) Boston naming test. Lea & Febiger, Philadelphia
Karnofsky DA, Burchenal JH (1949) The clinical evaluation of chemo-therapeutic agents in cancer. In: Maclead CM (ed) Evaluation of chemotherapeutic agents. Columbia University Press, New York, pp 191–205
Kløve H (1963) Grooved pegboard. Lafayette Instruments, Indiana
Lawton MP, Brody EM (1969) Assessment of older people: self-maintaining and instrumental activities of daily living. Gerontologist 9:179–186
McNair DM, Lorr M, Droppleman LF (1981) Profile of mood states. Educational and Industrial Testing Service, San Diego, CA
Meyer AC, Boscardin WJ, Kwasa JK, Price RW (2013) Is it time to rethink how neuropsychological tests are used to diagnose mild forms of HIV-associated neurocognitive disorders? Impact of false-positive rates on prevalence and power. Neuroepidemiology 41:208–216
Morgan EE, Iudicello JE, Weber E, Duarte NA, Riggs PK, Delano-Wood L, Ellis R, Grant I, Woods SP, HNRP Group (2012) Synergistic effects of HIV infection and older age on daily functioning. J Acquir Immune Defic Syndr 61:341–348. doi:10.1097/QAI.0b013e31826bfc53
Obermeit LC, Beltran J, Casaletto KB, Franklin DR, Letendre S, Ellis R, Fennema-Notestine C, Vaida F, Collier AC, Marra CM, Clifford D, Gelman B, Sacktor N, Morgello S, Simpson D, McCutchan JA, Grant I, Heaton RK; CNS HIV Anti-Retroviral Therapy Effects Research (CHARTER) Group (2016). Evaluating the accuracy of self-report for the diagnosis of HIV associated neurocognitive disorder (HAND): defining "symptomatic" versus "asymptomatic" HAND. J Neurovirol. [Epub ahead of print] PubMed
Piatt AL, Fields JA, Paolo AM, Tröster AI (1999) Action (verb naming) fluency as an executive function measure: convergent and divergent evidence of validity. Neuropsychologia 37:1499–1503
Psychological Corporation (1997) WAIS-III and WMS-III technical manual. Author, San Antonio, TX
Psychological Corporation (2001) Manual for the Wechsler test of adult reading (WTAR). Author, San Antonio
Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, Wu J et al (2007) The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 21(14):1915–1921
Seider TR, Luo X, Gongvatana A, Devlin KN, de la Monte SM, Chasman JD et al (2014) Verbal memory declines more rapidly with age in HIV infected versus uninfected adults. J Clin Exp Neuropsychol 36:356–367. doi:10.1080/13803395.2014.892061
Sevigny JJ, Albert SM, McDermott MP, Schifitto G, McArthur JC, Sacktor N et al (2007) An evaluation of neurocognitive status and markers of immune activation as predictors of time to death in advanced HIV infection. Arch Neurol 64:97–102
Sheppard DP, Woods SP, Bondi MW, Gilbert PE, Massman PJ, Doyle KL (2015) Does older age confer an increased risk of incident neurocognitive disorders among persons living with HIV disease? Clin Neuropsychol 29:656–677
Simioni, S, Cavassini, M, Annoni, J, Rimbault Abraham, A, Bourquin, I, Schiffer, V. Du Pasquier, RA (2010). Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. AIDS (London, England), 24(9), 1243
Su T, Schouten J, Geurtsen GJ, Wit FW, Stolte IG, Prins M, Portegies P, Caan MWA, Reiss P, Majoie CB, Schmand BA, AGE HIV Cohort Study Group (2015) Multivariate normative comparison, a novel method for more reliably detecting cognitive impairment in HIV infection. AIDS 29:547–557. doi:10.1097/QAD.0000000000000573
Wechsler D (1997) Wechsler memory scale-third edition. The Psychological Corporation, San Antonio, TX
Woods SP, Rippeth JD, Frol AB, Levy JK, Ryan E, Soukup VM, Heaton RK (2004) Interrater reliability of clinical ratings and neurocognitive diagnoses in HIV. J Clin Exp Neuropsychol 26:759–778. doi:10.1080/ 13803390490509565
Woods SP, Morgan EE, Dawson M, Scott JC, Grant I, HNRC Group (2006) Action (verb) fluency predicts dependence in instrumental activities of daily living in persons infected with HIV-1. J Clin Exp Neuropsychol 28:1030–1042. doi:10.1080/13803390500350985
World Health Organization (1998). Composite international diagnostic interview. World Health Organization; Geneva, Switzerland (CIDI, version 2.1)
Acknowledgements
The authors have no financial conflicts of interest related to this work. This study was supported by NIH grants R01-MH073419 and P30-MH62512. The authors are grateful to the UC San Diego HIV Neurobehavioral Research Program (HNRP) Group (I. Grant, PI) for their infrastructure support of the parent R01. In particular, we thank Donald Franklin, Dr. Erin Morgan, Clint Cushman, and Stephanie Corkran for their assistance with data processing, Marizela Verduzco for her assistance with study management, Drs. Scott Letendre and Ronald J. Ellis for their assistance with the neuromedical aspects of the parent project, and Dr. J. Hampton Atkinson and Jennifer Marquie Beck for their assistance with participant recruitment and retention. The views expressed in this article are those of the authors and do not reflect the official policy or position of the Department of the Navy, Department of Defense, nor the US Government. The authors thank the study volunteers for their participation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Tierney, S.M., Sheppard, D.P., Kordovski, V.M. et al. A comparison of the sensitivity, stability, and reliability of three diagnostic schemes for HIV-associated neurocognitive disorders. J. Neurovirol. 23, 404–421 (2017). https://doi.org/10.1007/s13365-016-0510-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13365-016-0510-z