Executive function and processing speed in Brazilian HIV-infected children and adolescents

Haase, Vitor Geraldi; Nicolau, Nelsa Carol; Viana, Virgínia Nunes; Pinto, Jorge Andrade

doi:10.1590/S1980-57642014DN81000006

ABSTRACT

Background: Cognitive disorders in infants and children who are vertically infected with human immunodeficiency virus (HIV) have been recognized since the inception of the epidemic. Objective: The present study investigated neuropsychological performance in a cohort of vertically infected Brazilian children and adolescents who underwent antiretroviral therapy. The neuropsychological tasks were designed to evaluate executive function and processing speed. Methods: Children and adolescents were recruited at a major research and treatment reference center for human immunodeficiency virus/acquired immunodeficiency syndrome (HIV) in Minas Gerais, Brazil. Forty-one individuals aged 5 to 17 years were enrolled. Twelve were mildly symptomatic (HIV-infected group, Centers for Disease Control and Prevention [CDC] class A or B), and 29 had advanced clinical disease (AIDS group, CDC class C). Results: The results showed that HIV-infected children and adolescents exhibited lower performance on neuropsychological tasks than sociodemographically comparable, typically developing controls. Motor and cognitive processing speed and executive function appeared to be the most discriminative domains. Conclusion: HIV-infected individuals with more-advanced disease stages exhibited lower performance levels and had greater performance heterogeneity on neuropsychological tasks. Thus, the observed neuropsychological impairments, although more pronounced in participants with more advanced stages of the disease, did not correlate with the variable used (CDC stage).

Key words:
HIV; AIDS; neuropsychology; executive function; processing speed

RESUMO

Introdução: Comprometimentos cognitivos em crianças e adolescentes verticalmente afetadas por HIV são reconhecidos desde do início da epidemia. Objetivos: O presente estudo investigou o desempenho neuropsicológico em uma coorte de crianças e adolescentes verticalmente infectadas por HIV e que fazem uso da terapia antirretroviral no Brasil. As tarefas neuropsicológicas foram selecionadas para avaliar, principalmente, funções executivas e velocidade de processamento. Métodos: As crianças e adolescentes foram recrutados em um grande centro de referência de pesquisa e tratamento para o vírus da imunodeficiência humana / síndrome da imunodeficiência adquirida (HIV / AIDS), em Minas Gerais, Brasil. Quarenta e um indivíduos com idade entre 5 e 17 anos foram selecionados. Doze estavam com sintomas leves (grupo infectado pelo HIV, Centros para Controle e Prevenção de Doenças [CDC] Classe A ou B), e 29 tiveram a doença clínica avançada (grupo AIDS, CDC classe C). Resultados: Os resultados mostraram que as crianças e adolescentes infectados pelo HIV apresentaram menor desempenho em tarefas neuropsicológicas quando comparadas com o grupo controle pareado socio-demograficamente. Habilidades motoras, velocidade de processamento e função executiva são os domínios mais discriminativos. Conclusão: Indivíduos infectados pelo HIV com estágios da doença mais avançados apresentaram níveis mais baixos de desempenho e tiveram maior heterogeneidade no desempenho em tarefas neuropsicológicas. Entretanto, os prejuízos neuropsicológicos observados, apesar de se mostrarem mais pronunciados com estágios mais avançados da doença, não se correlacionaram com a variável utilizada (estágio do CDC).

Palavras-chave:
HIV; AIDS; neuropsicologia; funções executivas; velocidade de processamento

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REFERENCES

¹
Allison S, Wolters PL, Brouwers P. Youth with HIV/AIDS: neurobehavioral consequences. In: Paul RH, Sacktor NC, Valcour V, Tashima, KT. (Eds). HIV and the brain. New challenges in the modern era. New York: Humana; 2009:187-211.
²
Centers for Disease Control and Prevention. Reduction in perinatal transmission of HIV infection. United States:1985-2005. MMWR Morb Mortal Wkly Rep 2006;55:592-597.
³
Nachman SA, Chernoff M, Gona P, et al.; PACTG 219C Team. Incidence of noninfectious conditions in perinatally HIV-infected children and adolescents in the HAART era. Arch Pediatr Adolesc Med. 2009;163:164-167.
⁴
Kakehasi FM, Pinto JA, Romanelli RM, et al. Determinants and trends in perinatal human immunodeficiency virus type 1 (HIV-1) transmission in the metropolitan area of Belo Horizonte, Brazil: 1998 - 2005. Mem Inst Oswaldo Cruz 2008;103:351-357.
⁵
Matida LH, Ramos AN Jr, Heukelbach J, Hearst N. Brazilian Study Group on Survival of Children with AIDS. Continuing improvement in survival for children with acquired immunodeficiency syndrome in Brazil. Pediatr Infect Dis J 2009;28:920-922.
⁶
Hazra R, Siberry GK, Mofenson LM. Growing up with HIV: children, adolescents, and young adults with perinatally acquired HIV infection. Annu Rev Med 2010;61:169-185.
⁷
Woods SP, Moore DJ, Weber E, Grant I. Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 2009; 19:152-168.
⁸
Sherr L, Mueller J, Varrall R. A systematic review of cognitive development and child human immunodeficiency virus infection. Psychol Health Med 2009;14:387-404.
⁹
Frank EG, Foley GM, Kuchuk A. Cognitive functioning in school-age children with human immunodeficiency virus. Percept Mot Skills 1997; 85:267-272.
¹⁰
Levenson RL Jr, Mellins CA, Zawadzki R, Kairam R, Stein Z. Cognitive assessment of human immunodeficiency virus-exposed children. Am J Dis Child 1992;146:1479-1483.
¹¹
Piazza F, Astori MG, Maccabruni A, Caselli D, Bossi G, Lanzi G. [Neuropsychological development of children born to HIV-positive mothers]. Pediatr Med Chir 1995;17:331-333.
¹²
Tardieu M, Mayaux MJ, Seibel N, et al. Cognitive assessment of school-age children infected with maternally transmitted human immunodeficiency virus type 1. J Pediatr 1995;126:375-379.
¹³
Koekkoek S, de Sonneville LM, Wolfs TF, Licht R, Geelen SP. Neurocognitive function profile in HIV-infected school-age children. Eur J Paediatr Neurol 2008;12:290-297.
¹⁴
Bisiacchi PS, Suppiej A, Laverda A. Neuropsychological evaluation of neurologically asymptomatic HIV-infected children. Brain Cogn 2000; 43:49-52.
¹⁵
Blanchette N, Smith ML, King S, Fernandes-Penney A, Read S. Cognitive development in school-age children with vertically transmitted HIV infection. Dev Neuropsychol 2002;21:223-241.
¹⁶
Bagenda D, Nassali A, Kalyesubula I. Health, neurologic, and cognitive status of HIV-infected, long-surviving, and antiretroviral-naive Ugandan children. Pediatrics 2006;117:729-740.
¹⁷
Martin SC, Wolters PL, Toledo-Tamula MA, Zeichner SL, Hazra R, Civitello L. Cognitive functioning in school-aged children with vertically acquired HIV infection being treated with highly active antiretroviral therapy (HAART). Dev Neuropsychol 2006;30:633-657.
¹⁷
18. Hasan KM, Eluvathingal TJ, Kramer LA, Ewing-Cobbs L, Dennis M, Fletcher JM. White matter microstructural abnormalities in children with spina bifida myelomeningocele and hydrocephalus: a diffusion tensor tractography study of the association pathways. J Magn Reson Imaging 2008;27:700-709.
¹⁹
Filley CM. The Behavioral Neurology of White Matter. 2nd ed. New York: Oxford University Press; 2002:448.
²⁰
20. Patel SH, Inglese M, Glosser G, Kolson DL, Grossman RI, Gonen O. Whole-brain N-acetylaspartate level and cognitive performance in HIV infection. AJNR Am J Neuroradiol 2003;24:1587-1591.
²¹
Gabis L, Belman A, Huang W, Milazzo M, Nachman S. Clinical and imaging study of human immunodeficiency virus-1-infected youth receiving highly active antiretroviral therapy: pilot study using magnetic resonance spectroscopy. J Child Neurol 2006;21:486-490.
²²
Dawes S, Suarez P, Casey CY, et al. Variable patterns of neuropsychological performance in HIV-1 infection. J Clin Exp Neuropsychol 2008; 30:613-626.
²³
Angelini, AL, Alves ICB, Custódio EM, Duarte WF, Duarte JLM. Raven. Manual Matrizes Progressivas Coloridas de Raven: Escala especial. São Paulo: Centro Editor de Testes e Pesquisas em Psicologia; 1999.
²⁴
Santucci H. Prova gráfica de organização perceptiva para crianças de 4 a 6 anos. In: Zazzo R (Eds.) Manual para o exame psicológico da criança. São Paulo: Mestre Jou; 1981;1:396-438.
²⁵
Fuster, J. The prefrontal cortex.4th Ed. San Diego: Academic; 2008:424.
²⁶
Garon N, Bryson SE, Smith IM. Executive function in preschoolers: a review using an integrative framework. Psychol Bull 2008;134:31-60.
²⁷
Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex "Frontal Lobe" tasks: a latent variable analysis. Cogn Psychol 2000;41:49-100.
²⁸
Natale LL, Teodoro MLM, Barreto G V, Haase VG. Propriedades psicométricas de tarefas para avaliar funções executivas em pré-escolares. Psicol Pesquisa 2008;2:23-35.
²⁹
Wechsler D. WISC-III: Escala de Inteligência Wechsler para crianças: Manual. São Paulo: Casa do Psicólogo; 1991.
³⁰
Gerstadt CL, Hong YJ, Diamond A. The relationship between cognition and action: performance of children 3 1/2-7 years old on a Stroop-like day-night test. Cognition 1994;53:129-153.
³¹
Welsh MC, Pennington BF, Ozonoff S, Rouse B, McCabe ER. Neuropsychology of early-treated phenylketonuria: specific executive function deficits. Child Dev 1990;6:1697-1713.
³²
Zimmermann P, Fimm B. Test for Attention Performance (TAP). Psytest, Würselen; 1995.
³³
Klahr D, Robinson M. Formal assessment of problem solving and planning processes in preschool children. Cognitive Psycholog 1981;13: 113-148.
³⁴
Haase VG, Lacerda SS, Wood GMO, Daker MV, Lana-Peixoto MA. Estudos clínicos iniciais com o Teste de Discriminação de Listas (TDL-UFMG). Psicologia: Reflexão e Crítica 2001;14:289-304.
³⁵
LeFever FF, Kumkova EI. The recency test: clinical adaptation of an experimental procedure for studying frontal lobe function with implications for lateral specialization and different modes of temporal judgment. Brain Cognition 1996;30:286-289.
³⁶
Milner B, McAndrews MP, Leonard G. Frontal lobes and memory for the temporal order of recent events. Cold Spring Harb Symp Quant Biol 1990;55:987-994.
³⁷
Hardy DJ, Hinkin CH. Reaction time performance in adults with HIV/AIDS. J Clin Exp Neuropsychol 2002;24:912-929.
³⁸
Fischer JS, Jak AJ, Kniker JE, Rudick RA (eds.) Multiple Sclerosis Functional Composite (MSFC): Administration and scoring manual. New York: National Multiple Sclerosis Society; 2001.
³⁹
Poole JL, Burtner PA, Torres TA, et al. Measuring dexterity in children using the Nine-hole Peg Test. J Hand Ther 2005;18:348-351.
⁴⁰
Smith YA, Hong E, Presson C. Normative and validation studies of the Nine-hole Peg Test with children. Percept Mot Skills 2000:823-843.
⁴¹
Strauss E, Sherman EMS, Spreen O (eds.). A compendium of Neuropsychological Testes: Administration, Norms and Commentary 3rd ed. New York: Oxford University Press; 2006:1240.
⁴²
Abubakar A, Van Baar A, Van de Vijver FJ, Holding P, Newton CR. Paediatric HIV and neurodevelopment in sub-Saharan Africa: a systematic review. Trop Med Int Health 2008;13:880-887.
⁴³
Puthanakit T, Aurpibul L, Louthrenoo O, et al. Poor cognitive functioning of school-aged children in thailand with perinatally acquired HIV infection taking antiretroviral therapy. AIDS Patient Care STDS 2010;24:141-146.
⁴⁴
Berkman A, Garcia J, Muñoz-Laboy M, Paiva V, Parker R. A critical analysis of the Brazilian response to HIV/AIDS: lessons learned for controlling and mitigating the epidemic in developing countries. Am J Public Health 2005;95:1162-1672.
⁴⁵
Brackis-Cott E, Kang E, Dolezal C, Abrams EJ, Mellins CA. The impact of perinatal HIV infection on older school-aged children's and adolescents'receptive language and word recognition skills. AIDS Patient Care STDS. 2009;23:415-421.
⁴⁶
Kail RV, Ferrer E. Processing speed in childhood and adolescence: longitudinal models for examining developmental change. Child Dev 2007; 78:1760-1770.
⁴⁷
Deary IJ. Reaction time and psychometric intelligence: Jensen's contribution. In Nyborg H (Eds). The scientific study of general intelligence: tribute to Arthur R. Jensen. New York: Elsevier; 2003:53-75.
⁴⁸
Bayliss DM, Jarrold C, Gunn DM, Baddeley AD. The complexities of complex span: explaining individual differences in working memory in children and adults. J Exp Psychol Gen 2003;132:71-92.
⁴⁹
Al-Khindi T, Zakzanis KK, van Gorp WG. Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. J Int Neuropsychol Soc 2011;17:956-69.
⁵⁰
TOZZI V, BALESTRA P, BELLAGAMBA R, ET AL. PERSISTENCE OF NEUROPSYCHOLOGIC DEFICITS DESPITE LONG-TERM HIGHLY ACTIVE ANTIRETROVIRAL THERAPY IN PATIENTS WITH HIV-RELATED NEUROCOGNITIVE IMPAIRMENT: PREVALENCE AND RISK FACTORS. J ACQUIR IMMUNE DEFIC SYNDR 2007;45:174-182.

Publication Dates

Publication in this collection
Jan-Mar 2014

History

Received
10 Oct 2013
Accepted
12 Dec 2014

This is an open-access article distributed under the terms of the Creative Commons Attribution License

[1] ¹
Allison S, Wolters PL, Brouwers P. Youth with HIV/AIDS: neurobehavioral consequences. In: Paul RH, Sacktor NC, Valcour V, Tashima, KT. (Eds). HIV and the brain. New challenges in the modern era. New York: Humana; 2009:187-211.

[2] ²
Centers for Disease Control and Prevention. Reduction in perinatal transmission of HIV infection. United States:1985-2005. MMWR Morb Mortal Wkly Rep 2006;55:592-597.

[3] ³
Nachman SA, Chernoff M, Gona P, et al.; PACTG 219C Team. Incidence of noninfectious conditions in perinatally HIV-infected children and adolescents in the HAART era. Arch Pediatr Adolesc Med. 2009;163:164-167.

[4] ⁴
Kakehasi FM, Pinto JA, Romanelli RM, et al. Determinants and trends in perinatal human immunodeficiency virus type 1 (HIV-1) transmission in the metropolitan area of Belo Horizonte, Brazil: 1998 - 2005. Mem Inst Oswaldo Cruz 2008;103:351-357.

[5] ⁵
Matida LH, Ramos AN Jr, Heukelbach J, Hearst N. Brazilian Study Group on Survival of Children with AIDS. Continuing improvement in survival for children with acquired immunodeficiency syndrome in Brazil. Pediatr Infect Dis J 2009;28:920-922.

[6] ⁶
Hazra R, Siberry GK, Mofenson LM. Growing up with HIV: children, adolescents, and young adults with perinatally acquired HIV infection. Annu Rev Med 2010;61:169-185.

[7] ⁷
Woods SP, Moore DJ, Weber E, Grant I. Cognitive neuropsychology of HIV-associated neurocognitive disorders. Neuropsychol Rev 2009; 19:152-168.

[8] ⁸
Sherr L, Mueller J, Varrall R. A systematic review of cognitive development and child human immunodeficiency virus infection. Psychol Health Med 2009;14:387-404.

[9] ⁹
Frank EG, Foley GM, Kuchuk A. Cognitive functioning in school-age children with human immunodeficiency virus. Percept Mot Skills 1997; 85:267-272.

[10] ¹⁰
Levenson RL Jr, Mellins CA, Zawadzki R, Kairam R, Stein Z. Cognitive assessment of human immunodeficiency virus-exposed children. Am J Dis Child 1992;146:1479-1483.

[11] ¹¹
Piazza F, Astori MG, Maccabruni A, Caselli D, Bossi G, Lanzi G. [Neuropsychological development of children born to HIV-positive mothers]. Pediatr Med Chir 1995;17:331-333.

[12] ¹²
Tardieu M, Mayaux MJ, Seibel N, et al. Cognitive assessment of school-age children infected with maternally transmitted human immunodeficiency virus type 1. J Pediatr 1995;126:375-379.

[13] ¹³
Koekkoek S, de Sonneville LM, Wolfs TF, Licht R, Geelen SP. Neurocognitive function profile in HIV-infected school-age children. Eur J Paediatr Neurol 2008;12:290-297.

[14] ¹⁴
Bisiacchi PS, Suppiej A, Laverda A. Neuropsychological evaluation of neurologically asymptomatic HIV-infected children. Brain Cogn 2000; 43:49-52.

[15] ¹⁵
Blanchette N, Smith ML, King S, Fernandes-Penney A, Read S. Cognitive development in school-age children with vertically transmitted HIV infection. Dev Neuropsychol 2002;21:223-241.

[16] ¹⁶
Bagenda D, Nassali A, Kalyesubula I. Health, neurologic, and cognitive status of HIV-infected, long-surviving, and antiretroviral-naive Ugandan children. Pediatrics 2006;117:729-740.

[17] ¹⁷
Martin SC, Wolters PL, Toledo-Tamula MA, Zeichner SL, Hazra R, Civitello L. Cognitive functioning in school-aged children with vertically acquired HIV infection being treated with highly active antiretroviral therapy (HAART). Dev Neuropsychol 2006;30:633-657.

[18] ¹⁷
18. Hasan KM, Eluvathingal TJ, Kramer LA, Ewing-Cobbs L, Dennis M, Fletcher JM. White matter microstructural abnormalities in children with spina bifida myelomeningocele and hydrocephalus: a diffusion tensor tractography study of the association pathways. J Magn Reson Imaging 2008;27:700-709.

[19] ¹⁹
Filley CM. The Behavioral Neurology of White Matter. 2nd ed. New York: Oxford University Press; 2002:448.

[20] ²⁰
20. Patel SH, Inglese M, Glosser G, Kolson DL, Grossman RI, Gonen O. Whole-brain N-acetylaspartate level and cognitive performance in HIV infection. AJNR Am J Neuroradiol 2003;24:1587-1591.

[21] ²¹
Gabis L, Belman A, Huang W, Milazzo M, Nachman S. Clinical and imaging study of human immunodeficiency virus-1-infected youth receiving highly active antiretroviral therapy: pilot study using magnetic resonance spectroscopy. J Child Neurol 2006;21:486-490.

[22] ²²
Dawes S, Suarez P, Casey CY, et al. Variable patterns of neuropsychological performance in HIV-1 infection. J Clin Exp Neuropsychol 2008; 30:613-626.

[23] ²³
Angelini, AL, Alves ICB, Custódio EM, Duarte WF, Duarte JLM. Raven. Manual Matrizes Progressivas Coloridas de Raven: Escala especial. São Paulo: Centro Editor de Testes e Pesquisas em Psicologia; 1999.

[24] ²⁴
Santucci H. Prova gráfica de organização perceptiva para crianças de 4 a 6 anos. In: Zazzo R (Eds.) Manual para o exame psicológico da criança. São Paulo: Mestre Jou; 1981;1:396-438.

[25] ²⁵
Fuster, J. The prefrontal cortex.4th Ed. San Diego: Academic; 2008:424.

[26] ²⁶
Garon N, Bryson SE, Smith IM. Executive function in preschoolers: a review using an integrative framework. Psychol Bull 2008;134:31-60.

[27] ²⁷
Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD. The unity and diversity of executive functions and their contributions to complex "Frontal Lobe" tasks: a latent variable analysis. Cogn Psychol 2000;41:49-100.

[28] ²⁸
Natale LL, Teodoro MLM, Barreto G V, Haase VG. Propriedades psicométricas de tarefas para avaliar funções executivas em pré-escolares. Psicol Pesquisa 2008;2:23-35.

[29] ²⁹
Wechsler D. WISC-III: Escala de Inteligência Wechsler para crianças: Manual. São Paulo: Casa do Psicólogo; 1991.

[30] ³⁰
Gerstadt CL, Hong YJ, Diamond A. The relationship between cognition and action: performance of children 3 1/2-7 years old on a Stroop-like day-night test. Cognition 1994;53:129-153.

[31] ³¹
Welsh MC, Pennington BF, Ozonoff S, Rouse B, McCabe ER. Neuropsychology of early-treated phenylketonuria: specific executive function deficits. Child Dev 1990;6:1697-1713.

[32] ³²
Zimmermann P, Fimm B. Test for Attention Performance (TAP). Psytest, Würselen; 1995.

[33] ³³
Klahr D, Robinson M. Formal assessment of problem solving and planning processes in preschool children. Cognitive Psycholog 1981;13: 113-148.

[34] ³⁴
Haase VG, Lacerda SS, Wood GMO, Daker MV, Lana-Peixoto MA. Estudos clínicos iniciais com o Teste de Discriminação de Listas (TDL-UFMG). Psicologia: Reflexão e Crítica 2001;14:289-304.

[35] ³⁵
LeFever FF, Kumkova EI. The recency test: clinical adaptation of an experimental procedure for studying frontal lobe function with implications for lateral specialization and different modes of temporal judgment. Brain Cognition 1996;30:286-289.

[36] ³⁶
Milner B, McAndrews MP, Leonard G. Frontal lobes and memory for the temporal order of recent events. Cold Spring Harb Symp Quant Biol 1990;55:987-994.

[37] ³⁷
Hardy DJ, Hinkin CH. Reaction time performance in adults with HIV/AIDS. J Clin Exp Neuropsychol 2002;24:912-929.

[38] ³⁸
Fischer JS, Jak AJ, Kniker JE, Rudick RA (eds.) Multiple Sclerosis Functional Composite (MSFC): Administration and scoring manual. New York: National Multiple Sclerosis Society; 2001.

[39] ³⁹
Poole JL, Burtner PA, Torres TA, et al. Measuring dexterity in children using the Nine-hole Peg Test. J Hand Ther 2005;18:348-351.

[40] ⁴⁰
Smith YA, Hong E, Presson C. Normative and validation studies of the Nine-hole Peg Test with children. Percept Mot Skills 2000:823-843.

[41] ⁴¹
Strauss E, Sherman EMS, Spreen O (eds.). A compendium of Neuropsychological Testes: Administration, Norms and Commentary 3rd ed. New York: Oxford University Press; 2006:1240.

[42] ⁴²
Abubakar A, Van Baar A, Van de Vijver FJ, Holding P, Newton CR. Paediatric HIV and neurodevelopment in sub-Saharan Africa: a systematic review. Trop Med Int Health 2008;13:880-887.

[43] ⁴³
Puthanakit T, Aurpibul L, Louthrenoo O, et al. Poor cognitive functioning of school-aged children in thailand with perinatally acquired HIV infection taking antiretroviral therapy. AIDS Patient Care STDS 2010;24:141-146.

[44] ⁴⁴
Berkman A, Garcia J, Muñoz-Laboy M, Paiva V, Parker R. A critical analysis of the Brazilian response to HIV/AIDS: lessons learned for controlling and mitigating the epidemic in developing countries. Am J Public Health 2005;95:1162-1672.

[45] ⁴⁵
Brackis-Cott E, Kang E, Dolezal C, Abrams EJ, Mellins CA. The impact of perinatal HIV infection on older school-aged children's and adolescents'receptive language and word recognition skills. AIDS Patient Care STDS. 2009;23:415-421.

[46] ⁴⁶
Kail RV, Ferrer E. Processing speed in childhood and adolescence: longitudinal models for examining developmental change. Child Dev 2007; 78:1760-1770.

[47] ⁴⁷
Deary IJ. Reaction time and psychometric intelligence: Jensen's contribution. In Nyborg H (Eds). The scientific study of general intelligence: tribute to Arthur R. Jensen. New York: Elsevier; 2003:53-75.

[48] ⁴⁸
Bayliss DM, Jarrold C, Gunn DM, Baddeley AD. The complexities of complex span: explaining individual differences in working memory in children and adults. J Exp Psychol Gen 2003;132:71-92.

[49] ⁴⁹
Al-Khindi T, Zakzanis KK, van Gorp WG. Does antiretroviral therapy improve HIV-associated cognitive impairment? A quantitative review of the literature. J Int Neuropsychol Soc 2011;17:956-69.

[50] ⁵⁰
TOZZI V, BALESTRA P, BELLAGAMBA R, ET AL. PERSISTENCE OF NEUROPSYCHOLOGIC DEFICITS DESPITE LONG-TERM HIGHLY ACTIVE ANTIRETROVIRAL THERAPY IN PATIENTS WITH HIV-RELATED NEUROCOGNITIVE IMPAIRMENT: PREVALENCE AND RISK FACTORS. J ACQUIR IMMUNE DEFIC SYNDR 2007;45:174-182.

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