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Published in: Journal of Neurology 5/2020

Open Access 01-05-2020 | Human Immunodeficiency Virus | Original Communication

Microalbuminuria: a sentinel of neurocognitive impairment in HIV-infected individuals?

Authors: Antoine Moulignier, Anne-Claire Viret-Vilayphon, François-Xavier Lescure, Emmanuelle Plaisier, Laurence Salomon, Cédric Lamirel, Gilles Pialoux, The ALCOVE Study Group

Published in: Journal of Neurology | Issue 5/2020

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Abstract

Background

According to population-based studies, microalbuminuria is associated with subsequent cognitive decline over a 4–6-year period, because of cerebral small-vessel disease (CSVD). This prospective cross-sectional study (NCT02852772) was designed to evaluate whether a history of microalbuminuria is associated with subsequent cognitive decline in combined antiretroviral therapy (cART)-treated persons living with human immunodeficiency virus (PLHIVs).

Methods

From our computerized medical database, we identified 30 PLHIVs (median age 52 years), immunovirologically controlled on cART, who had microalbuminuria in 2008 and had undergone, between 2013 and 2015, a comprehensive neuropsychological assessment (NPA) including seven domains (cases): information-processing speed, motor skills, executive functions, attention/working memory, learning/memory, reasoning and verbal fluency. Forty-nine PLHIVs matched for age (median age 48 years; p = 0.19), sex, and year of first HIV-seropositivity without microalbuminuria in 2008 were identified and underwent the same NPA between 2013 and 2015 (controls).

Results

Cases performed less well than controls for information-processing speed (p = 0.01) and motor skills (p = 0.02), but no differences were found for the other cognitive domains and global z-scores. A multivariable linear-regression model adjusted for confounding factors confirmed the microalbuminuria effect for the information-processing-speed z score.

Conclusion

cART-treated PLHIVs with a history of microalbuminuria subsequently had worse cognitive performances for the information-processing-speed domain, possibly because of CSVD. Our observations should be considered preliminary findings of a temporal link between microalbuminuria, CSVD, and subsequent cognitive impairment.
Literature
1.
go back to reference Lee M, Ovbiagele B (2011) Reno-cerebrovascular disease: linking the nephron and neuron. Expert Rev Neurother 11:241–249CrossRef Lee M, Ovbiagele B (2011) Reno-cerebrovascular disease: linking the nephron and neuron. Expert Rev Neurother 11:241–249CrossRef
2.
go back to reference Mogi M, Horiuchi M (2011) Clinical interaction between brain and kidney in small vessel disease. Cardiol Res Pract 2011:1–5CrossRef Mogi M, Horiuchi M (2011) Clinical interaction between brain and kidney in small vessel disease. Cardiol Res Pract 2011:1–5CrossRef
3.
go back to reference Toyoda K (2015) Cerebral small vessel disease and chronic kidney disease. J Stroke 17:31–37CrossRef Toyoda K (2015) Cerebral small vessel disease and chronic kidney disease. J Stroke 17:31–37CrossRef
4.
go back to reference Chillon J-M, Massy ZA, Stengel B (2016) Neurological complications in chronic kidney disease patients. Nephrol Dial Transplant 31:1606–1614CrossRef Chillon J-M, Massy ZA, Stengel B (2016) Neurological complications in chronic kidney disease patients. Nephrol Dial Transplant 31:1606–1614CrossRef
5.
go back to reference Monk RD, Bennett DA (2006) Reno-cerebrovascular disease? The incognito kidney in cognition and stroke. Neurology 67:196–198CrossRef Monk RD, Bennett DA (2006) Reno-cerebrovascular disease? The incognito kidney in cognition and stroke. Neurology 67:196–198CrossRef
6.
go back to reference Jabbari B, Vaziri ND (2018) The nature, consequences, and management of neurological disorders in chronic kidney disease: neurology and chronic kidney disease. Hemodial Int 22:150–160CrossRef Jabbari B, Vaziri ND (2018) The nature, consequences, and management of neurological disorders in chronic kidney disease: neurology and chronic kidney disease. Hemodial Int 22:150–160CrossRef
7.
go back to reference Georgakis MK, Dimitriou NG, Karalexi MA et al (2017) Albuminuria in association with cognitive function and dementia: a systematic review and meta-analysis. J Am Geriatr Soc 65:1190–1198CrossRef Georgakis MK, Dimitriou NG, Karalexi MA et al (2017) Albuminuria in association with cognitive function and dementia: a systematic review and meta-analysis. J Am Geriatr Soc 65:1190–1198CrossRef
8.
go back to reference Georgakis MK, Chatzopoulou D, Tsivgoulis G, Petridou ET (2018) Albuminuria and cerebral small vessel disease: a systematic review and meta-analysis. J Am Geriatr Soc 66:509–517CrossRef Georgakis MK, Chatzopoulou D, Tsivgoulis G, Petridou ET (2018) Albuminuria and cerebral small vessel disease: a systematic review and meta-analysis. J Am Geriatr Soc 66:509–517CrossRef
9.
go back to reference Weiner DE, Bartolomei K, Scott T et al (2009) Albuminuria, cognitive functioning, and white matter hyperintensities in homebound elders. Am J Kidney Dis 53:438–447CrossRef Weiner DE, Bartolomei K, Scott T et al (2009) Albuminuria, cognitive functioning, and white matter hyperintensities in homebound elders. Am J Kidney Dis 53:438–447CrossRef
10.
go back to reference Martens RJH, Kooman JP, Stehouwer CDA et al (2017) Estimated GFR, albuminuria, and cognitive performance: the Maastricht study. Am J Kidney Dis 69:179–191CrossRef Martens RJH, Kooman JP, Stehouwer CDA et al (2017) Estimated GFR, albuminuria, and cognitive performance: the Maastricht study. Am J Kidney Dis 69:179–191CrossRef
11.
go back to reference Wada M, Nagasawa H, Kurita K et al (2007) Microalbuminuria is a risk factor for cerebral small vessel disease in community-based elderly subjects. J Neurol Sci 255:27–34CrossRef Wada M, Nagasawa H, Kurita K et al (2007) Microalbuminuria is a risk factor for cerebral small vessel disease in community-based elderly subjects. J Neurol Sci 255:27–34CrossRef
12.
go back to reference Weiner DE, Gaussoin SA, Nord J et al (2017) Cognitive function and kidney disease: baseline data from the systolic blood pressure intervention trial (SPRINT). Am J Kidney Dis 70:357–367CrossRef Weiner DE, Gaussoin SA, Nord J et al (2017) Cognitive function and kidney disease: baseline data from the systolic blood pressure intervention trial (SPRINT). Am J Kidney Dis 70:357–367CrossRef
13.
go back to reference Moulignier A, Savatovsky J, Assoumou L et al (2018) Silent cerebral small-vessel disease is twice as prevalent in middle-aged individuals with well-controlled, combination antiretroviral therapy-treated human immunodeficiency virus (HIV) than in HIV-uninfected individuals. Clin Infect Dis 66:1762–1769CrossRef Moulignier A, Savatovsky J, Assoumou L et al (2018) Silent cerebral small-vessel disease is twice as prevalent in middle-aged individuals with well-controlled, combination antiretroviral therapy-treated human immunodeficiency virus (HIV) than in HIV-uninfected individuals. Clin Infect Dis 66:1762–1769CrossRef
14.
go back to reference Januel E, Godin O, Moulignier A et al (2019) Impact of ART classes on the increasing risk of cerebral small-vessel disease in middle-aged, well-controlled, cART-treated, HIV-infected individuals; Microvascular Brain Retina And Kidney (MicroBREAK) Study Group. J Acquir Immune Defic Syndr 81:547–551CrossRef Januel E, Godin O, Moulignier A et al (2019) Impact of ART classes on the increasing risk of cerebral small-vessel disease in middle-aged, well-controlled, cART-treated, HIV-infected individuals; Microvascular Brain Retina And Kidney (MicroBREAK) Study Group. J Acquir Immune Defic Syndr 81:547–551CrossRef
15.
go back to reference Cysique LA, Brew BJ (2019) Vascular cognitive impairment and HIV-associated neurocognitive disorder: a new paradigm. J Neurovirol (Epub ahead of print) Cysique LA, Brew BJ (2019) Vascular cognitive impairment and HIV-associated neurocognitive disorder: a new paradigm. J Neurovirol (Epub ahead of print)
16.
go back to reference Su T, Wit FWNM, Caan MWA et al (2016) White matter hyperintensities in relation to cognition in HIV-infected men with sustained suppressed viral load on combination antiretroviral therapy. AIDS 30:2329–2339CrossRef Su T, Wit FWNM, Caan MWA et al (2016) White matter hyperintensities in relation to cognition in HIV-infected men with sustained suppressed viral load on combination antiretroviral therapy. AIDS 30:2329–2339CrossRef
17.
go back to reference Schouten J, Su T, Wit FW et al (2016) Determinants of reduced cognitive performance in HIV-1-infected middle-aged men on combination antiretroviral therapy. AIDS 30:1027–1038CrossRef Schouten J, Su T, Wit FW et al (2016) Determinants of reduced cognitive performance in HIV-1-infected middle-aged men on combination antiretroviral therapy. AIDS 30:1027–1038CrossRef
18.
go back to reference Janssen MAM, Meulenbroek O, Steens SCA et al (2015) Cognitive functioning, wellbeing and brain correlates in HIV-1 infected patients on long-term combination antiretroviral therapy. AIDS 29:2139–2148CrossRef Janssen MAM, Meulenbroek O, Steens SCA et al (2015) Cognitive functioning, wellbeing and brain correlates in HIV-1 infected patients on long-term combination antiretroviral therapy. AIDS 29:2139–2148CrossRef
19.
go back to reference Meyer A-CL, 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 41:208–216CrossRef Meyer A-CL, 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 41:208–216CrossRef
20.
go back to reference Lescure F-X, Fellahi S, Pialoux G, et al (2019) Prevalence of tubulopathy and association with renal function loss in HIV-infected patients. Nephrol Dial Transplant (Epub ahead of print) Lescure F-X, Fellahi S, Pialoux G, et al (2019) Prevalence of tubulopathy and association with renal function loss in HIV-infected patients. Nephrol Dial Transplant (Epub ahead of print)
21.
go back to reference Antinori A, Arendt G, Becker JT et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799CrossRef Antinori A, Arendt G, Becker JT et al (2007) Updated research nosology for HIV-associated neurocognitive disorders. Neurology 69:1789–1799CrossRef
22.
go back to reference McDonnell J, Haddow L, Daskalopoulou M et al (2014) Minimal cognitive impairment in UK HIV-positive men who have sex with men: effect of case definitions and comparison with the general population and HIV-negative men. J Acquir Immune Defic Syndr 67:120–127CrossRef McDonnell J, Haddow L, Daskalopoulou M et al (2014) Minimal cognitive impairment in UK HIV-positive men who have sex with men: effect of case definitions and comparison with the general population and HIV-negative men. J Acquir Immune Defic Syndr 67:120–127CrossRef
23.
go back to reference Underwood J, De Francesco D, Leech R et al (2018) Medicalising normality? Using a simulated dataset to assess the performance of different diagnostic criteria of HIV-associated cognitive impairment. PLoS ONE 13:e0194760CrossRef Underwood J, De Francesco D, Leech R et al (2018) Medicalising normality? Using a simulated dataset to assess the performance of different diagnostic criteria of HIV-associated cognitive impairment. PLoS ONE 13:e0194760CrossRef
24.
go back to reference Gisslén M, Price RW, Nilsson S (2011) The definition of HIV-associated neurocognitive disorders: are we overestimating the real prevalence? BMC Infect Dis 11:356CrossRef Gisslén M, Price RW, Nilsson S (2011) The definition of HIV-associated neurocognitive disorders: are we overestimating the real prevalence? BMC Infect Dis 11:356CrossRef
25.
go back to reference Nightingale S, Winston A, Letendre S et al (2014) Controversies in HIV-associated neurocognitive disorders. Lancet Neurol 13:1139–1151CrossRef Nightingale S, Winston A, Letendre S et al (2014) Controversies in HIV-associated neurocognitive disorders. Lancet Neurol 13:1139–1151CrossRef
26.
go back to reference Azam B, Whitfield TJ, Radford D et al (2016) Trends in referred patient profiles in a memory clinic over 20 years. Dementia 15:789–797CrossRef Azam B, Whitfield TJ, Radford D et al (2016) Trends in referred patient profiles in a memory clinic over 20 years. Dementia 15:789–797CrossRef
27.
go back to reference Hamilton M (1967) Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 6:278–296CrossRef Hamilton M (1967) Development of a rating scale for primary depressive illness. Br J Soc Clin Psychol 6:278–296CrossRef
28.
go back to reference Thomas-Antérion C, Honoré-Masson S, Laurent B (2006) The cognitive complaint interview (CCI). Psychogeriatrics 6:S18–S22CrossRef Thomas-Antérion C, Honoré-Masson S, Laurent B (2006) The cognitive complaint interview (CCI). Psychogeriatrics 6:S18–S22CrossRef
29.
go back to reference Röhrig B, du Prel J-B, Wachtlin D, Blettner M (2009) Types of study in medical research: part 3 of a series on evaluation of scientific publications. Dtsch Arzteblatt Int 106:262–268 Röhrig B, du Prel J-B, Wachtlin D, Blettner M (2009) Types of study in medical research: part 3 of a series on evaluation of scientific publications. Dtsch Arzteblatt Int 106:262–268
30.
go back to reference Omair A (2016) Selecting the appropriate study design: case–control and cohort study designs. J Health Spec 4:37–41CrossRef Omair A (2016) Selecting the appropriate study design: case–control and cohort study designs. J Health Spec 4:37–41CrossRef
31.
go back to reference Kalayjian RC, Wu K, Evans S et al (2014) Proteinuria is associated with neurocognitive impairment in antiretroviral therapy treated HIV-infected individuals. J Acquir Immune Defic Syndr 67:30–35CrossRef Kalayjian RC, Wu K, Evans S et al (2014) Proteinuria is associated with neurocognitive impairment in antiretroviral therapy treated HIV-infected individuals. J Acquir Immune Defic Syndr 67:30–35CrossRef
32.
go back to reference Prins ND, van Dijk EJ, den Heijer T et al (2005) Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain 128:2034–2041CrossRef Prins ND, van Dijk EJ, den Heijer T et al (2005) Cerebral small-vessel disease and decline in information processing speed, executive function and memory. Brain 128:2034–2041CrossRef
33.
go back to reference ter Telgte A, van Leijsen EMC, Wiegertjes K et al (2018) Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol 14:387–398CrossRef ter Telgte A, van Leijsen EMC, Wiegertjes K et al (2018) Cerebral small vessel disease: from a focal to a global perspective. Nat Rev Neurol 14:387–398CrossRef
34.
go back to reference Fellows RP, Byrd DA, Morgello S (2014) Effects of information processing speed on learning, memory, and executive functioning in people living with HIV/AIDS. J Clin Exp Neuropsychol 36:806–817CrossRef Fellows RP, Byrd DA, Morgello S (2014) Effects of information processing speed on learning, memory, and executive functioning in people living with HIV/AIDS. J Clin Exp Neuropsychol 36:806–817CrossRef
35.
go back to reference Sacre JW, Magliano DJ, Zimmet PZ et al (2018) Associations of chronic kidney disease markers with cognitive function: a 12-year follow-up study. J Alzheimers Dis 70:S19–S30CrossRef Sacre JW, Magliano DJ, Zimmet PZ et al (2018) Associations of chronic kidney disease markers with cognitive function: a 12-year follow-up study. J Alzheimers Dis 70:S19–S30CrossRef
36.
go back to reference Makinson A, Dubois J, Eymard-Duvernay S, et al (2019) Increased prevalence of neurocognitive impairment in aging people living with human immunodeficiency virus: the ANRS EP58 HAND 55–70 Study. Clin Infect Dis (Epub ahead of print) Makinson A, Dubois J, Eymard-Duvernay S, et al (2019) Increased prevalence of neurocognitive impairment in aging people living with human immunodeficiency virus: the ANRS EP58 HAND 55–70 Study. Clin Infect Dis (Epub ahead of print)
37.
go back to reference Fleming J, Mathews WC, Rutstein RM et al (2019) Low level viremia and virologic failure in persons with HIV infection treated with antiretroviral therapy. AIDS 33:2005–2012CrossRef Fleming J, Mathews WC, Rutstein RM et al (2019) Low level viremia and virologic failure in persons with HIV infection treated with antiretroviral therapy. AIDS 33:2005–2012CrossRef
38.
go back to reference Dyer AR (2004) Evaluation of measures of urinary albumin excretion in epidemiologic studies. Am J Epidemiol 160:1122–1131CrossRef Dyer AR (2004) Evaluation of measures of urinary albumin excretion in epidemiologic studies. Am J Epidemiol 160:1122–1131CrossRef
39.
go back to reference Bakker AJ (1999) Detection of microalbuminuria. Receiver operating characteristic curve analysis favors albumin-to-creatinine ratio over albumin concentration. Diabetes Care 22:307–313CrossRef Bakker AJ (1999) Detection of microalbuminuria. Receiver operating characteristic curve analysis favors albumin-to-creatinine ratio over albumin concentration. Diabetes Care 22:307–313CrossRef
Metadata
Title
Microalbuminuria: a sentinel of neurocognitive impairment in HIV-infected individuals?
Authors
Antoine Moulignier
Anne-Claire Viret-Vilayphon
François-Xavier Lescure
Emmanuelle Plaisier
Laurence Salomon
Cédric Lamirel
Gilles Pialoux
The ALCOVE Study Group
Publication date
01-05-2020
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 5/2020
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-019-09674-6

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