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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 16  |  Issue : 1  |  Page : 108-114

A study of neurocognitive dysfunction in HIV-positive patients in a tertiary care center in South India


1 Department of General Medicine, JSSAHER, Mysuru, Karnataka, India
2 Department of Undergraduate Student JSSMC, JSSAHER, Mysuru, Karnataka, India

Date of Submission24-Sep-2019
Date of Decision18-Nov-2020
Date of Acceptance30-Dec-2020
Date of Web Publication29-Jul-2021

Correspondence Address:
Dr. Rajendra Prasad Shivaswamy
JSSMC, JSSAHER, Mysore, Karnataka
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1319-4534.322599

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  Abstract 


Context: HIV-associated neurocognitive disorder (HAND) is an ongoing problem among HIV-positive patients, irrespective of whether the patients are on antiretroviral treatment (ART) or not. ART has helped in halting the progression of the disease, but still, research needs to be done in reversing the disorder. Patients on ART are still known to have a mild neurocognitive disorder. The prevalence of HAND is estimated in approximately 40%–50% of all cases. Aims: (1) To determine the presence of neurocognitive dysfunction in HIV-positive patients. (2) To determine sociodemographic factors that influence this condition. (3) To determine the relationship between CD4 count and neurocognitive dysfunction. Settings and Design: The sampling technique was purposive sampling. A cross-sectional study was undertaken in a sample size of 162 among patients attending the outpatient department of medicine department using the International HIV Dementia Scale (IHDS). Subjects and Methods: IHDS has the maximum possible score of 12 points. A patient with a score of ≤10 should be evaluated further for possible dementia. Statistical Analysis: Data entry was done in an Excel sheet. Data analysis was done using SPSS. Results: It was found that of the 162 patients who participated in the study, 71% were found to be at risk for the neurocognitive disorder. The factors which had a significant association were age, education, spouse alive or not, and HIV status of the spouse. Conclusion: It was found that out that neurocognitive disorder is common in the ART era and also it can be detected by simple bedside tests.

Keywords: HIV, HIV-associated neurocognitive disorder, neurocognitive disorder


How to cite this article:
Shivaswamy RP, Ashok A, Jayaram SC, Thandure V, Dowerah J. A study of neurocognitive dysfunction in HIV-positive patients in a tertiary care center in South India. J Datta Meghe Inst Med Sci Univ 2021;16:108-14

How to cite this URL:
Shivaswamy RP, Ashok A, Jayaram SC, Thandure V, Dowerah J. A study of neurocognitive dysfunction in HIV-positive patients in a tertiary care center in South India. J Datta Meghe Inst Med Sci Univ [serial online] 2021 [cited 2021 Sep 16];16:108-14. Available from: http://www.journaldmims.com/text.asp?2021/16/1/108/322599




  Introduction Top


HIV-associated neurocognitive disorder (HAND) is still an ongoing problem among HIV-positive patients, irrespective of whether the patients are on antiretroviral treatment (ART) or not.[1],[2],[3] Although modern ART has helped in halting the progression of the disease, a lot of research need to be done in reversing the disorder.[4] Patients on ART are still known to have mild neurocognitive disorder (MND).[5]

The prevalence of HAND is estimated in approximately 40%–50% of all cases. MND and asymptomatic neurocognitive impairment are now more common than HIV-associated dementia (HAD).[1]

The reason for neurocognitive disorders in HIV patients is still unclear. It is known that the central nervous system (CNS) is one of the target organs where HIV can be detected soon after primary infection.[1]

While HIV can affect many tissues, there are two major targets, the immune system and the CNS. The macrophages and the microglia are the predominant cell types affected in the brain.[6] Virtually all patients with HIV infection have some degree of nervous system involvement.

The risk factors associated with neurocognitive disorders are not well established in the post highly active ART (HAART) era. Some of them include host factors such as genetic predisposition, metabolic disorders, cardiovascular risk factor or aging, HIV-related factors such as AIDS, immune activation, drug resistance, and comorbidities such as hepatitis C virus coinfection or depression. Poor immunological status in the form of low CD4 cell count has been associated with neurocognitive impairment before and after HAART.[7],[8],[9]

Evaluating all patients of HIV for HAND will go a long way in detecting the condition early and manage them with suitable ART, thereby improving the quality of life.


  Subjects and Methods Top


Objectives of the study

  1. To determine the presence of neurocognitive disorder in HIV-positive patients
  2. To determine sociodemographic factors that influence this condition
  3. To determine the relationship between CD4 count and neurocognitive disorder


Study design

The study is a cross-sectional study.

Methodology

Materials

  1. Sociodemographic sheet
  2. International HIV Dementia Scale (IHDS) Created by Sactktor et al. AIDS 2005 19:1367-1374 [Annexure].


IHDS has the maximum possible score of 12 points. A patient with a score of ≤10 should be evaluated further for possible dementia.

Sampling

A cross-sectional study was undertaken in a sample size of 162 among patients attending the Outpatient Department (OPD) of the Medicine Department at JSS Hospital, Mysuru in Karnataka. The sampling technique was purposive sampling.

The sample size was obtained by the formula () 2*p*q/d 2, where P = 18.8 and d = 6. This came up to 162 patients.

Study population

The study population included HIV-positive patients attending the (OPD) of medicine and both ART naïve and patients who are already on ART.

Eligibility

Inclusion criteria

All HIV-positive patients who are >18 years were included in the study.

Exclusion criteria

  1. Patients who are <18 years
  2. Patients already suffering from mental illness
  3. Pregnant women who are HIV positive.


Assessment of endpoints

Primary

  1. Presence of neurocognitive dysfunction in HIV-positive patients.
  2. To determine sociodemographic factors
  3. To measure the CD4 count of the patient.


Secondary

  1. To determine the relationship between CD4 count and neurocognitive dysfunction
  2. To determine the relationship between sociodemographic factors and neurocognitive dysfunction.


Method of data collection

Sociodemographic details of the patient like age, sex, occupation, education, income, marital status, drug abuse, alcohol consumption, and comorbidities were recorded. The patient's CD4 count was noted.

Confidentiality agreement

Confidentiality regarding the patient's name and their personal details was strictly maintained. Written consent was obtained in the local language before recruiting the patients to the study. Ethical clearance was obtained from the Institutional Ethical committee.

Procedure

Patients satisfying the inclusion criteria were assessed for HAD by the IHDS.

Data analysis

Data entry was done in an Excel sheet. Data analysis was done using SPSS version 25 (SPSS Inc., Chicago, Ill., USA). Descriptive statistics such as the mean and standard deviation for quantitative data and percentage (rates) for the qualitative data were estimated. Inferential statistical tests such as Chi-square test, unpaired t-test, and Pearson's correlation were applied. Data were interpreted statistically significant at P < 0.05.

Ethical clearance

The study was conducted after obtaining ethical clearance from JSS Medical College, Mysore Ref no : JSSMC/IEC/010219/20 NCT/2019-20 Dated: 4th Feb 2019.


  Results Top


Descriptive analysis

Using the aforementioned methodology, a sample of 162 patients who attended the medicine OPD, who were HIV positive, was assessed for neurocognitive impairment.

The following were the results obtained

The mean age of the population was around 43.06 years, with a standard deviation of 11.572. The median number of years of the patients who were on anti-retroviral treatment was 3 years, with least being 1.8 years and maximum being 5 years. The average CD4 count was 362.5 with maximum and minimum of 554 and 196, respectively. The mean International HIV Dementia Score was in the range from 7 to 11, with an average of 9.

Of the 162 patients who were interviewed, 54.9% were male and 44.4% were female and 0.6% (n = 1) were transgender. Of the 162 patients, 143 were married (88.27%).

When the place of residence was analyzed, it was found that 38.9% were from urban areas, 59.3% hailed from semi urban areas, and 1.9% were from rural areas.

When the education level of the patients was analyzed, it was found that 21% were illiterates, 28.4% were educated up to secondary school, 26.5% were educated up to primary school, and 24.1% were educated up to college.

Housewives formed the large chunk with 28.4%, followed by people in the service sector (19.1%) and agricultural laborers were 16%. The details of the various occupations of the patients are given in [Table 1].
Table 1: Details of the occupation of the patients

Click here to view


About 89.5% reported no history of smoking, whereas 4.3% and 6.2% were smokers and past smokers, respectively. Almost 90.7% were nonalcoholics, 3.7% were habitual alcoholics, 1.9% were social drinkers, and 3.7% were alcoholics in the past. Cessation of habits such as smoking and alcohol can go a long way in treating HAND and was therefore considered here.

The spouses of 69.1% of the population were alive, 19.8% of the population were dead, and 11.1% of the population data were not married. The HIV status of the spouse/family members was looked into to assess the possible risk of transmission and for putting them on treatment. About 38.9% had a family member with HIV-positive status, 31.5% did not have a family member with HIV-positive status, and in 18.5% of the patients, the HIV status of the spouse was unknown.

Details of previous antiretroviral were taken. Almost 91.4% had not received any antiretroviral in the past.

Seventy-one percent of the sample was found to have an IHDS score ≤10 (dementia) and therefore would need to undergo further evaluations for dementia. Twenty-nine percent had an IHDS score of ≥11 and were therefore not considered to have a risk for dementia. The details are given in [Table 2].
Table 2: Frequency of dementia among the patients

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There wa a significant association between age and IHDS score distribution. The mean age of those with an IHDS score of ≤10 was 45.46, with a mean deviation of 10.8, and the mean age of those with an IHDS score of >10 was 37.17 with a mean deviation of 11.351 [Table 3].
Table 3: Age-wise distribution of International HIV Dementia Scale score (n=162)

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A similar analysis was done between gender and IHDS score. There was no significant association between gender and IHDS score distribution (P < 0.732). Since only one transgender was a part of the study, it was excluded as it did not affect the statistics significantly.

The association between literacy and IHDS score was significant. The details are given in [Table 4]. Almost 94.1% of those who were illiterate had an IHDS score of ≤10 and 67.4% of those who were educated up to secondary school had an IHDS score of ≤10. About 79.1% of those who were educated up to primary school had an IHDS score of ≤10 and 46.2% of those who were educated up to college had an IHDS score of ≤10.
Table 4: Literacy-wise distribution of International HIV Dementia Scale score (n=162)

Click here to view


Unemployed included those who were retired, students, housewives, and unemployed. There was no significant association between IHDS score and occupation of the patient. The details are given in [Table 5].
Table 5: Occupation-wise distribution of International HIV Dementia Scale score (n=162)

Click here to view


There was no significant association between tenofavir, lamivudine, and efavirenz (TLE) regimen and IHDS score. About 66.1% of the patients who were on this regimen had an IHDS score of ≤10. Other regimens were clubbed into single category to obtain statistically significant results since a majority of them were on TLE regimen. The details are given in [Table 6].
Table 6: Regimen-wise distribution of International HIV Dementia Scale score (n=162)

Click here to view


The habit of smoking did not have an impact on the IHDS score (P = 0.969). Smokers included past and current smokers. As depicted in [Table 7], there was no significant association between alcohol habit and IHDS score. This included past, current, and social alcoholic habits.
Table 7: Distribution of International HIV Dementia Scale score based on alcohol habit (n=162)

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There was no significant association between marital status and IHDS score (P = 0.739). Similarly, past exposure to anti-retoviral medication and IHDS score were analyzed. There was no significant association between the IHDS score and the usage of antiretroviral in the past (P = 0.069).

The relationship between the HIV status of the spouse and IHDS score was analyzed. There was a significant relationship between the IHDS score and the HIV status of the spouse (P = 0.017). About 61.3% of those with an HIV-positive spouse had an IHDS Score of ≤10 and 72.5% of those with an HIV-negative spouse had an IHDS score of ≤10 [Table 8].
Table 8: Distribution of International HIV Dementia Scale score based on the HIV status of the spouse (n=143)

Click here to view


Nearly 66.7% of those whose spouses were dead had an IHDS score of ≤10 and 87.5% of those whose spouses were alive had an IHDS score of >10. The association was significant. The existence of the spouse seemed to have a significant effect on the mental makeup of the patient (P = 0.022). This might have affected the IHDS score significantly [Table 9].
Table 9: Distribution of International HIV Dementia Scale score based on whether the spouses of the study participants were alive or dead

Click here to view


The association between CD4 count and IHDS was compared [Table 10]. Here, there was no significant relationship between the CD4 count and IHDS score (P = 0.383).
Table 10: Distribution of International HIV Dementia Scale score based on CD4 count of the patients

Click here to view



  Discussion Top


One of the main objectives of the study was to find the prevalence of neurocognitive disorder among HIV-positive patients. A total of 162 patients were recruited in our study, of which 115 (71%) had an IHDS score which was found to be ≤10. In few of the studies conducted in Botswana and South Ethiopia, the prevalence of HAND was around 68% and 65.6%, respectively.[10],[11] However, a study conducted by Yusuf et al. showed a low prevalence (19%).[12] This could be due to the difference in viral clades with variation in neurovirulence and variation in the sociodemographic profiles may play a role.[11]

Its association with various sociodemographic factors such as age, gender, education, employment, smoking, marital status, regimen, and alcohol habit was made.

There was a significant association between age and neurocognitive disorder in this study (P < 0.001). In this study, the mean age of patients whose IHDS score was <10 was 45.46 ± 10.8 years. In a study done by Sacktor et al., at the Johns Hopkins University, the age of patients with similar scores varied from 43.9 to 48.9, with older age group having severe neurocognitive disorder.[13] Similar findings have been reported by Tedaldi et al.[14] This is because the age itself is a risk factor for dementia, and with increased survival of HIV-positive patients, the chances of the developing neurocognitive disorder are high.[15] In a study done by Kinai et al. and Chan et al., it was found that age >55 years was identified as a risk factor for HAND, and also, older age patients used to show the disorder in the early stage of the disease.[16],[17]

In this study, there was no significant association between gender and IHDS score. In the study done by Animut et al. in Ethiopia, there was no such association.[11] According to Sundermann EE and Maki PM, the neurocognitive disorder was more common among females, this could be due to low educational status.[18],[19]

As per this study, there is a significant association between literacy and IHDS score (P < 0.001). Lesser education level was associated with an IHDS score of <10. A similar finding was seen in the study conducted byYusuf et al.[12] This could be due to the fact that lesser education makes a patient to reach health-care setting late, and also, the understanding of the tests to be performed may have been affected.

Marital Status had no significant association with the IHDS score (P = 0.739). However, in a 2017 Ethiopian study conducted, there was a significant association between the IHDS score and marital status, with the highest being in single individuals.[11] The reason could be that family support could have prevented the patients from developing neurocognitive disorder.[11]

Another factor which affected the IHDS score significantly was whether the study participant's spouse was alive or not (P = 0.022). Although there were no reference study to compare this finding with. Majority of those whose spouses were alive had an IHDS score of >ten. The existence of the spouse seemed to have a significant effect on the mental makeup of the patient. This might have affected the IHDS score significantly.

Another finding made in this study was that of the association between the IHDS and the HIV status of the spouse, wherein more number of those with HIV-negative spouses were found to have an IHDS score of ≤ (P = 0.017), which was very surprising. There was no reference available in this regard.

There was no significant association between the regimen and the IHDS score. Other studies have mentioned that tenofovir has lesser CNS penetration when compared to drugs such as zidovudine and lamivudine.[11]

There was no significant association between the past antiretroviral status and the IHDS score. There were no relevant studies in this regard.

CD4 count was compared with the IHDS score. There was no significant relationship between CD4 count and IHDS score (P = 0.383). Similar findings were found in a study conducted by Sacktor et al. at the Johns Hopkins University.[13] However, the study conducted by Yusuf et al. in Northern Nigeria and Pinheiro et al. in South Brazil and Chan et al. in Asia found a significant relationship between CD4 count and IHDS score. Patients with low CD4 count had neurocognitive disorder.[12],[17],[20] Recent research has suggested that cognitive impairment may become more likely with the lower value of the nadir CD4 cell count than the current CD4 count.[10] In our study, we did not know the nadir CD4 count.

Alcohol consumption had no effect on the status of neurocognitive function in this study, which is very surprising. A similar finding was found in the Ethiopian study. This could be because the participants did not use alcohol in large amount.[11] Some studies have shown to have an effect on neurocognitive function. Heavy alcohol affects ART adherence.[21] Research has shown that certain brain areas are affected by both HIV infection and chronic alcohol abuse. Chronic alcohol abuse increases the metabolic injury in the brains of HIV-infected people.[22],[23]

Smoking habit though known to impair the immune system, it is known that nicotine found in cigarettes and HIV together may contribute to hasten the progression to HAND.[24] However, in this study, there was no such significant association with the IHDS score. A similar finding has been reported by Tsima et al. from the University of Botswana.[25] However, according to Bryant et al., there was a role of smoking in neurocognitive dysfunction. This difference could be the difference in methodology, and also, we did not consider the duration of smoking. It is thought that smoking increases HIV replication.[14],[26]

Occupational status and thereby the level of income seemed to hold a significant relationship with the IHDS score in a recent study conducted in Ethiopia,[11],[14] There was a high incidence of neurocognitive disorders among patients who were unemployed and who had less income when compared to employed.[27] However, surprisingly in this study, employment did not have a significant impact on the IHDS score (P = 0.181).

The place where the patient resided, i.e. urban, rural, and semi-urban, did not make a difference to the IHDS score in this study. However, in the study done in Ethiopia, there was a high incidence among the urban population compared to the rural population.[11]


  Conclusion Top


There is a high prevalence of HAND even in the era of ART. All patients have to be evaluated for its presence using simple bedside techniques. If IHDS score is <10, further evaluation has to be done to rule out dementia. This will help in treating these patients early and also if necessary make suitable modification in the ART regimen, which crosses the blood–brain barrier and acts on HIV virus lodged in the CNS, thereby improving the quality of life of affected patients. There are several factors which influence it. Some of the factors differ from the previous studies.

Acknowledgment

We would like to acknowledge the counselors in the medicine OPD, who helped in getting the information of the patients.

Financial support and sponsorship

The JSS Academy of Higher Education and Research funded Rs. 10,000/- (Ten thousand only) for the project.

Conflicts of interest

There are no conflicts of interest.


  Annexure Top



  International HIV Dementia Scale: Top


Memory Registration – Give four words to recall (dog, hat, bean, and red) – 1 s to say each. Then, ask the patient all four words after you have said them. Repeat words if the patient does not recall them all immediately. Tell the patient you will ask for recall of the words again a bit later.

1.Motor Speed: Have the patient tap the first two fingers of the nondominant hand as widely and as quickly as possible.

  • 4 = 15 in 15 s
  • 3 = 11–14 in 5 s
  • 2 = 7–10 in 5 s
  • 1 = 3–6 in 5 s
  • 0=0–2 in 5 s.


2. Psychomotor Speed: Have the patient perform the following movements with the nondominant hand as quickly as possible:

  • Clench hand in fist on flat surface
  • Put hand flat on surface with palm down.
  • Put hand perpendicular to flat surface on the side of the 5th digit.
  • Demonstrate and have patient perform twice for practice.


  • o 4 = 4 sequences in 10 s

    o 3 = 3 sequences in 10 s

    o 2 = 2 sequences in 10 s

    o 1 = 1 sequence in 10 s

    o 0=unable to perform


3. Memory Recall: Ask the patient to recall the four words. For words not recalled, prompt with a semantic clue as follows: Animal (dog); piece of clothing (hat);

vegetable (bean); and color (red).

Give 1 point for each word spontaneously recalled.

Give 0.5 points for each correct answer after prompting

Maximum – 4 points.

Total International HIV Dementia Scale Score:

This is the sum of the scores on items 1–3. The maximum possible score is 12 points. A patient with a score of ≤ 10 should be evaluated further for possible dementia.[13]



 
  References Top

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Sanmarti M, Ibáñez L, Huertas S, Badenes D, Dalmau D, Slevin M, et al. HIV-associated neurocognitive disorders. J Mol Psychiatry 2014;2:2-10.  Back to cited text no. 1
    
2.
Heaton RK, Franklin DR, Ellis RJ, McCutchan JA, Letendre SL, Leblanc S, et al. HIV-associated neurocognitive disorders before and during the era of combination antiretroviral therapy: Differences in rates, nature, and predictors. J Neurovirol 2011;17:3-16.  Back to cited text no. 2
    
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Mateen FJ, Shinohara RT, Carone M, Miller EN, McArthur JC, Jacobson LP, et al. Neurologic disorders incidence in HIV+vs HIV − men: Multicenter AIDS cohort study. Neurology 2012;79:1873-80.  Back to cited text no. 3
    
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Clifford DB. HIV-associated neurocognitive disorder. Curr Opin Infect Dis 2017;30:117-22.  Back to cited text no. 4
    
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Simioni S, Cavassini M, Annoni JM, Rimbault Abraham A, Bourquin I, Schiffer V, et al. Cognitive dysfunction in HIV patients despite long-standing suppression of viremia. AIDS 2010;24:1243-50.  Back to cited text no. 5
    
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Spudich S, González-Scarano F. HIV-1-related central nervous system disease: Current issues in pathogenesis, diagnosis, and treatment. Cold Spring Harb Perspect Med 2012;2: a007120.  Back to cited text no. 6
    
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Heaton RK, Clifford DB, Franklin DR Jr, Woods SP, Ake C, Vaida F, et al. HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 2010;75:2087-96.  Back to cited text no. 7
    
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Robertson KR, Smurzynski M, Parsons TD, Wu K, Bosch RJ, Wu J, et al. The prevalence and incidence of neurocognitive impairment in the HAART era. AIDS 2007;21:1915-21.  Back to cited text no. 8
    
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Tozzi V, Balestra P, Serraino D, Bellagamba R, Corpolongo A, Piselli P, et al. Neurocognitive impairment and survival in a cohort of HIV-infected patients treated with HAART. AIDS Res Hum Retroviruses 2005;21:706-13.  Back to cited text no. 9
    
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Lawler K, Mosepele M, Ratcliffe S, Seloilwe E, Steele K, Nthobatsang R, et al. Neurocognitive impairment among HIV-positive individuals in Botswana: A pilot study. J Int AIDS Soc 2010;13:15.  Back to cited text no. 10
    
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Debalkie Animut M, Sorrie MB, Birhanu YW, Teshale MY. High prevalence of neurocognitive disorders observed among adult people living with HIV/AIDS in Southern Ethiopia: A cross-sectional study. PLoS One 2019;14:e0204636.  Back to cited text no. 11
    
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Yusuf AJ, Hassan A, Mamman AI, Muktar HM, Suleiman AM, Baiyewu O. Prevalence of HIV-Associated Neurocognitive Disorder (HAND) among Patients Attending a Tertiary Health Facility in Northern Nigeria. J Int Assoc Provid AIDS Care 2017;16:48-55.  Back to cited text no. 12
    
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Sacktor NC, Wong M, Nakasujja N, Skolasky RL, Selnes OA, Musisi S, et al. The International HIV Dementia Scale: A new rapid screening test for HIV dementia. AIDS 2005;19:1367-74.  Back to cited text no. 13
    
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Tedaldi EM, Minniti NL, Fischer T. HIV-associated neurocognitive disorders: The relationship of HIV infection with physical and social comorbidities. Biomed Res Int 2015;2015:641913.  Back to cited text no. 14
    
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Tozzi V, Balestra P, Salvatori MF, Vlassi C, Liuzzi G, Giancola ML, et al. Changes in cognition during antiretroviral therapy: Comparison of 2 different ranking systems to measure antiretroviral drug efficacy on HIV-associated neurocognitive disorders. J Acquir Immune Defic Syndr 2009;52:56-63.  Back to cited text no. 15
    
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Kinai E, Komatsu K, Sakamoto M, Taniguchi T, Nakao A, Igari H, et al. Association of age and time of disease with HIV-associated neurocognitive disorders: A Japanese nationwide multicenter study. J Neurovirol 2017;23:864-74.  Back to cited text no. 16
    
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Chan LG, Kandiah N, Chua A. HIV-associated neurocognitive disorders (HAND) in a South Asian population-contextual application of the 2007 criteria. BMJ Open 2012;2:e000662.  Back to cited text no. 17
    
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Sundermann EE, Heaton RK, Pasipanodya E, Moore RC, Paolillo EW, Rubin LH, et al. Sex differences in HIV-associated cognitive impairment. AIDS 2018;32:2719-26.  Back to cited text no. 18
    
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Maki PM, Martin-Thormeyer E. HIV, cognition and women. Neuropsychol Rev 2009;19:204-14.  Back to cited text no. 19
    
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Pinheiro CA, Souza LD, Motta JV, Kelbert EF, Souza MS, Martins CS, et al. Depression and diagnosis of neurocognitive impairment in HIV-positive patients. Braz J Med Biol Res 2016;49:e5344.  Back to cited text no. 20
    
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Samet JH, Cheng DM, Libman H, Nunes DP, Alperen JK, Saitz R. Alcohol consumption and HIV disease progression. J Acquir Immune Defic Syndr 2007;46:194-9.  Back to cited text no. 21
    
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Gongvatana A, Morgan EE, Iudicello JE, Letendre SL, Grant I, Woods SP, et al. A history of alcohol dependence augments HIV-associated neurocognitive deficits in persons aged 60 and older. J Neurovirol 2014;20:505-13.  Back to cited text no. 22
    
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Meyerhoff DJ. Effects of alcohol and HIV infection on the central nervous system. Alcohol Res Health 2001;25:288-98.  Back to cited text no. 23
    
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Atluri VS, Pilakka-Kanthikeel S, Samikkannu T, Sagar V, Kurapati KR, Saxena SK, et al. Vorinostat positively regulates synaptic plasticity genes expression and spine density in HIV infected neurons: Role of nicotine in progression of HIV-associated neurocognitive disorder. Mol Brain 2014;7:37.  Back to cited text no. 24
    
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Tsima B, Ratcliffe SJ, Schnoll R, Frank I, Kolson DL, Gross R. Is tobacco use associated with neurocognitive dysfunction in individuals with HIV? J Int Assoc Provid AIDS Care 2018;17:2325958218768018.  Back to cited text no. 25
    
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Bryant VE, Kahler CW, Devlin KN, Monti PM, Cohen RA. The effects of cigarette smoking on learning and memory performance among people living with HIV/AIDS. AIDS Care 2013;25:1308-16.  Back to cited text no. 26
    
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Rueda S, Raboud J, Mustard C, Bayoumi A, Lavis JN, Rourke SB. Employment status is associated with both physical and mental health quality of life in people living with HIV. AIDS Care 2011;23:435-43.  Back to cited text no. 27
    



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9], [Table 10]



 

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