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. Author manuscript; available in PMC: 2021 Mar 1.
Published in final edited form as: J Clin Exp Neuropsychol. 2019 Nov 7;42(2):118–130. doi: 10.1080/13803395.2019.1687651

One-Year Stability of Prospective Memory Symptoms and Performance in Aging and HIV Disease

Victoria M Kordovski 1, Kelli L Sullivan 1, Savanna M Tierney 1, Steven Paul Woods 1
PMCID: PMC7002214  NIHMSID: NIHMS1541787  PMID: 31698985

Abstract

Introduction:

HIV disease and aging can both affect prospective memory (PM), which describes the complex process of executing delayed intentions and plays an essential role in everyday functioning. The current study investigated the course of PM symptoms and performance over approximately one year in younger and older persons with and without HIV disease.

Method:

Participants included 77 older (>50 years) and 35 younger (<40 years) HIV+ individuals and 44 older and 27 younger seronegative adults. Participants completed the Memory for Intentions Test to measure PM in the laboratory, the Prospective and Retrospective Memory Questionnaire to measure PM symptoms in daily life, and several clinical measures of executive functions and retrospective memory as a part of a comprehensive neurocognitive evaluation at baseline and at 14-month follow-up.

Results:

Findings showed additive, independent main effects of HIV and aging on time- and event-based PM performance in the laboratory, but no change in PM over time. There were no interactions between time and HIV or age groups. Parallel findings were observed for clinical measures of retrospective memory and executive functions. Older HIV+ adults endorsed the greatest frequency of PM symptoms, but there was no change in PM symptom severity over time and no interactions between time and HIV or age groups. There were no effects of HIV or aging on naturalistic PM performance longitudinally.

Conclusion:

Overall these findings suggest that PM symptoms and performance in the laboratory are stably impaired over the course of a year in the setting of aging and HIV disease.

Keywords: AIDS dementia complex, episodic memory, prospective memory, everyday memory, memory for intentions

Introduction

Prospective memory (PM) is a complex neurocognitive function that involves remembering to execute a future intention. PM plays an important role in everyday life and is an independent predictor of activities of daily living (e.g., Tierney, Bucks, Weinborn, Hodgson, & Woods, 2016) and health behaviors (e.g., Woods, Weinborn, Velnoweth, Rooney & Bucks, 2012). PM tasks may be time-based, in which the intended action is completed at a specific time (e.g., taking medication at 8:00 a.m.), or event-based, in which the intention is executed in response to an event-based cue (e.g., turning off the stove after cooking). The Multiprocess Model views PM tasks as occurring along a continuum, from those that require a high degree of strategic processing to those that are relatively automatic (McDaniel & Einstein, 2000). PM tasks that require substantial self-initiated monitoring for the PM cue, such as time-based and non-focal event-based tasks, are considered to be highly strategic and are associated with prefrontal networks (e.g., Cona, Bisiacchi, Sartori, & Scarpazza, 2016) and executive functions (e.g., Kamat et al., 2014). In contrast, in more automatic PM tasks, such as those with salient event-based cues, the intention may be spontaneously remembered when the participant notices the PM cue (e.g., McDaniel & Einstein, 2000). PM tasks that rely on these automatic processes are associated with medial temporal lobe volumes (Gordon, Shelton, Bugg, McDaniel, & Head, 2011) and retrospective memory (e.g., Kamat et al., 2014).

HIV and PM

HIV disease is associated with mild-to-moderate PM performance deficits across the lifespan (Carey et al., 2006; Harris et al., 2018; Woods et al., 2010). HIV predominantly affects fronto-striato-thalamo-cortical circuits (for a review see Ellis, Langford, & Masliah, 2007) and often disrupts executive functions (Walker & Brown, 2018). Thus it is not surprising that HIV has a greater impact on the more strategically demanding time-based PM tasks (Cohen’s d = .61) compared to event-based PM (d = .37) across the literature (see Avci et al., 2018). Specifically, when asked to complete laboratory PM tasks in response to time-based cues, HIV+ adults commit more omission errors, monitor the time less frequently (Doyle et al., 2013), and perform worse on tasks with longer delay periods (Morgan et al., 2012) compared to their seronegative counterparts. HIV+ individuals can also demonstrate event-based PM deficits, which may reflect a combination of retrospective memory errors (Zogg et al., 2011) as well as poor allocation of attention (Loft, Bowden, Ball, & Brewer, 2014; Woods et al., 2014). HIV-related PM difficulties are also relevant outside of the laboratory, as shown by studies indicating that HIV+ individuals perform worse on naturalistic PM tasks (e.g., Avci et al., 2016; Carey et al., 2006) and endorse elevated rates of PM symptoms (e.g., Woods et al., 2007) compared to uninfected adults. Importantly, laboratory, naturalistic, and self-report measures of PM are all reliably associated with functional outcomes in HIV disease (Avci et al., 2018), including medication adherence (e.g., Woods et al., 2009), employment (Woods, Weber, Weicz, Twamley, & Grant, 2011), risk-taking behaviors (Weinborn et al., 2013), and quality of life (e.g., Doyle et al., 2012).

Aging and PM in HIV

Among seronegative individuals, aging is strongly and independently associated with deficits in PM (Henry, MacLeod, Phillips, & Crawford, 2004), particularly for PM tasks with high strategic demands (for a review see McDaniel & Einstein, 2011). Aging can also modulate the effects of HIV on PM performance. As reviewed by Avci et al. (2018), studies have consistently found additive effects of aging (d = .71) and HIV (d = .62) on laboratory PM, which are independent of overall neurocognitive functioning and HIV disease severity (Avci et al., 2016; Weber et al., 2011; Woods et al., 2010). These additive effects are strongest for PM tasks with high strategic monitoring demands; however, there does not seem to be a synergistic effect of aging and HIV on PM performance in the laboratory (Avci et al., 2016; Weber et al., 2011; Woods et al., 2010). In contrast to findings from laboratory PM tasks, adults aging with HIV often perform comparably on naturalistic PM tasks and report similar levels of everyday PM symptoms compared to their younger HIV+ counterparts (Avci et al., 2016; Weber et al., 2011). According to the “age-PM paradox,” older age is sometimes associated with better naturalistic PM performance among seronegative adults (e.g., Rendell & Thomson, 1999), yet this aging benefit has not been observed in HIV disease. Among HIV+ older adults, better naturalistic PM performance is associated with compensatory strategy use (Weber et al., 2011), which suggests that HIV+ adults may fail to demonstrate strong PM performance in naturalistic settings due to problems deploying and executing effective strategies in everyday settings.

Trajectory of PM and Neurocognition in Aging and HIV

Although the detrimental effects of age and HIV on PM performance are well documented in cross-sectional research, the trajectory of PM in the setting of HIV disease is not known. In fact, there are only a handful of studies that have examined the course of PM in clinical populations. In individuals with first-episode schizophrenia, both time-based and event-based PM performance improve over a two-year period, although deficits in time-based PM persist while deficits in event-based PM appear to remit (Cheung et al., 2018). Among HIV+ individuals, lower laboratory-based PM performance at baseline is associated with a higher risk of incident HIV-associated neurocognitive disorders (HAND) one year later (d = .96; Sheppard et al., 2015); however, longitudinal changes in PM have not been studied in HIV. We are aware of only one prospective study of the effects of aging on PM among seronegative individuals (Serrani, 2010). In this study of 46 adults who were between the ages of 65 to 67 at baseline, declines in both event-based and time-based experimental PM tasks were documented after 5-year and 10-year follow-up intervals (Serrani, 2010). Thus, there is much to be learned about the course of PM symptoms and functioning in both HIV and aging.

Research on the trajectories of non-PM cognitive changes in HIV+ older adults may guide predictions about the course of PM. In the era of combination antiretroviral therapy (cART), approximately 30–50% of HIV+ adults have HIV-associated neurocognitive disorders (HAND; e.g. Heaton et al., 2010), with an annual incidence rate of approximately 15–20% (Robertson et al., 2007; Sheppard et al., 2015). While older HIV+ adults are more likely to have HAND than younger individuals, age is not a significant risk factor for one-year incidence of HAND (Becker, Lopez, Dew, & Aizenstein, 2004; Sheppard et al., 2015). Unlike many other neurocognitive disorders, HAND is not universally progressive. In one study of 436 HIV+ individuals, 22.7% of the sample demonstrated neurocognitive decline, 60.8% remained stable, and 16.5% improved after a mean follow-up interval of 35 months (Heaton et al., 2015). Executive functions and episodic memory, which support PM, are among the most commonly affected neurocognitive domains in HIV (e.g., Woods, Moore, Weber, & Grant, 2009); however, short-term longitudinal studies of these functions have found mixed results. In one study of 701 HIV+ adults, only 2–5% of participants declined on measures of executive functions over 36 months, while zero participants declined on measures of verbal fluency or delayed memory (Brouillette et al., 2016). A one-year longitudinal study of 82 Dutch HIV+ adults found that participants declined on measures of verbal fluency, mildly improved on other measures of executive functions, and showed no significant change in delayed retrospective memory (Janssen, Koopmans, & Kessels, 2017). Finally, Seider et al. (2014) found significant one-year declines in delayed verbal memory among older (age ≥55 years), but not younger (age 40–54 years), HIV+ adults.

Thus, while neurocognitive impairment seems to remain generally stable over short follow-up intervals in HIV, domain-specific findings are variable, with most studies documenting either stability or mild decline in executive functions and memory. In this study, we investigate how older age and HIV disease affect PM over time using a 2×2 factorial and longitudinal design in a well-characterized sample that had completed a comprehensive series of well-validated measures of PM symptoms, laboratory-based PM ability, and naturalistic PM performance. In parallel, we examined the effects of older age and HIV disease over time on well-validated clinical measures of retrospective memory and executive functions, which are hypothesized to support PM and have been widely demonstrated in studies of PM (Martin, Kliegel, and McDaniel, 2003; Clune-Ryberg et al., 2011). Considering the literature reviewed above, we expected to observe modest declines in laboratory-based PM and associated neurocognitive functions, which would be greatest among older HIV-infected adults.

Method

Participants

The total study sample included 183 individuals recruited from HIV clinics, community-based organizations, and the local San Diego community. Participants were included if they were aged 18 to 40 (i.e., Younger) or 50 years or older (i.e., Older). Consistent with National Institutes of Health neuroAIDS research recommendations (Stoff et al., 2004), this prospective study employed a discrepant age design using an age 50 cut-off for inclusion in the older group because there is: 1) a very low prevalence of HIV+ persons in the US who are age 65 and older (CDC, 2018); 2) a growing incidence and prevalence of HIV+ persons who are aged 50 and older (CDC, 2018); and 3) the possibility that HIV infection may accelerate (and accentuate) the neurocognitive changes associated with typical aging, which would result in earlier than expected declines (e.g., Sheppard et al., 2017). HIV serostatus was determined with a Western blot/ELISA or a MedMira rapid test. Individuals were excluded at baseline if they had an estimated verbal IQ score less than 70 on the Wechsler Test of Adult Reading (WTAR; Psychological Corporation, 2001) or histories of psychotic disorders, intellectual disability, or neurological conditions such as active central nervous system opportunistic infections, seizure disorders, head injury with a loss of consciousness more than 30 minutes, stroke with neurological sequelae, or non-HIV-related dementias. Individuals were also excluded if they met Diagnostic and Statistical Manual of Mental Disorders (4th ed.; American Psychiatric Association, 1994) criteria for substance use disorders (including marijuana) within 1 month of the baseline evaluation or if they tested positive in a urine toxicology screen for illicit drugs (except marijuana) on the day of baseline testing.

Materials and Procedure

Study procedures were approved by the human subjects institutional review board. Each participant provided written, informed consent and was administered standardized PM assessments and a comprehensive medical, psychiatric, and neurocognitive evaluation. Participants were recruited from the greater San Diego community and local HIV clinics and recruitment efforts were intended to provide a representative sample of the demographics of persons living with HIV in San Diego County (Health and Human Services Agency, 2012). All participants completed a full evaluation at baseline and returned for a follow-up evaluation 14 months later (M = 14.0, SD = 2.6). While this interval is relatively short, it nevertheless: 1) maps on to the current standard of care in clinical neuropsychological practice; 2) is scientifically justified based on the extant literature, which shows that central nervous system changes can be detected in HIV over this time period (e.g., Chang et al., 2008; Sheppard et al., 2015; Tierney, Woods, Sheppard, & Ellis., 2019); and 3) represents a notable methodological advance over existing cross-sectional research on aging and PM. This study focuses on the longitudinal findings from this cohort, whose baseline PM functioning was detailed in Avci et al. (2016); note that, there is also overlap between the sample described here and the sample described in Sheppard et al. (2015). The present sample is derived from a larger sample of 373 participants who were initially recruited and tested at baseline. A total of 176 participants were lost to follow-up. The 183 retained participants were younger (p<.001) and had higher rates of lifetime Major Depressive Disorders (p=.032) relative to those who were lost. The retained and lost participants were comparable across HIV serostatus, education level, estimated IQ, ethnic/racial composition, lifetime rates of substance dependence and anxiety disorders, and current affective distress (ps> .05). Interestingly, even when controlling for age, the retained participants had poorer baseline time-based PM (p=.003, d=.31) and event-based PM (p=.013, d=.28) as measured by the research version of the Memory for Intentions Test (MIsT; Woods et al., 2008b; Raskin, 2009). However, the retained participants had better performance on the 24-hour naturalistic trial on the MIsT (i.e., naturalistic PM), than individuals who were lost at follow-up, even when controlling for clinicodemographic variables (odds ratio: 1.66 [1.05–2.63], p= .030). Still, the retained and lost participants reported comparable levels of PM and RM symptoms on the Prospective and Retrospective Memory Questionnaire (Smith, Della Sala, Logie, & Maylor, 2000; ps> .05).

Prospective Memory

Three aspects of PM were measured using well-validated assessments: viz., laboratory-based performance, naturalistic performance, and self-reported symptoms.

Laboratory-based PM.

Laboratory-based PM performance was assessed with the research version (Woods et al., 2008b) of the Memory for Intentions Test (MIsT; Raskin, Buckheit, & Sherrod, 2010). This 30-minute measure includes four time-based PM trials and four event-based PM trials that are completed in the context of an ongoing word-search puzzle. The time- and event-based scales are balanced in terms of delay interval (e.g., 2 or 15 min) and response modality (e.g., verbal or action). Each trial is worth two possible points: one point is awarded for a correct response and one point is awarded for responding at the appropriate time or to the appropriate event-based cue. Total scores were generated for event-based and time-based PM performance subscales. Scores for each subscale ranged from 0–8. Participants were administered an alternate form of the MIsT during their follow-up evaluation. This alternate research form was identical in structure and format to the form administered on baseline assessment, but differed in content for the word searches, the time-based intentions, and the event-based cues and intentions. For example, one event-based command on the standard version of the MIsT is, “When I show you a red pen, sign your name on the paper,” whereas the comparable item on the alternate form is, “When I show you a green pen, write today’s date on the paper.” One time-based command on the standard form is, “In 2 minutes, ask me what time this session ends today,” whereas a comparable item on the alternate form is, “In 2 minutes, tell me a time of day when I can call you tomorrow.”

Naturalistic PM.

A naturalistic 24-hour probe was also administered in which participants were instructed to leave a telephone message for the examiner reporting the number of hours slept the night after the assessment. Participants were considered to have “passed” if they called the examiner, regardless of whether they called at the correct time or left the correct message. They were considered to have “failed” if they did not call. Thus, performance on the naturalistic PM task was evaluated as a dichotomous outcome. The same naturalistic PM task was administered at the baseline and follow-up examinations.

Self-reported PM.

Self-reported symptoms of PM were measured using the Prospective and Retrospective Memory Questionnaire (PRMQ), which is a 16-item questionnaire that assesses the frequency of everyday memory-related symptoms in daily life (Smith et al., 2000). It consists of 8 PM items and 8 retrospective memory items that are rated on a 5-point Likert-type scale that ranges from 1 (“never”) to 5 (“often”). Scores on the PRMQ PM or RM subscales range from 8–40. Participants completed the same version of the PRMQ at both evaluations.

Neurocognitive Evaluation

The neurocognitive evaluation included an estimate of verbal IQ (i.e., WTAR) alongside a comprehensive neurocognitive test battery designed to assess the domains most commonly impacted in HIV. In accordance with the Frascati research criteria (Antinori et al., 2007), the full test battery included measures of executive functions, attention/working memory, episodic learning, memory, information processing speed, and motor skills (see Sheppard et al., 2015 for full details). For this study, we only present data on the delayed memory and executive functions domains, which tend to show the strongest conceptual (e.g., McDaniel & Einstein, 2000) and statistical associations (e.g., Gupta et al., 2010) with PM. Delayed memory was measured using the unit score of the Logical Memory II subtest from the Wechsler Memory Scale, 3rd edition (WMS-III; Wechsler, 1997) and Long Delay Free Recall of the California Verbal Learning Test 2nd Edition (CVLT-II; Delis, Kramer, Kaplan, & Ober, 2000). Executive functions were measured using the Trail making Test, Part B time (Army Individual Test Battery, 1944) and the Total Moves score from the Tower of London Test (Drexel Version; Culbertson & Zillmer, 1999). The alternate form of the CVLT-II was administered at the follow-up assessment. For all other tests, the same version was given at both the baseline and the follow-up assessment. Raw scores on each individual test were converted to sample-based z-scores, which were then averaged to create domain-based z-scores.

Psychiatric Evaluation

Current (i.e., within the last 30 days) and lifetime major depressive, anxiety, and substance use disorders were determined using the Composite International Diagnostic Interview (CIDI, version 2.1, World Health Organization, 1998). The CIDI is a comprehensive, fully structured lay-administered interview that assesses the presence of mental disorders in accordance with the diagnostic criteria of the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (American Psychiatric Association, 1994). Acute affective distress was measured with the Profile of Mood States (POMS; McNair, Lorr, & Droppleman, 1981). The POMS is a 65-item, self-report measure that asks participants to rate various adjectives on a 5-point Likert scale which ranges from 0 (“not at all”) to 4 (“extremely”) based on their experience over the week prior to evaluation. The six subscales measure tension/anxiety, depression/dejection, anger/hostility, vigor/activity, fatigue/inertia, and confusion/bewilderment. For the purposes of this study, we utilized the total mood disturbance score.

Medical Evaluation

The neuromedical evaluation was completed by research nurses and consisted of a blood draw, review of current medications, and thorough assessment of comorbid health conditions such as hepatitis C virus (HCV) infection. For HIV+ participants, nadir CD4 count, AIDS diagnosis, and estimated duration of infection were derived from interviews.

Data Analyses

Baseline between-group differences in health and demographic characteristics were assessed using analysis of variance (ANOVA) for continuous dependent variables and chi square tests for categorical variables. Our primary hypotheses for the MIsT, PRMQ, and standard neurocognitive variables were tested with a mixed-model ANOVA with age group and HIV disease status as between-subjects factors and cognitive scores at baseline and follow-up as within-subjects factors.

Covariates were included in analyses to increase confidence that any observed findings regarding the effects of HIV and aging on PM were not exclusively an artifact of any natural and expected group differences. That is, our goal in selecting covariates was to determine whether age, HIV, and their interaction are related to PM and related cognitive functions once the effects of potentially confounding variables were explained. The assumption of linearity was determined by examining the correlation and p value of the pairwise correlations and by visual inspection of the scatter plot. The assumption of parallel slopes was determined by examination of the primary outcomes with and without the addition of the covariates. Covariates were selected from the variables listed in Table 1 based on the following criteria: 1) they differed significantly between the four study groups; and 2) they were related to the variables of interest at either the baseline or follow-up assessment in the entire cohort. This process was repeated for each dependent variable which resulted in a different set of covariates for nearly each outcome variable.

Table 1.

Demographic and Clinical Characteristics of the Study Groups.

Younger HIV − (n = 27) Older HIV − (n = 44) Younger HIV + (n = 35) Older HIV + (n = 77) p Group Differences
Age (years) 30.0 (6.5) 56.0 (4.8) 32.3 (5.2) 56.4 (5.9) <.0001 Y−, Y+ < O−, O+
Education (years) 13.5 (1.8) 14.5 (2.3) 12.6 (1.5) 14.4 (2.5) .0003 Y+ < O+, O−
Ethnicity (% white) 40.7 70.5 45.7 66.2 .016 Y−, Y+ < O−, O+
Gender (% men) 63.0 68.2 82.9 85.7 .032 Y−, O− < Y+, O+
Estimated Verbal IQ (WTAR) 102.2 (10.1) 104.9 (9.9) 99.5 (11.4) 102.0 (10.7) .212 --
POMS Total Score (out of 200) 45.7 (22.5) 45.7 (29.2) 51.8 (39.9) 58.4 (35.3) .156 --
Generalized Anxiety
 Disordera (%) 3.7 4.5 11.4 20.8 .019 Y−, O− < Y+, O+
Major Depressive
 Disordera (%) 48.1 50.0 60.0 61.0 .506 --
Substance Dependencea (%) 51.9 59.1 48.6 49.4 .735 --
Hepatitis C Virus (%) 3.7 15.9 5.7 33.8 .0001 Y−, Y+, O− < O+
HIV Duration (months) - - 88.6 (66.5) 202.2 (87.9) <.0001 Y+ < O+
AIDS (%) - - 37.1 63.6 .009 Y+ < O+
CD4 Count (cells/μL) - - 552.7 (241.6) 580.8 (309.9) .772 --
Nadir CD4 (cells/μL) - - 260.5 (182.3) 178.4 (159.0) .017 O+ < Y+
Prescribed cART Status (%) - - 85.7 90.9 .402 --
RNA in Plasma Detectable (%) - - 31.3 19.7 .204 --
 Among Subjects on cART - - 18.5 14.5 .630 --
Global Deficit Score 0.2 (0.2) 0.2 (0.3) 0.4 (0.5) 0.4 (0.4) .001 Y−, O− <O+
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Note. Data represents M (SD) or %. Younger <50 years; Older ≥ 50 years; WTAR = Wechsler Test of Adult Reading; HCV = Hepatitis C Virus; AIDS = Acquired Immune Deficiency Syndrome; CD4 = Cluster of Differentiation 4; cART = combination antiretroviral therapy; Global Deficit Score is a summary measure of neurocognitive functioning based on clinical, demographically-adjusted tests, whereby higher scores represent greater levels of neurocognitive impairment

Significant effects were further analyzed using univariate ANOVAs. Interactions were probed with planned paired-samples or independent-samples t-tests. The partial eta squared (ηp2) statistics and Cohen’s d statistic were included as estimates of effect size. The McNemar’s test statistic was generated to evaluate group effects of naturalistic PM performance over time. To assess potential group effects that would modulate any observed null findings, we classified individuals on their change status on the naturalistic PM task over 14 months and assessed group differences. We then conducted a nominal logistic regression, regressing the change variable on age group, HIV serostatus, the interaction term, and any relevant covariates. The critical alpha was set to .05 for all analyses. All analyses were conducted using JMP Pro software package (version 13.1.0) and SPSS (IBM SPSS Statistics version 26).

Results

Effects of Age, HIV, and Time on PM

Laboratory-based PM

Education was the only variable that met criteria for inclusion as a covariate in the analyses of time-based PM. Results (see Figure 1) showed a main effect of age group (F(1,178)=40.1, p<.0001) such that Older persons performed significantly below Younger persons (p<.001, ηp2=.18) on time-based PM. There was also a main effect of HIV status (F(1,178)=8.9, p=.003, ηp2=.050), such that the HIV+ persons performed significantly below HIV- persons (p<.001) on time-based PM. Education also significantly contributed to the model (F(1,178) = 15.53, p=.001, ηp2=.087). There was no effect of the HIV × age interaction term (F(1,178)=0.109, p=.74, ηp2=.001). The effect of time on time-based PM was small and non-significant (F(1,178)=.37, p=.82, d=.17).

Figure 1.

Figure 1.

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Time- and event-based Prospective Memory (PM) scores on the Memory for Intentions Test (MIsT) at baseline and 14-month follow-up across study groups.

Sex was included as a covariate for the analyses of event-based PM. Results (see Figure 1) showed a main effect of age (F(1,178)=14.99, p=.0002, ηp2=.079) such that Older persons performed worse than Younger persons (p<.001) on event-based PM. There was a main effect of serostatus (F(1,178)=4.11, p=.044, ηp2=.028) with HIV+ persons performing worse than HIV- persons (p=.015) on event-based PM. There was no effect of the HIV × age interaction (F(1,178)=0.72, p=.398, ηp2=.006) or sex (F(1,178) = 1.43, p=.234, ηp2=.014) in this model. The effect of time on event-based PM was small and non-significant (F(1,178)=1.84, p=.177, d=.09).

Naturalistic PM

Results of longitudinal analyses revealed no effect of naturalistic PM performance over the 14-month follow-up (χ2 = 2.96, p=.085; Figure 2). Sixty-nine percent of participants had stable naturalistic PM performance, 19% improved and 12% declined. These 3-level change groups did not differ on ethnicity/race, sex, lifetime GAD, education, or HCV infection (ps>.05). Thus, only age group, serostatus group, and their interaction were included in a nominal logistic model predicting naturalistic PM change. The overall model was not significant (χ2 =3.24, p=.77) and no variables emerged as a significant individual predictor (ps > .20, likelihood ratio χ2 range 0.72 – 0.99).

Figure 2.

Figure 2.

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Frequency of participants who “passed” the 24-hour semi-naturalistic Prospective Memory (PM) task at baseline and 14-month follow-up across study groups

Self-Reported PM Symptoms

Education, lifetime history of GAD, and HCV infection were included as covariates in the analyses of the PRMQ PM scale. Results (see Figure 2) showed null effects of HIV (F(1,173) = 1.30, p=.256, ηp2=.016) and age (F(1,173)=0.58, p=.445, ηp2=.006). However, the HIV × age interaction term was significant (F(1,173)=4.57, p=.039, ηp2=.034), such that, irrespective of time, Older HIV+ persons reported more PM symptoms than Younger HIV+ (p=.002, Cohen’s d = .58), Younger HIV- (p=.021, d = .59), and Older HIV- (p=.002, d=.69) persons. Lifetime diagnoses of GAD (F(1,173) = 7.16, p=.008, ηp2=.046) and HCV infection (F(1,173)= 13.31, p=.003, ηp2=.046) were also significant predictors of higher PM symptoms. There was no effect of education (F(1,173)= 2.56 p=.113, ηp2=.019) in the PM symptoms model. Time was also not significant and the effect was very small (F(1,173)=.129, p=.719, d=.010; Figure 3).

Figure 3.

Figure 3.

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Prospective and retrospective memory symptoms reported on the Prospective and Retrospective Memory Questionnaire (PRMQ) at baseline and 14-month follow-up across study groups.

Effects of Age, HIV, and Time on Other Neurocognitive Functions.

Retrospective Memory (RM)

Education, sex, and HCV infection were included as covariates in the analysis of retrospective memory performance. Figure 4 shows that there was a main effect of HIV on retrospective memory performance (F(1,175)=6.91, p=.009, ηp2=.041) such that HIV+ persons had lower performance than HIV- persons (p<.001). There was also a main effect of age on retrospective memory performance (F(1,175)=10.06, p=.0018, ηp2=.062) such that Older persons performed below Younger persons (p=.04). Higher education (F(1,175)= 26.2, p<.001, ηp2=.132) and female sex (F(1,175)= 6.69, p=.011, ηp2=.037) were also significant predictors of better retrospective memory performance. There was no effect of the HIV × age interaction term (F(1,175)=0.794, p=.374, ηp2=.041) or HCV infection (F(1,175)= 0.139, p=.710, ηp2=.041) in this model. The effect of time was very small and non-significant (F(1,175)=0.375, p=.541, d=.01).

Figure 4.

Figure 4.

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Retrospective memory and executive functions at baseline and 14-month follow-up across study groups.

Self-Reported RM Symptoms

HCV and any lifetime history of GAD were included as covariates in the model predicting the PRMQ RM scale. Figure 3 (above) shows there were no significant effects of age (F(1,166)=2.01, p=.194, ηp2=.014), HIV (F(1,166) = 2.22, p=.138, ηp2=.019), their interaction (F(1,166)=2.28, p=.133, ηp2=.031), or lifetime presence of GAD (F(1,166)=.85, p=.35, ηp2=.013) on RM symptoms. The effect of time was small and non-significant (F(1,166)=.335, p=.564, d=.11). HCV infection emerged as the sole significant predictor of the PRMQ RM scale in this model (F(1,166)=126, p<.001, ηp2=.078).

Executive Functions

Education, ethnicity/race, and HCV infection were included as covariates in the analyses of executive functions. Figure 4 shows a main effect of serostatus F(1,172)=4.26, p=.025) such that HIV+ persons had poorer performance on tests of executive functioning than HIV- persons (p=.006). There was also a main effect of age on executive functions (F(1,172)=12.72, p=.0005, ηp2=.070) such that Older persons performed below Younger persons (p=.02). Education also emerged as a significant predictor in this model (F(1,172) = 16.824, p<.0001, ηp2=.090). The HIV × age interaction term (F(1,172)=.729, p=.395, ηp2=.004) was non-significant and there were no main effects of ethnicity/race (F(1,172)= 3.00, p=.085, ηp2=.041) or HCV infection (F(1, 172)=.127, p=.722, ηp2=.018) on executive functions. The effect of time was very small and non-significant (F(1,172)=.0019, p=.966, d=.04).

Discussion

PM plays a significant role in activities of daily living (e.g., Tierney, Bucks, Weinborn, Hodgson, & Woods, 2016) and health behaviors (Woods et al., 2008a), but we know very little about its trajectory in neuropsychological populations who suffer from deficits in this aspect of everyday memory. The current study investigated this important question in the setting of aging and HIV disease, both of which are associated with mild-to-moderate PM deficits in cross-sectional studies (Henry et al., 2004; Avci et al., 2016), but for whom little is known about the trajectories of impairment. We observed a similar stability of performance-based measures of PM, RM, and executive functions over a 14-month follow-up period across all groups. Notably, these patterns were present even when controlling for important cofactors such as years of education, sex, ethnicity/race, anxiety, and HCV, which have all been linked to neurocognition, but do not appear to be serious confounding factors in this sample. While interaction effects were not present, important independent and additive main effects were observed in this sample and are consistent with other studies from our group on PM (e.g., Woods et al., 2010; Avci et al., 2016), as well as general neurocognition and neuroimaging (e.g., Thomas et al., 2013). However, replication studies are needed in different samples since covariate analyses may not adequately control group differences and may in fact under-correct in diverse samples that are not fully matched on clinicodemographic factors (Adams, Brown, & Grant, 1985). Nevertheless, the primary findings with regard to age, HIV, and time on different aspects of PM remained consistent when these covariates were removed from the above-detailed statistical models.

Consistent with prior work (e.g. Avci et al., 2016), we also observed main effects of HIV and aging on both laboratory and self-reported symptoms of PM, with mildly larger-sized effects on strategically demanding PM tasks (i.e., time-based PM). In parallel, we also observed main effects of HIV and age on standard clinical measures of RM and executive functions, which are thought to support PM (McDaniel & Einstein, 2000) and are affected in both HIV and aging (Walker & Brown, 2018; Carey et al., 2006, Morgan et al., 2012; Zogg et al., 2012, Kliegel, Jäger, Phillips, 2008). Furthermore, this finding supports the Multiprocess Model of PM (McDaniel & Einstein, 2000) by demonstrating the parallels between PM and the cognitive domains that recruit heavily from the frontostriatal circuitry as well as the relative effects of age and HIV on each domain.

This study extends that literature by demonstrating that the PM deficits that are associated with HIV and aging are stable over one year. That is, we observed no meaningful group-level changes in PM performance using an alternate form version of a well-validated PM test. Contrary to our expectations, stability in PM was evident and comparable across age and HIV serostatus groups. This finding is consistent with prior longitudinal studies in HIV demonstrating that 60% of individuals with HIV evidence stable neurocognitive functioning over 1–3 years (Heaton et al., 2010). Our findings are somewhat inconsistent with Serrani (2010), who showed a decline in both time- and event-based PM over time in sample of elderly Argentinian adults. However, our sample was followed for a shorter period (i.e., 14 months versus 5–10 years), and our older groups were markedly younger than the participants described by Serrani (2010). These differences suggest that 14 months may not be a long enough period to detect subtle changes in PM performance, even in the more strategically demanding time-based PM task, where one might suspect declines would be observed. However, studies have also consistently shown that nearly a quarter of HIV+ individuals show incident decline in cognitive functioning (Cysique et al., 2010; Heaton et al., 2015) and that declining cognition is associated with symptomatic baseline neurocognitive impairment (Heaton et al., 2015), older age, AIDS, lower nadir CD4 and more plasma detectable virus (Cysique et al., 2010). Thus, one possible reason that no changes in laboratory tasks of PM were observed is that our sample was relatively healthier than those previously studied. In fact, our HIV+ sample had low rates of detectable plasma RNA (23%) and syndromic neurocognitive impairment (16%; e.g., Antinori et al., 2007).

Similar levels of stability were observed for self-reported PM symptoms. Across time points, Older HIV+ adults perceived the highest levels of PM, but not RM, failures in their daily lives. As with laboratory-based PM performance, these detrimental effects of aging and HIV on PM symptoms were independent of relevant co-factors (e.g., education, anxiety, and HCV) and remained fairly consistent over the one-year test-retest interval. This finding is consistent with the stability of PM complaints over one year observed in healthy adults (Mäntylä, 2003), and this is the first study to demonstrate the stability of PM symptoms in HIV disease. This is important because prior studies show that PM complaints are elevated in HIV disease (e.g., Woods et al., 2007; Avci et al., 2016; Sheppard, Woods, Massman, & Gilbert., 2019) and are strong, independent predictors of activities of daily living and health-related quality of life (e.g., Doyle et al., 2013).

In our sample, there were no differences in depressive symptoms across groups (see Table 1), thus the observed declines were similarly independent of depressive symptoms. While both performance-based and self-report measures of PM have been linked to ADL dependence such that more complaints of PM are associated with greater dependence (Woods et al., 2008a), the results suggest that subjective complaints of PM in older HIV+ adults may be susceptible to additive effects of age and HIV disease before such effects are observed on performance-based PM measures (Weber et al., 2011; Woods et al., 2010). Although complaints are commonly dismissed due to their limited correspondence to laboratory-based tests of ability (e.g., Woods et al., 2007), they nevertheless are commonly queried and integrated into diagnostic assessments. For example, Tierney et al. (2017) found that the inclusion of a subjective cognitive complaint enhanced sensitivity of the DSM-5 diagnostic criteria for an HIV-related neurocognitive disorder. More recently, Sheppard et al. (2019) found higher rates of subjective cognitive impairment in HIV+ individuals, which are self-perceived cognitive declines that can precede the onset of objective deficits. Although cognitive complaints do not always map onto objective test performance in HIV+ samples, as was the case in the current study, they may nevertheless serve as an important risk factor for later decline observed perhaps beyond a one-year interval. Subjective cognitive impairment is thought to represent a transitional phase between age-appropriate cognitive functioning and pathological decline (Matthews et al., 2008). While little is known about the role of PM in the pathway from normal cognition to HAND, it is possible that complaints about cognition, particularly on tasks that can recruit several neural networks (e.g., PM tasks), may be a sensitive and meaningful marker for further cognitive decline.

Although PM complaints represent an individual’s perception to complete tasks involving PM in everyday life, and changes were observed in older HIV+ adults, we did not observe a worsening of performance on the naturalistic PM task in any group. We did, however, observe age-related effects on naturalistic PM performance cross-sectionally, such that older HIV- adults evidenced the highest success rate on the naturalistic task among the groups (X2=9.62, p=.0215) though only at the baseline assessment (Figure 2). This finding is consistent with previous reports showing a benefit of age on naturalistic PM task performance among older adults (i.e., the aging-PM paradox, Weber et al., 2011). As noted above, the individuals who failed the naturalistic task at the baseline assessment were 1.6 times more likely to drop out of the study by follow-up despite the fact that they demonstrated better laboratory-based PM scores and lower levels of global neurocognitive impairment. The reasons for drop out are unknown but could have been due to lack of motivation, low conscientiousness, lack of compensatory strategies, or some combination of these factors (Schnitzspahn, Ihle, Henry, Rendell, & Kliegel, 2011). Nevertheless, similar to the pattern observed on the other performance-based measures, performance on the naturalistic task was stable over a 14-month period within the remaining sample of participants.

The current study is not without its limitations. As noted above, the 14-month period between baseline and follow-up may have limited the sensitivity to detect subtle changes in PM functioning. However, changes in neuroimaging and biomarkers (Chang et al., 2008), incident HAND (odds ratio: 4.6; Sheppard et al., 2015) and incident neuromotor signs (odds ratio: 3.6; Tierney et al., 2019) have been observed in HIV over comparably short follow-up periods, which lends support to the use of a one-year follow-up period. Nevertheless, studies with longer follow-up intervals and multiple time-points are clearly needed to determine the trajectory of PM in HIV. Additionally, the attrition rate of the current sample (47%) is quite high, even compared to other longitudinal studies in HIV (e.g., Cattie et al., 2015), which may have limited the variability in PM performance and the generalizability of the findings. Indeed, our attrition analyses indicated that the individuals who were lost to follow-up were older, had poorer naturalistic PM, and had better laboratory-based PM than those who were retained. It is possible that this critical subset of older adults who had higher laboratory PM at baseline were driving the age-related declines in time and event-based PM that are observed in other longitudinal studies (Serrani, 2010). As such, these data should be interpreted cautiously. Additionally, practice effects on tests, particularly on those without an alternate form available, may have been a confounding factor, although the full factorial study design helps to mitigate that concern somewhat. Lastly, the purpose of the current study was to identify age and HIV effects over time at a group level. It may be that a clinically and functionally (e.g., Woods et al., 2008) meaningful decline is occurring in a subset of participants in the present study, which the current study design was not able to detect.

Despite these weaknesses, the study has several strengths. One notable strength is our comprehensive measurement of PM using three different methods (i.e., performance-based, self-report, and naturalistic tasks), which all have relative advantages and disadvantages (e.g., Laverick et al., 2017; Woods et al., 2004). Yet, despite the differences between the approaches, a consistent pattern of stability in PM emerged in the present sample which makes it unlikely that the null findings were due to measurement error or biases. Future studies of longitudinal PM should assess for clinically meaningful change in laboratory-measured, naturalistic, and self-report of PM performance.

The current study provides important insights into the short-term stability of PM and supports the additive effects of aging and HIV on this complex cognitive function. Consistent with other work (e.g., Thomas et al., 2013), we observe that age and HIV confer additive risk on PM and related constructs but remain stable over the course of one year. The reasons for the observed stability are unclear but may be due to the contribution of protective factors such as cognitive reserve (e.g, Sheppard et al., 2015) or advancements in cART and improved management of CD4 and viral load (e.g., Cysique et al., 2009). The present findings have important clinical implications for short term treatment planning of patients with HIV disease and for the study of the trajectory of PM in HIV disease. The observed stability suggests that drastic improvements or declines in PM over a typical one-year follow-up are unlikely in the setting of stable HIV disease and typical aging. For HIV+ individuals with impaired PM, this may bolster the need for ongoing support in the form of compensatory strategies to aid with critical health behaviors (e.g., treatment adherence, appointment attendance) and other ADLs (e.g., shopping, financial management). Future studies should aim to expand the observation period to better elucidate the trajectory in HIV disease and understand the role of age and important clinical and demographic factors in PM.

Acknowledgements:

We are grateful to Marizela Verduzco for study coordination, Dr. Scott Letendre for overseeing the neuromedical aspects of the parent project, Dr. J. Hampton Atkinson and Jennifer Marquie Beck for participant recruitment, and Donald R. Franklin, Stephanie Corkran, for data processing.

Footnotes

Disclosure of interest: The authors declare that they have no conflict of interest. This research was supported by grants R01-MH073419 and P30-MH62512 from the National Institutes of Health. 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 United States Government.

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