Screening for HIV-Associated Neurocognitive Disorders: Sensitivity and Specificity

Robbins, Reuben N.; Scott, Travis M.; Gouse, Hetta; Marcotte, Thomas D.; Rourke, Sean B.

doi:10.1007/7854_2019_117

Neurocognitive Complications of HIV-Infection pp 429-478 | Cite as

Screening for HIV-Associated Neurocognitive Disorders: Sensitivity and Specificity

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Authors and affiliations

Reuben N. Robbins
Travis M. Scott
Hetta Gouse
Thomas D. Marcotte
Sean B. Rourke

Chapter

First Online: 17 July 2020

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Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 50)

Abstract

HIV-associated neurocognitive disorder (HAND) remains prevalent among people living with HIV (PLWH), especially the mild forms, even those with well-controlled HIV. Recommendations from the literature suggest routine and regular screening for HAND to detect it early and manage it effectively and adjust treatments, if warranted, when present. However, screening for HAND is not routinely done, as there are no current guidelines on when to screen and which test or tests to use. Furthermore, many of the available screening tools for HAND often cannot accurately detect the mild forms of HAND and require highly trained healthcare professionals to administer and score the tests, a requirement that is not feasible for those low- and middle-income countries with the highest HIV incidence and prevalence rates. The purpose of this chapter was to review recent research on screening tests to detect HAND and report on the strengths, limitations, and psychometric properties of those tests to detect HAND.

Keywords

HAND HIV Neurocognitive impairment Psychometrics Screening Test

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Appendix

Table 2

Neuropsychological tests used in each study by cognitive domain

Study	Premorbid ability	Motor/fine motor	Attention/working memory	Psychomotor speed/reaction time	Learning and memory	Executive function	Language	Visuo-construction
Chalermchai et al. (2013)		GP FT		TMTA CT1 Coding, SS	BVMT AVLT	CT2 First names fluency	SemFl	Block design
Sakamoto et al. (2013)		GP	LNS PASAT	TMTA Coding SS	SMLT FMLT	WCST LetFl TMTB	SemFl
Moore et al. (2012)		GP	PASAT Digits	TMTA Coding SS Stroop Color	HVLT BVMT	Stroop CWT WCST LetFl ActFl TMTB	SemFl
Becker et al. (2011)				X	^aX	X	X	X
Joska et al. (2011)		FT GP		Coding CT1 TMTA	BVMT HVLT	CT2 CWT MAT MCT WCST
Levine et al. (2011)		GP	LNS PASAT	Coding SS	BVMT HVLT	CWT TMTB LetFl WSCT
Simioni et al. (2010)	NART		Digits SpWM	RT TMTA VIP		TMTB
Skinner et al. (2009)		GP		^bCalCAP SDMT TMTA		TMTB
Morgan et al. (2008)		GP	LNS PASAT	Coding SS TMTA	BVMT HVLT	TMTB LetFl WCST
Singh et al. (2008)			Digits	TMTA		TMTB		RCFT copy
Bottiggi et al. (2007)	NART	FO GP TG	Ruff 2 and 7 Seq RT	SDMT TMTA	FMLT RAVLT	CWT TMTB LetFl
Wojna et al. (2007)		GP		SDMT, TMTA VCRT	RAVLT	CWT TMTB
Cysique et al. (2006)		GP	Digit span	SDMT TMTA	CVLT RCFT 3 min	Similarities TMTB LetFl	BNT SemFl	RCFT copy
Ellis et al. (2005)	Vocabulary	TG GP	PASAT	SS	HVLT
Richardson et al. (2005)		GP	Digit span	^bCalCAP TMTA	RAVLT	CWT TMTB		RCFT copy
Sacktor et al. (2005) (American)		GP		^bCalCAP SDMT	RAVLT	Odd man out LetFl		RCFT copy
Sacktor et al. (2005) (Ugandan)		GP TG	Digit span	CT1 SDMT	VLT	CT2
Carey et al. (2004)		GP	LNS PASAT	Coding SS TMTA	BVMT HVLT	CWT HCT TMTB LetFl WCST	SemFl
Gonzalez et al. (2003)		GP	Digit span PASAT VisSp	CT1 SDMT TMTA	RAVLT	CT2 CWT HCT TMTB LetFl		Block design
Smith et al. (2003)		GP	LNS	bCalCAP CT1	CVLT Faces	CT2 CWT

NART national adult reading test, GP grooved pegboard, FT finger tapping, FO finger oscillation, TG timed gait, LNS letter number sequencing; PASAT paced auditory serial addition test, SpWM spatial working memory, CANTAB, SeqRT sequential reaction time, CalCAP, VisSp visual span, TMTA trial making test A, CT1 color trails test 1, SS symbol search, SDMT symbol digit modalities test, RT reaction time, CANTAB, VIP visual information processing, CANTAB, VCRT visual choice reaction time, HVLT hopkins verbal learning test, BVMT brief visuo-spatial memory test, SMLT story memory learning test, FMLT figure memory learning test, RAVLT rey auditory verbal learning test, CVLT california verbal learning test, RCFT 3 min rey complex figure test, 3 min delay, VLT World Health Organisation/University of California verbal learning test, MAT mental alternation test, MCT mental control test, CT2 color trails 2, CWT stroop color word interference test, WCST Wisconsin card sort test, LetFl letter fluency, TMTB trail making test B, HCT halstead category test, SemFl semantic fluency, BNT boston naming test, RCFT copy rey complex figure test copy

“X” test not specified

^aVerbal and visuo-spatial learning and memory

^bIndividual tests not specified, assumed that the whole battery was administered

Table 3

Screen versus gold standard NP impairment rates and standard criterion validity indexes across studies (%)

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See reference list for numbered studies. Rounded to nearest whole value. Ordered with balance of highest sensitivity and specificity. Studies with ≥70% sensitivity and specificity are bold. Studies ≤ 70% sensitivity and specificity are in gray. Values are based on standard cut-off scores unless otherwise stated. Values represent percentages unless otherwise stated and are to the nearest decimal reported. NP neuropsychology, IR impairment rate, PPP positive predictive power, NPP negative predictive power, Acc classification accuracy, AUC area under the curve, – not reported. Sensitivity refers to the proportion of individuals identified as impaired on both the gold standard and the screen. Specificity refers to the proportion of individuals identified as unimpaired on both the gold standard and the screen. PPP relates to specificity and is defined as the probability that an individual has HAND given their positive screen result. NPP relates to sensitivity and is the probability that an individual does not have HAND given their negative screen result.

^aProportion

^bManually calculated

^cValues reported

^dBased on test scores only

^eBased on a cut-off score of 12 or less

^f“Any neurocognitive impairment”

^gSample excluded ANI category

Table 4

Screen versus gold standard NP impairment rates and standard criterion validity indexes for studies where sensitivity and specificity are 70% or higher (%)

Study	Screen	NP IR	Screen IR	Cut-off	Sample	Sensitivity	Specificity	Accuracy
Morgan et al. (2008)	HDS	43^a	–	T<40	HAD only	93	73	–
Moore et al. (2012)	4 NP tests	19^b	–	4 tests T < 40, or 2 tests T < 40 + 1 test T < 35, or 2 tests T < 35, or 1 test T < 40 + 1 test T< 30, or 1 test T < 25	Entire sample	87	87	–
Moore et al. (2012)	3 NP tests	19^b	–	3 tests T < 40 or 1 test T < 40 + 1 test T < 35, or 1 test T < 30	Entire sample	87	76	–
Cysique et al. 2012	CogState	62^a	62^a	–	Entire sample	81	70	–
Carey et al. (2004)	NP tests (HVLT-R and ndGP)	29^a	34^a	T<40 on 1 test or T<35 on 2 tests	Entire sample	78	85	83
Morgan et al. (2008)	HDS	43^a	–	T<40	MND only	77	73	–
Carey et al. (2004)	NP tests (HVLT-R and Cod)	29^a	–	T<40 on 1 test or T<35 on 2 tests	Entire sample	75	92	87
Moore et al. (2012)	2 NP tests	19^b	–	2 tests T < 40 or 1 test T ≤ 35	Entire sample	73	83	–
Sacktor et al. (2005) (American)	IHDS	38^a	–	≤10.5	Entire sample	71	79	–
Becker et al. (2011)	CAMCI	31^a	30^b	–	Entire sample^c	72	98	–

Consideration of the sample in question is needed for the proper selection of the screen. See reference list for numbered studies. Rounded to nearest whole value. Ordered with balance of highest sensitivity and specificity. NP neuropsychology, IR impairment rate, Accuracy overall correct classification accuracy, – not reported. Sub-sample refers to the subset of the overall sample upon which criterion validity indexes were calculated. Sensitivity refers to the proportion of individuals identified as impaired on both the gold standard and the screen. Specificity refers to the proportion of individuals identified as unimpaired on both the gold standard and the screen. HAD HIV-associated dementia, MND mild neurocognitive disorder, HVLR-R Hopkins verbal learning test, revised, ndGP nondominant hand grooved pegboard, Cod coding

^aManually calculated

^bValues reported

^cSample excluded ANI category

Table 5

Characteristics of studies on brief screening tools for HIV-associated neurocognitive disorders

Author, date; location	Design	Recruitment method	Participants (mean age; mean years education; percent male)	Tools examined
Becker et al. (2011); USA	Cross-sectional	Convenience sampling	Age: 51 (HIV+); 51 (HIV−) Education: 15 (HIV+); 15 (HIV−) Male: 96% (HIV+); 78% (HIV−)	The computer assessment of mild cognitive impairment (CAMCI)
Bottiggi et al. (2007); Kentucky, USA	Cross-sectional	Convenience sampling	Age: 39 Education: 14 Male: 87%	HIV dementia scale
Carey et al. (2004); San Diego, USA	Cross-sectional	Convenience sampling	Age: 41 Education: 14 Male: 84%	Hopkins verbal learning test revised and grooved pegboard test nondominant hand (PND) pair; Hopkins verbal learning test revised and WAIS-III digit symbol (DS) subtest pair; HIV dementia scale
Cysique et al. (2006); Sydney, Australia	Cross-sectional	Random sampling	Age: 47 (Advanced HIV); 48 (ADC); 49 (HIV−) Education: 14 (Advanced HIV); 14 (ADC); 15 (HIV−) Male: 98% (Advanced HIV); 100% (ADC); 100% (HIV−)	CogState
Cysique et al. (2010); Sydney, Australia	Cross-sectional	Convenience sampling	Age: 49 (HIV+); 47 (HIV−) Education: 14 (HIV+); 15 (HIV−) Male: 100% (HIV+); 100% (HIV−)	Screening algorithm
Ellis et al. (2005); 15 sites, USA	Cross-sectional	Convenience sampling	Age: 44 Education: 14 Male: 86%	The NeuroScreen – brief neurocognitive screen (BNCS) and brief peripheral neuropathy screen (BPNS)
Fogel (1991); USA	Cross-sectional	NR	Age: NR Education: NR Male: 92%	Brief Cognitive Screen (BCS) – memory subtest, verbal fluency items, and conflicting stimulus test of the high sensitivity cognitive screen (HSCS)
Ganasen et al. (2008); Western Cape, South Africa	Cross-sectional	Convenience sampling	Age: 34 Education: 10 Male: 26%	HIV dementia scale
Garvey et al. (2009); London, UK	Cross-sectional	Convenience sampling	Age: 48 Education: NR Male: 84%	Prospective and retrospective memory questionnaire (PRMQ)
Gonzalez et al. (2003); USA	Cross-sectional	Not reported	Age: 40 Education: 14 Male: 100%	California computerized assessment package (CalCAP), mini-version
Jones et al. (1993); Baltimore, USA	Cross-sectional	Convenience sampling	Age: NR Education: 13 Male: 79%	Mental alternation test
Joska et al. (2011); Cape Town, South Africa	Cross-sectional	Convenience sampling	Age: 30 (HIV+); 25 (HIV−) Education: 10 (HIV+); 11 (HIV−) Male: 21% (HIV+); 38% (HIV−)	International HIV dementia scale
Knippels et al. (2002); Netherlands and Flanders, Belgium	Cross-sectional	Convenience sampling	Age: 39 Education: NR Male: 100%	Medical outcomes study HIV (MOS-HIV), four-item version in Dutch
Kwasa et al. (2012); Kisumu, Kenya	Cross-sectional	Convenience sampling	Age: 39 Education: NR Male: 57%	HIV dementia diagnostic tool
Lyon et al. (2009); Washington, DC; USA	Cross-sectional	Convenience sampling	Age: 17 (Dementia); 17 (No Dementia) Education: NR Male: 83% (Dementia); 45% (No Dementia)	HIV dementia scale; mini-mental state examination
Maruff et al. (2009); Melbourne, Australia	Cross-sectional	Convenience sampling	Age: 46 (ADC); 47 (controls, AIDS but no ADC or MND) Education: 13 (ADC); 12 (controls, AIDS but no ADC or MND) Male: 89% (ADC); 91% (controls, AIDS but no ADC or MND)	CogState (brief battery)
Minor et al. (2010); USA	Cross-sectional	Convenience sampling	Age: 38 Education: 12 Male: 52%	Coin rotation test
Morgan et al. (2008); San Diego, USA	Cross-sectional	Random sampling	Age: 40 (HIV+); 37 (HIV−) Education: 13 (HIV+); 14 (HIV−) Male: 83% (HIV+); 68% (HIV−)	HIV dementia scale
Muniyandi et al. (2012); Thanjavur, India	Cross-sectional	Convenience sampling	Age: NR Education: NR Male: 61%	Mini-mental state examination (MMSE); Bender gestalt test (BGT); Wechsler memory scale; International HIV dementia scale (IHDS)
Overton et al. (2011); St. Louis, USA	Cross-sectional	Convenience sampling	Age: 40 (median) Education: NR Male: 72%	CogState
Parsons et al. (2007); USA	Cross-sectional	Convenience SAMPLING	Age: 24 Education: 13 Male: 66%	Motor battery (timed gait, grooved pegboard, finger-tapping)
Power et al. (1995); Baltimore, USA	Cross-sectional	Convenience sampling	Age: 42 (HIV−); 37 (Asymptomatic HIV+); 36 (Non-Demented AIDS); 39 (Mildly Demented AIDS); 39 (Severely Demented AIDS) Education: 15 (HIV−); 14 (Asymptomatic HIV+); 14 (Non-Demented AIDS); 14 (Mildly Demented AIDS); 11 (Severely Demented AIDS) Male: 89%	HIV dementia scale; mini-mental state examination; grooved pegboard
Revicki et al. (1998); Baltimore-Washington, USA	Longitudinal	Convenience sampling	Age: 37 Education: NR Male: 66%	4-item cognitive function scale (CF4) from HIV health survey and complete 6-item cognitive function scale (CF6) from medical outcomes study (MOS)
Richardson et al. (2005); Boston Area, USA	Cross-sectional	Convenience sampling	Age: 41 Education: 12 Male: 65%	HIV dementia scale
Robertson et al. (2006); ACTG sites all over the world NYC, Chapel Hill and 42 sites around the world	Cross-sectional	Convenience sampling	Age: 38 (AIDS); 39 (SX); 35 (ASX); 35 (HIV−) Education: 14 (AIDS); 15 (SX); 15 (ASX); 16 (HIV−) Male: 87% (AIDS); 96% (SX); 91% (ASX); 56% (HIV−)	Timed gait test
Sacktor et al. (2005); Baltimore, USA and Uganda	Cross-sectional	Convenience sampling	Age: US HIV+: 43 (no impairment); 44 (subclinical impairment); 47 (mild dementia); 44 (moderate dementia); 49 (severe dementia); Uganda: 37 (HIV+); 31 (HIV−) Education: US HIV+: 14 (no impairment); 13 (subclinical impairment); 13 (mild dementia); 12 (moderate dementia); 13 (severe dementia); Uganda: 9 (HIV+); 10 (HIV−) Male: NR	International HIV dementia scale
Simioni et al. (2010); Geneva, Switzerland	Cross-sectional	Convenience sampling	Age: NR Education: NR Male: 72%	HIV dementia scale
Singh et al. (2008); Durban, South Africa	Cross-sectional	Convenience sampling	Age: 34 (median) Education: NR Male: 40%	International HIV dementia scale
Smith et al. (2003); USA	Cross-sectional	Not reported	Age: 41 (NP normal); 41 (NP abnormal) Education: 14 (NP normal); 13 (NP abnormal) Male: NR	HIV dementia scale
Von Giesen et al. (2005); Dusseldorf, Germany	Cross-sectional	Convenience sampling	Age: 45 (mildly demented); 41 (not demented) Education: NR Male: 100% (mildly demented); 100% (not demented)	HIV dementia scale
Wojna et al. (2007); Puerto Rico, USA	Cross-sectional	Convenience sampling	Age: 36 (HIV+); 34 (HIV−) Education: 12 (HIV+); 13 (HIV−) Male: 0%	HIV dementia scale, Spanish

AAN 2007 HAND Criteria: Asymptomatic Neurocognitive Disorder (ANI): prevalence of 30–35% and characterized by at least mild neurocognitive impairment in two domains but with no evidence of difficulty with day-to-day functioning; Mild Neurocognitive Disorder (MND): prevalence of 20–25% and characterized by at least mild neurocognitive impairment in two domains and with mild interference with day-to-day functioning; and HIV-Associated Dementia (HAD): prevalence of 2–3% with generally moderate to severe impairments in neurocognitive functioning and marked difficulties with everyday functioning [3]

ADC AIDS dementia complex, MND mild neurocognitive disorder, ASX asymptomatic; SX symptomatic, NR not reported

Table 6

Study outcome in literature on screening tools for HIV-associated neurocognitive disorders

Study (author, date; location)	Sample size (total; by group)	Impairment evaluated (type(s); classification system)	Tool characteristics (person can administer; time to administer; materials needed)	Reference test	Reference test details (size of battery; objective assessment; domains assessed; language of administration)	Sensitivity; specificity	Main findings
HIV Dementia Scale (HDS)
Bottiggi et al. (2007); Kentucky, USA	46	Types: MCMD, HAD, neurocognitive deficits or impairment (memory, attention, psychomotor, and construction) Classification: 1991	Person: NR Time: NR Materials: NR	NP battery	Size: large Objective: NR Domains: intelligence, attention/concentration, memory, language, executive functioning, visuo-spatial, speed of processing, motor Language: English	Cut-off<=10: Sensitivity: 0.36 Specificity: 0.94	HDS is not efficient in predicting the presence of subtle and mild HIV Dementia
Carey et al. (2004); San Diego, USA	190	Type: NP impaired and unimpaired Classification: DSM-IV 1994, AAN 1991, Grant and Atkinson 1995	Person: NR Time: 5 min Materials: NR	NP battery	Size: large Objective: NR Domains: intelligence, attention/concentration, memory, language, executive functioning. visuo-spatial, speed of processing, motor Language: English	Cut-off <11: Sensitivity: 0.09 Specificity: 0.98	HDS is less accurate than paired NP test combinations – Hopkins Verbal Learning Test Revised (HVLTR; Total Recall) and the Grooved Pegboard Test nondominant hand (PND) pair, and the HVLTR and WAIS-III Digit Symbol (DS) subtest pair – in classifying HIV+ participants as NP impaired or not
Ganasen et al. (2008); Western Cape, South Africa	474	Type: NP impaired and unimpaired Classification: MMSE used as the gold standard	Person: NR Time: NR Materials: NR	Mini-mental state examination (MMSE)	Size: small Objective: NR Domains: attention/concentration, memory, motor Language: Xhosa, Afrikaans	Cut-off ≤10 Sensitivity: 0.80 Specificity: 0.80	HDS and MMSE were significantly correlated and showed significant agreement. Nonetheless, the HDS identified more participants that demonstrated cognitive impairment than the MMSE. HDS cut-off of ≤10 yielded a sensitivity of 80%, specificity of 80%, and discriminated between the presence and absence of cognitive impairment 90% of the time
Lyon et al. (2009); Washington, DC, USA	71	Type: HAD, HIV encephalopathy in adolescents Classification: 1991	Person: NR Time: 10 min Materials: NR	ANI 1991 criteria	Size: NR Objective: NR Domains: intelligence, attention/memory, language Language: NR	Cut-off of ≤10: Sensitivity: 0.83 Specificity: 0.79 Cut-off of ≤9: Sensitivity: 0.88 Specificity: 0.83	No statistically significant differences in sensitivity and specificity between the HDS and MMSE. Using standard cut-offs, HDS had 83% sensitivity and 79% specificity, although MMSE had 50% sensitivity and 92% specificity. The optimal cut-off score for the HDS, producing the highest sensitivity and specificity, was ≤9, providing 88% sensitivity and 83% specificity (87% correct classification)
Morgan et al. (2008); San Diego, California	317; 135 (HIV+), 182 (HIV−)	Type: ANI, MCMD, HAD Classification: 1991	Person: NR Time: 5–10 min Materials: NR	Modified AAN 1991 criteria and Grant and Atkinson 1995 criteria	Size: large Objective: yes Domains: NR Language: NR	Demographically adjusted T-score <40: Sensitivity: 0.71 Specificity: 0.74 Raw cut-off score ≤10: Sensitivity: 0.17 Specificity: 0.94	In comparison to the traditional HDS cut-off score (raw score total ≤10), use of the demographically adjusted normative standards significantly improved the sensitivity (from 17 to 71%) and overall classification accuracy (increasing the odds ratio from 3 to approximately 6). The application of demographically adjusted normative standards on the HDS improves the clinical applicability and accuracy
Power et al. (1995); Baltimore, USA	130	Type: HAD Classification: 1991	Person: NR Time: NR Materials: NR	Memorial sloan kettering dementia evaluation; mini-mental state exam (MMSE); grooved pegboard (PB)	Size: small Objective: NR Domains: attention/concentration, memory, executive functioning, motor Language: English	Cut-off ≤10: Sensitivity: 0.80 Specificity: 0.91	HDS demonstrated greater efficiency in identifying HIV dementia compared to Grooved Pegboard and the Mini-Mental State Examination
Richardson et al. (2005); Boston Area, USA	40	Types: neurocognitive deficit or impairment (impairment in attention and concentration, psychomotor functioning, behavioral inhibition, constructional praxis) Classification: performance at least 2 standard deviation units below established norms on one or more independent NP measures in two or more domains of functioning	Person: NR Time: 10 min Materials: NR	NP battery	Size: medium Objective: yes Domains: memory, executive functioning, motor Language: English	Cut-off <=10: Sensitivity: 0.55 Specificity: 0.75	HDS prediction resulted in modest sensitivity and moderate specificity. In ROC curve analysis, area under the curve was only modestly better than chance (0.58). Optimal cut-off for the HDS is ≤10
Simioni et al. (2010), Geneva, Switzerland	100 (50 with cognitive complaints, 50 without cognitive complaints)	Types: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP battery	Size: medium Objective: no Domains: intelligence, attention/concentration, memory, language, executive functioning, speed of processing, motor Language: NR	Cut-off 10: Sensitivity: 0.54 Specificity: 0.96 Cut-off 14: Complaining: Sensitivity: 0.83 Specificity: 0.63 Non-Complaining: Sensitivity: 0.88 Specificity: 0.67	Prevalence of HAND is high even in long-standing aviremic HIV-positive patients. HAND without functional repercussion in daily life is most frequent. Cut-off of 14 points or less seemed to provide a useful tool to screen for HANDs
Smith et al. (2003); USA	90	Type: neurocognitive deficit or impairment (subtle HIV-related cognitive dysfunction) Classification: cognitive “abnormality” defined as performance that deviated at least 2 SD units below established norms on at least two independent NP measures	Person: NR Time: NR (noted “brief”) Materials: NR	NP battery	Size: medium Objective: no Domains: intelligence, memory, executive functioning, visuo-spatial, speed of processing, motor Language: English	Cut-off<=10: Sensitivity: 0.39 Specificity: 0.85	HDS lacks sufficient sensitivity to screen for NP abnormality beyond frank dementia. Intact performance (i.e., performance above established cut-off levels) contributes to a significant number of false-negative errors, suggesting need for NP battery for subtle neurocognitive deficits
Von Giesen et al. (2005); Dusseldorf, Germany	266; 55 (mildly demented), 211 (not demented)	Types: mild dementia, no dementia Classification: mild dementia (HDS score ≤ 10), no dementia (HDS score >10)	Person: NR Time: NR (noted “brief”) Materials: NR	NP battery	Size: small Objective: NR Domains: motor Language: German	Sensitivity: NR Specificity: NR	Patients with mild dementia showed significant slowing of most rapid alternating movement (MRAM) and significantly prolonged contraction time compared to non-demented patients. Motor performance correlated significantly with time-dependent HDS sub-scores for psychomotor speed and construction
Wojna et al. (2007); Puerto Rico, USA	96; 60 (HIV+), 36 (HIV−)	Types: asymptomatic cognitive impairment and symptomatic impairment (MCMD, HAD) Classification: modified 1991	Person: NR Time: NR (noted “rapid”) Materials: NR	NP battery	Size: medium Objective: yes Domains: intelligence, memory, executive functioning, speed of processing, motor Language: Spanish	Cut-off ≤12: Sensitivity: 0.63 Specificity: 0.84 Cut-off ≤13: Sensitivity: 0.87 Specificity: 0.46	HDS-Spanish total score and sub-scores for psychomotor speed and memory recall showed significant difference between HIV-negative women and HIV-positive women with dementia and between HIV-positive women with normal cognition and with dementia. Optimal cut-off point was ≤13
International HIV Dementia Scale
Joska et al. (2011); Cape Town, South Africa	190; 96 (HIV+); 94 (HIV−)	Types: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP battery	Size: medium Objective: no Domains: attention/concentration, memory, executive function, visuo-spatial, motor Language: isiXhosa, Afrikaans	Cut-off of 10: Sensitivity=0.45 Specificity=0.79	In ART naïve sample, HIV+ individuals displayed greater impairment compared to HIV− on IHDS and range of NP tests. With ROC analysis, the area under curve was 0.64. This data suggests that the IHDS may have limitations as a tool to screen for HAD in South Africa
Muniyandi et al. (2012); Thanjavur, India	33	Type: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP Battery	Size: NR Objective: yes Domains: NR Language: NR	NR	Tests which assess cognitive and motor speed may be more helpful than clinical psychiatric interview to spot the AIDS patients who have cognitive impairment. The International HIV Dementia Scale was the most sensitive instrument
Sacktor et al. (2005); Uganda/Baltimore, USA	247; 66 (HIV+ USA), 81 (HIV+ Uganda), 100 (HIV− control, Uganda)	Type: HAD Classification: 1991	Person: Non-neurologist Time: 2–3 min Materials: watch with a second hand	Memorial sloan kettering dementia staging; NP Battery	Size: medium Objective: yes Domains: attention/concentration, memory, language, executive functioning, speed of processing, motor Language: English, Luganda	Cut-off <=10: USA: Sensitivity: 0.80 Specificity: 0.57 Uganda: Sensitivity: 0.80 Specificity: 0.55	IHDS may be a useful screening test to identify individuals at risk for HIV dementia in both industrialized and developing world. Full NP testing should be performed to confirm diagnosis of HIV dementia
Singh et al. (2008); Durban, South Africa	20	Type: neurocognitive deficit or impairment (moderate and severe) Classification: Moderate – beyond the norms on at least 2 tests; Severe – three or more tests abnormal	Person: non-specialist Time: 2–3 min Materials: none	NP battery	Size: small Objective: NR Domains: attention, memory, executive functioning, motor Language: English, isiZulu	Cut-off of 10: Specificity=0.88 Sensitivity=0.50	Low specificity may limit clinical utility of IHDS. Research needed to verify the high burden on neurocognitive impairment among people with low CD4. Larger study needed to validate IHDS in South Africa
CogState
Cysique et al. (2006); Sydney, Australia	81	Types: ADC; neurocognitive deficits or impairments (psychomotor speed, working memory, attention, learning) Classification System: ≤−2 SD in 2 of 14 neuropsychological measures (Cysique 2004)	Person: NR Time: 10–15 min Materials: desktop computer	NP battery	Size: large Objective: yes Domains: intelligence, attention/concentration, memory, language, executive functioning, visuo-spatial, motor Language: English	Sensitivity: 0.81 Specificity: 0.70	Study supports utility of brief computerized battery in detection of HIV-associated neurocognitive impairment. Good agreement between standard neuropsychological tests and the CogState indices in identifying neurocognitive impairment
Maruff et al. (2009); Melbourne, Australia	293; 20 (ADC), 20 (ADC controls); 253 healthy adults	Type: ADC Definition: Price and Brew, 1988	Person: NR Time: 8–10 min Materials: personal computer	NP battery	Size: medium Objective: NR Domains: memory, visuo-spatial processing, motor Language: English	Sensitivity: NR Specificity: NR	Brief CogState battery has adequate construct validity and is sensitive to subtle cognitive impairment in ADC. Recommends that assessment of attention, processing speed, memory, and working memory based only on CogState can support solely on broad conclusions
Overton et al. (2011); St. Louis, USA	46	Type: neurocognitive deficit or impairment (mild to moderate impairment) Classification: Carey et al. (2004)	Person: NR Time: 12–15 min Materials: Computer and computer program	NP battery	Size: medium Objective: NR Domains: attention/concentration, memory, language, executive functioning, motor Language: English	GDS≥0.5 Sensitivity: NR Specificity: NR	Measures of both simple detection tests and identification task correlated with GDS and had highest level of correlation with tests in CHARTER battery. Other tests correlated poorly with NP testing. Composite score of 5 tests (significant in ROC analyses) correctly classified 90% of individuals according to impairment
Mini-Mental State Examination (MMSE)
Lyon et al. (2009); Washington, DC, USA	71	Type: HIV-encephalopathy in adolescents Classification: 1991	Person: NR Time: 10 min Materials: NR	ANI 1991 criteria	Size: NR Objective: NR Domains: NR Language: NR	Cut-off <24 Sensitivity: 0.50 Specificity: 0.92	MMSE identified 3 of 6 cases of encephalopathy. HDS appeared to be more clinically useful
Muniyandi et al. (2012); Thanjavur, India	33	Type: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP battery	Size: NR Objective: yes Domains: NR Language: NR	NR	Tests which assess cognitive and motor speed may be more helpful than clinical psychiatric interview to spot the AIDS patients who have cognitive impairment. The International HIV Dementia Scale was the most sensitive instrument
Power et al. (1995); Baltimore, USA	130	Type: HAD Classification: 1991	Person: NR Time: NR Materials: NR	Memorial sloan kettering dementia evaluation; HIV dementia scale (HDS); grooved pegboard (PB)	Size: Small Objective: NR Domains: attention/concentration, memory, executive functioning, motor Language: English	Cut-off≤28: Sensitivity: 0.50 Specificity: 0.88	MMSE was less efficient at identifying HIV Dementia than the HDS and the Grooved Pegboard
Brief Neurocognitive Screen (Component NeuroScreen)
Ellis et al. (2005); 15 sites, USA	301	Type: MCMD, HAD, neurocognitive deficits or impairment (speed of information processing, mental flexibility, working memory) Classification: 1991	Person: non-neurologist Time: 12–15 min Materials: NR	NP battery	Size: medium Objective: yes Domains: attention/concentration, memory, language, speed of processing, motor Language: English	Sensitivity: 0.65 Specificity: 0.72	Designed to estimate the frequency of HIV-associated neurocognitive disorders. In ROC, when compared to NP battery the area under the curve was 0.74. Yields (NeuroScreen as a whole) a substantial number of false positives and negatives so more useful for tracking prevalence in large cohorts rather than individual patients
Bender Gestalt Test (BGT)
Muniyandi et al. (2012); Thanjavur, India	33	Type: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP battery	Size: NR Objective: yes Domains: NR Language: NR	NR	Tests which assess cognitive and motor speed may be more helpful than clinical psychiatric interview to spot the AIDS patients who have cognitive impairment. The International HIV Dementia Scale was the most sensitive instrument
California Computerized Assessment Package (CalCAP) Mini-Battery
Gonzalez et al. (2003); California, USA	82	Type: neurocognitive deficits (normal, mild, mild-moderate, moderate, moderate-severe, severe) or impairments (attention and speed of information processing, abstraction, learning) Heaton 1995	Person: NR Time: 10 min Materials: computer	NP battery	Size: large Objective: No Domains: attention/concentration, memory, executive functioning, visuo-spatial, speed of processing, motor Language: English	Cut-off D-score of ≥0.5: Sensitivity: 0.68 Specificity: 0.77	Traditional NP batteries and computerized reaction time tests do not measure the same thing. They are not interchangeable in examining HIV-related NP impairment
Coin Rotation Test
Minor et al. (2010); Louisiana, USA	204	Type: neurocognitive deficits or impairment (psychomotor performance) Classification: NR	Person: Not specified Time: 1 min Materials: NR (infer coin and timer)	Psychomotor speed subscale of the modified HIV dementia scale (MHDS-PS)	Size: small Objective: NR Domains: memory, executive functioning, motor Language: English	Cut-off of 20 Rotations: Sensitivity: 0.72 Specificity: 0.61	Good convergent validity between Coin Rotation Test and Modified HDS. Gender did not significantly affect CRT performance but did affect modified HDS performance. CRT performance was less affected by education than MHDS performance
The Computer Assessment of Mild Cognitive Impairment
Becker et al. (2011); USA	59; 29 (HIV+), 30 (HIV−)	Type: neurocognitive deficits or impairment (normal, borderline, impaired) Classification: Global Impairment Rating (Woods 2004)	Person: health professionals Time: 20 min Materials: tablet with touch screen	NP battery	Size: large Objective: NR Domains: memory, language, executive functioning, visuo-spatial, speed of processing, motor Language: English	Sensitivity: 0.72 Specificity: 0.97	Detected mild impairment and median stability over 12 and 24 weeks of follow-up were 0.32 and 0.46 (did not differ as a function of serostatus). Discriminate functional analysis (6 CAMCI scores) correctly classified 90% of subjects
Four-item scale from Health Survey; Six-item scale from MOS
Revicki et al. (1998); Baltimore, USA	162 (baseline) 131 follow-up	Type: Mild, severe impairment Classification: TMT manual (Reitan 1992)	Person: NR Time: Less than 2 min Materials: NR	Trail Making Test (TMT)	Size: Small Objective: No Domains: Executive Functioning, Speed of Processing, Motor Language: English	Sensitivity: NR Specificity: NR	Logistic regression analysis showed both four-item version (CF4) included in the HIV Health Survey and the complete six-item scale (CF6) from the Medical Outcomes Study (MOS) predicted mild cognitive impairment based on TMT scores (p = 0.046 − 0.008) and severe cognitive impairment based on TMT scores (p = 0.0012 − 0.0003). Baseline significant differences in mean CF6 and CF4 scores for mildly impaired compared to less than mildly impaired and severely impaired and less than severely impaired
Grooved Pegboard
Power et al. (1995); Baltimore, USA	130	Type: HAD Classification: 1991	Person: NR Time: NR Materials: NR	Memorial sloan kettering dementia evaluation; HIV dementia scale (HDS); Mini-mental state exam (MMSE);	Size: small Objective: NR Domains: attention/concentration, memory, executive functioning, motor Language: English	Cut-off ≥ 90 sec: Sensitivity: 0.91 Specificity: 0.82	Was efficient in detecting HAD (86%) compared with the HDS (84%) and MMSE (72%)
Brief Cognitive Screen (BCS) – memory subtest, verbal fluency items, and conflicting stimulus test of the High Sensitivity Cognitive Screen (HSCS)
Fogel (1991); 3 locations, USA	156	Type: neurocognitive deficits or impairment (memory, verbal fluency, conflicting stimulus) Classification: abnormality on the brief dementia screen	Person: NR Time: NR Materials: NR	Standardized dementia screen (registration and delayed memory for three simple words, months in reverse, five serial sevens, and orientation to month and year)	Size: Small Objective: No Domains: memory, language, orientation Language: English	Sensitivity: NR Specificity: NR	Patients with abnormal scores on the Brief Cognitive Screen showed greater symptoms and functional impairment
HIV Dementia Diagnostic Test
Kwasa et al. (2012); Kisumu, Kenya	26; 14 (ANI, MND), 6 (HAD)	Type: ANI, MDN, HAD Classification: 2007	Person: non-physician health-care worker Time: NR Materials: NR	NP battery	Size: medium Objective: yes Domains: attention/concentration, memory, language, executive functioning, speed of processing, motor Language: English, Dhulou	Cut-off ≤22: Sensitivity: 0.63 Specificity: 0.67	Moderate sensitivity and specificity for HAD. Reliability was poor, suggesting that substantial training and formal evaluations of training adequacy will be critical
Hopkins Verbal Test Revised and Grooved Pegboard Test Nondominant Hand
Carey et al. (2004); San Diego, USA	190	Type: neurocognitive deficits or impairment (NP impaired or unimpaired) Classification: DSM-IV 1994, AAN 1991, Grant and Atkinson 1995	Person: trained psychometrist Time: 5 min Materials: NR	NP battery	Size: large Objective: NR Domains: intelligence, attention/concentration, memory, language, executive functioning, visuo-spatial, speed of processing, motor Language: English	Sensitivity: 0.78 Specificity: 0.85	The combination of Hopkins verbal test revised and grooved pegboard test nondominant hand was more accurate than the HIV dementia scale (HDS) in classifying HIV+ participants as NP impaired or unimpaired
Hopkins Verbal Learning Test/WAIS-III Digit Symbol
Carey et al. (2004); San Diego, USA	190	Type: neurocognitive deficits or impairment (NP impaired and unimpaired) Classification: DSM-IV 1994, AAN 1991, Grant and Atkinson 1995	Person: trained psychometrist Time: 5 min Materials: NR	NP battery	Size: large Objective: NR Domains: intelligence, attention/concentration, memory, language, executive functioning, visuo-spatial, speed of processing, motor Language: English	Sensitivity: 0.75 Specificity: 0.92	The combination of Hopkins verbal test revised and WAIS-III digit symbol (DS) subtest was more accurate than the HIV dementia scale (HDS) in classifying HIV+ participants as NP impaired or unimpaired
Medical Outcome Study HIV (MOS-HIV) Health Survey
Knippels et al. (2002); Netherlands and Flanders, Belgium	82	Type: neurocognitive deficits or impairment (neuropsychological impairment) Classification: NR	Person: completed at home Time: NR Materials: questionnaire	NP battery	Size: medium Objective: No Domains: attention/concentration, memory, language, executive functioning, visuo-spatial, motor Language: Dutch	Sensitivity: NR Specificity: NR	Showed significant associations with NP test performance overall and, specifically, with the domains of abstraction, language, visuo-spatial abilities (controlling for CD4 cell count and CDC disease stage). Trend toward significance in memory domain. Seems particularly sensitive to changes in NP test performance in early HIV-infection
Mental Alternation Test
Jones et al. (1993); Baltimore, USA	62	Type: neurocognitive deficits or impairment (orientation, memory, concentration, language, praxis, psycho or speed, sequencing ability) Classification: Abnormal performance on MMSE and Trail making (Crum 1993, Bornstein 2005)	Person: NR Time: 60 sec Materials: NR	Mini-mental state examination; trail making part A and B	Size: small Objective: NR Domains: intelligence, attention/concentration, memory, language, executive functioning, speed of processing Language: English	With MMSE: Sensitivity: 0.95 Specificity: 0.79 With Trail making: Sensitivity: 0.78 Specificity: 0.93	Scores correlated significantly with MMSE and trail making test part B scores when controlled for confounders. ROC curve showed cut-off of 15 yielded best results for detection of abnormal performance on MMSE and trail making test Part B
Motor Battery (Timed Gait, Grooved Pegboard, Finger-tapping)
Parsons et al. (2007); USA	361	Type: neurocognitive deficits or impairment (attention, executive, figural memory, verbal memory, language) Classification: NR	Person: NR Time: NR (noted “brief”) Materials: NR	NP battery	Size: Large Objective: NR Domains: attention/concentration, memory, language, executive functioning, visuo-spatial, speed of processing, motor Language: English	Cut-off of −0.42: Sensitivity: 0.79 Specificity: 0.76	Significant correlation with comprehensive battery (52% variance). Increased variance to 73% when Digit Symbol and Trail making added. Motor battery may have broader utility to diagnose and monitor HIV-related neurocognitive disorder in international settings
Prospective and Retrospective Memory Questionnaire (PRMQ)
Garvey et al. (2009); London, UK	45	Types: neurocognitive deficits or impairment (asymptomatic neurocognitive impairment aNCI, memory) Classification: aNCI-performance score more than 1 SD below the normative mean in at least 2 domains of CogState	Person: NR Time: 10 min Materials: questionnaire, writing utensil	CogState	Size: small Objective: NR Domains: attention/concentration, memory, executive functioning, motor, learning Language: English	Sensitivity: NR Specificity: NR	No statistically significant associations between PRMQ and CogState; questionnaire should not be used as a screening tool. Association between PRMQ and set-shifting task of CogState; questionnaire able to capture part of the executive function deterioration in HIV-associated NCI
Screening Algorithm
Cysique et al. (2010); Sydney, Australia	127; 97 (HIV+), 30 (HIV−)	Types: neurocognitive deficits or impairment (HAND) Classification: 2007	Person: clinical individual Time: 3 min Materials: patient’s clinical characteristics	NP battery	Size: large Objective: yes Domains: intelligence, attention/concentration, memory, language, speed of processing, motor, reasoning Language: English	Sensitivity: 0.78 Specificity: 0.70	Good overall prediction accuracy and specificity. Proved useful to identify HIV-infected patients with advanced disease at high risk of HAND who require more formal assessment. Recommended for HIV-infected Caucasian men with advanced disease
Timed Gait Test
Robertson et al. (2006); ACTG sites all over the world	1549; 1122 (AIDS), 113 (symptomatic), 165 (asymptomatic), 87 (HIV−)	Type: ADC Classification: neurologic history (Robertson 1997)	Person: NR Time: NR Materials: stopwatch, recording sheet	ADC Staging; NP Battery	Size: NR Objective: yes Domains: memory, language, executive functioning, visuo-spatial processing, motor Language: English	Sensitivity: 0.83 Specificity: 0.59	Good sensitivity and moderate specificity for detection of ADC. Abnormal Timed Gait scores were also significantly correlated with abnormal scores on neurological and neuropsychological evaluations. Cutting scores on the Timed Gait procedure resulted in reasonably good classification rates of ADC staging, especially for use as a screening tool
Wechsler Memory Scale
Muniyandi et al. (2012); Thanjavur, India	33	Type: ANI, MND, HAD Classification: 2007	Person: NR Time: NR Materials: NR	NP battery	Size: NR Objective: Yes Domains: NR Language: NR	NR	Tests that assess cognitive and motor speed may be more helpful than clinical psychiatric interview to spot the AIDS patients who have cognitive impairment. The International HIV Dementia Scale was the most sensitive instrument

MCMD minor cognitive-motor disorder, HAD HIV-associated dementia, ANI asymptomatic neurocognitive disorder, MND mild neurocognitive disorder, ADC AIDS dementia complex; NP neuropsychological; aNCI asymptomatic neurocognitive impairment; NR not reported

Criteria for battery size: “short” battery/criterion was defined by testing that took <30 min to administer; “medium” battery/criterion was defined by testing that took 30–90 min to administer; and “long and comprehensive” battery/criterion was defined by testing which took >90 min to administer

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Authors and Affiliations

Reuben N. Robbins
- 1
Email author
Travis M. Scott
- 2
- 6
Hetta Gouse
- 3
Thomas D. Marcotte
- 4
Sean B. Rourke
- 5

1.HIV Center for Clinical and Behavioral Studies, New York State Psychiatric Institute and Columbia University Medical CenterNew YorkUSA
2.Department of PsychologyFordham UniversityThe BronxUSA
3.Department of Psychiatry and Mental HealthUniversity of Cape TownCape TownSouth Africa
4.HIV Neurobehavioral Research Program, Center for Medicinal Cannabis ResearchUniversity of California, San DiegoSan DiegoUSA
5.Centre for Urban Health Solutions, St Michael’s HospitalToronto UniversityTorontoCanada
6.VA Palo Alto Health Care System, Sierra Pacific MIRECCPalo AltoUSA

Screening for HIV-Associated Neurocognitive Disorders: Sensitivity and Specificity

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