• View in gallery

    Flow chart for study enrollment. WHOCCD = World Health Organization clinical case definition. Stage is defined by WHO classification criteria. 20

  • 1

    World Health Organization, 2006. Towards Universal Access by 2010: How WHO is Working with Countries to Scale-up HIV Prevention, Treatment, Care and Support Page. Available at: http://www.who.int/hiv/pub/advocacy/universalaccess/en/. Accessed March 5, 2008.

  • 2

    Tozzi V, Balestra P, Bellagamba R, Corpolongo A, Salvatori MF, Visco-Comandini U, Vlassi C, Giulianelli M, Galgani S, Antinori A, Narciso P, 2007. Persistence of neuropsychological deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: prevalence and risk factors. J Acquir Immune Defic Syndr 45: 174–182.

    • Search Google Scholar
    • Export Citation
  • 3

    Stringer JS, Zulu I, Levy J, Stringer EM, Mwango A, Chi BH, Mtonga V, Reid S, Cantrell RA, Bulterys M, Saag MS, Marlink RG, Mwinga A, Ellerbrock TV, Sinkala M, 2006. Rapid scale-up of antiretroviral therapy at primary care sites in Zambia: feasibility and early outcomes. JAMA 296: 782–793.

    • Search Google Scholar
    • Export Citation
  • 4

    Muula AS, Chipeta J, Siziya S, Rudatsikira E, Mataya RHK, Ataika E, 2007. Human resources requirements for highly active antiretroviral therapy scale-up in Malawi. BMC Health Serv Res 7: 208.

    • Search Google Scholar
    • Export Citation
  • 5

    Kober K, Van Damme W, 2004. Scaling up access to antiretroviral treatment in southern Africa: who will do the job? Lancet 364: 103–107.

    • Search Google Scholar
    • Export Citation
  • 6

    Clifford DB, Mitike MT, Mekonnen Y, Zhang J, Zenebe G, Melaku Z, Zewde A, Gessesse N, Wolday D, Messele T, Teshome M, Evans S, 2007. Neurological evaluation of untreated human immunodeficiency virus infected adults in Ethiopia. J Neurovirol 13: 67–72.

    • Search Google Scholar
    • Export Citation
  • 7

    Modi G, Hari K, Modi M, Mochan A, 2007. The frequency and profile of neurology in black South African HIV infected (clade C) patients: a hospital-based prospective audit. J Neurol Sci 254: 60–64.

    • Search Google Scholar
    • Export Citation
  • 8

    Sacktor NC, Wong M, Nakasujja N, Skolasky RL, Selnes OA, Musisi S, Robertson K, McArthur JC, Ronald A, Katabira E, 2005. The international HIV dementia scale: a new rapid screening test for HIV dementia. AIDS 19: 1367–1374.

    • Search Google Scholar
    • Export Citation
  • 9

    Power C, Selnes OA, Grim JA, McArthur JC, 1995. HIV dementia scale: a rapid screening test. J Acquir Immune Defic Syndr Hum Retrovirol 8: 273–278.

    • Search Google Scholar
    • Export Citation
  • 10

    Wojna V, Skolasky RL, Hechavarria R, May R, Selnes O, McArthur JC, Melendez LM, Maldonado E, Zorrilla CD, Garcia H, Kraiselburd E, Nath A, 2006. Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12: 356–364.

    • Search Google Scholar
    • Export Citation
  • 11

    WHO/UNAIDS, 2004. Epidemiological Fact Sheet on HIV/AIDS and Sexually Transmitted Infections: Zambia Page. Available at: http://www.who.int/globalatlas/predefinedReports/EFS2004/index.asp. Accessed March 5, 2008.

  • 12

    World Health Organization, 1990. Interim proposal for a WHO staging system for HIV infection and disease. Wkly Epidemiol Rec 65: 221–224.

    • Search Google Scholar
    • Export Citation
  • 13

    Miller WC, Thielman NM, Swai N, Cegielski JP, Shao J, Manyenga D, Mlalasi J, Lallinger GJ, 1995. Diagnosis and screening of HIV/AIDS using clinical criteria in Tanzanian adults. J Acquir Immune Defic Syndr Hum Retrovirol 9: 408–414.

    • Search Google Scholar
    • Export Citation
  • 14

    Folstein MF, Folstein SE, McHugh PR, 1975. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189–198.

    • Search Google Scholar
    • Export Citation
  • 15

    Maj M, D’Elia L, Satz P, Janssen R, Zaudig M, Uchiyama C, Starace F, Galderisi S, Chervinsky A, 1993. Evaluation of two new neuropsychologicalal tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: a WHO study. Arch Clin Neuropsychol 8: 123–135.

    • Search Google Scholar
    • Export Citation
  • 16

    Gladstone M, Lancaster G, Jones A, Maleta K, Mtitimila E, Ashorn P, Smyth R, 2007. Can Western developmental screening tools be modified for use in a rural Malawian setting? Arch Dis Child 93: 23–29.

    • Search Google Scholar
    • Export Citation
  • 17

    Maj M, Satz P, Janssen R, Zaudig M, Starace F, D’Elia L, Sughondhabirom B, Mussa M, Naber D, Ndetei D, 1994. WHO Neuropsychiatric AIDS study, cross-sectional phase II. Neuropsychologicalal and neurological findings. Arch Gen Psychiatry 51: 51–61.

    • Search Google Scholar
    • Export Citation
  • 18

    Sebit MB, 1995. Neuropsychiatric HIV-1 infection study: in Kenya and Zaire cross-sectional phase I and II. Cent Afr J Med 41: 315–322.

  • 19

    Belec PL, Testa J, Vohito MD, Gresenguet G, Martin MI, Tabo A, Di Costanzo B, Georges AJ, 1989. Neurologic and psychiatric manifestations of AIDS in Central African Republic [in French]. Bull Soc Pathol Exot Filiales 82: 297–307.

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  • 20

    Howlett WP, Nkya WM, Mmuni KA, Missalek WR, 1989. Neurological disorders in AIDS and HIV disease in the northern zone of Tanzania. AIDS 3: 289–296.

    • Search Google Scholar
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  • 21

    Wong MH, Robertson K, Nakasujja N, Skolasky R, Musisi S, Katabira E, McArthur JC, Ronald A, Sacktor N, 2007. Frequency of and risk factors for HIV dementia in an HIV clinic in sub-Saharan Africa. Neurology 68: 350–355.

    • Search Google Scholar
    • Export Citation
  • 22

    Dore GJ, Correll PK, Li Y, Kaldor JM, Cooper DA, Brew BJ, 1999. Changes to AIDS dementia complex in the era of highly active antiretroviral therapy. AIDS 13: 1249–1253.

    • Search Google Scholar
    • Export Citation
  • 23

    Janssen RS, Nwanyanwu OC, Selik RM, Stehr-Green JK, 1992. Epidemiology of human immunodeficiency virus encephalopathy in the United States. Neurology 42: 1472–1476.

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  • 24

    McGrath NM, Cooke GS, 2007. Frequency of and risk factors for HIV dementia in an HIV clinic in sub-Saharan Africa. Neurology 69: 411–412, author reply 412–413.

    • Search Google Scholar
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Closing Gaps in Antiretroviral Therapy Access: Human Immunodeficiency Virus–Associated Dementia Screening Instruments for Non-Physician Healthcare Workers

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  • 1 International Neurologic and Psychiatric Epidemiology Program, and College of Osteopathic Medicine, Michigan State University, East Lansing, Michigan; Department of Psychiatry, University of Zambia, Lusaka, Zambia; Department of Neurological Sciences, University of Nebraska, Omaha, Nebraska; Chikankata Health Services, Mazabuka, Zambia

Human immunodeficiency virus–associated dementia (HIV-D) is an indication for antiretroviral therapy (ART), but HIV-D is not routinely screened for in ART clinics in sub-Saharan Africa. Given the dearth of physicians in sub-Saharan Africa, enabling non-physician healthcare workers to identify HIV-D is crucial for early treatment initiation and preventing chronic neurologic disability. Non-physician healthcare workers administered locally adapted screening instruments to 48 persons living with acquired immunodeficiency syndrome (PLWAs), and 15 healthy comparison persons provided normative data. Stage IV PLWAs performed worse than the comparison group on all tests. Overall, 24 (50%) of 48 PLWAs had significant cognitive impairment. Among HIV staging categories, 1 stage II (33%), 6 stage III (42%), and 17 stage IV (55%) patients were identified as cognitively impaired. Our pilot study indicates that screening instruments used by non-physician healthcare workers can identify cognitive impairment in PLWAs and may facilitate appropriate initiation of ART in resource-poor settings.

INTRODUCTION

Human immunodeficiency virus–associated dementia (HIV-D) is a qualifying indication for antiretroviral therapy (ART) initiation according to World Health Organization (WHO) guidelines for resource-limited settings.1 However, this dementia is not routinely screened for in ART clinics in sub-Saharan Africa because of a lack of valid instruments with population-based normative data. Delays in treatment initiation may lead to irreversible neurologic damage that complicates future HIV management.2 However, the non-physician healthcare workers providing the bulk of HIV care in Sub-Saharan Africa35 have little experience in diagnosing these disorders.

Previous investigations for HIV-D in Sub-Saharan Africa have used physician specialists for evaluation.68 No previous studies have used non-physician healthcare workers for cognitive assessments. We trained non-physician healthcare workers in administration of locally adapted screening instruments. We report cross-sectional results of performance and frequency of cognitive impairment (CI) in persons living with acquired immunodeficiency syndrome (PLWAs) admitted to an urban hospice facility in Lusaka, Zambia.

METHODS

Study design.

This study includes a cohort of PLWAs recruited from a hospice in Kalingalinga, Lusaka, Zambia. In the absence of any validated neuropsychiatric tests in Zambia, we also collected data from a convenience sample of healthy volunteers from the same community to serve as a reference group for comparison purposes. This design has been used in several other populations in which normative data were unavailable for neuropsychological tests.810 We report the cross-sectional results of neuropsychological test performance and prevalence of cognitive impairment for PLWAs overall and by WHO HIV staging.

Participants.

All participants were recruited from a hospice facility in Kalingalinga, Lusaka, Zambia. The seroprevalence of HIV in Kalingalinga was reported to be 26% in 2002. 11 The hospice had a 24-bed capacity, but no laboratory or radiologic equipment available on site. All PLWAs ≥ 18 years of age admitted for the first time to the hospice from January 21, 2004 through March 22, 2004 were interviewed. Exclusion criteria included failure to meet the WHO clinical dase definition for acquired immunodeficiency syndrome (AIDS) (WHOCCD), 12 past medical history of a chronic neurologic disorder, psychiatric disorder, substance abuse, or a physical deficit, or severe medical illness that would interfere with study performance. To identify a reference group to provide normative data on neuropsychological tests, a convenience sample of non-spouse family members or friends of outpatients attending bi-weekly clinics were invited to undergo the study interview and neuropsychological tests.

Interview procedures.

This project was reviewed and approved by the Michigan State University Committee on Research Involving Human Subjects and the University of Zambia Research Ethics Committee. Twelve non-physician healthcare workers were trained in administration of study instruments. Three were clinical officers who receive three years of post-secondary clinical training, and were entirely responsible for clinical care at the hospice in the absence of a physician. The remaining healthcare workers included one nurse, one nursing student, and seven hospice-trained community health workers with at least three years of secondary school education. After informed consent procedures, participants underwent a structured interview assessing demographic information and past medical history. A chart review was also undertaken. Interviews were conducted in the patient’s language of choice between Chinyanja (67%) and English (33%).

HIV/AIDS diagnosis.

Status of HIV was assessed by the WHOCCD. 12,13 Comparison group participants with signs/symptoms of HIV were excluded from analysis (n = 3). The WHOCCD for AIDS was preferred over conducting HIV testing because of limited access to HIV testing. Patients were also assessed by WHO HIV staging criteria. 12 Subsidized ART were generally not available in Zambia during the study period.

Neuropsychological screening instruments.

The mini-mental state examination 14 (MMSE) was selected because of frequent informal use among clinical psychiatric officers in Lusaka. The HIV dementia scale9 (HDS) and color trails 1 (CT1) 15 were chosen because of the specificity of each in assessing HIV-D deficits. To adapt these instruments, focus group discussions were conducted with one of the authors, a local psychiatrist (AH), internists, and medical students to identify test items likely to be culturally or otherwise problematic. Once identified, the cognitive domain tested by each item and relationship to HIV-D was discussed and adaptation suggestions were provided. Adapted items involved tasks requiring reading and writing and were replaced with more appropriate items deemed to have content validity by the focus group. For example, the MMSE item for spelling WORLD backwards was replaced with an item requiring the participant to list the days of the week backwards. This change reduced the educational bias of this item and still assessed concentration and attention. The MMSE item requiring participants to read and follow the command “CLOSE YOUR EYES” was replaced with an item requiring the patient to look at the face of the examiner and do what the examiner does (closes eyes). Other similar adaptations were made to the MMSE (Appendix) and HDS.

For items in which an appropriate adaptation could not be identified, the item was tested in original form. No changes were made to CT1. After a careful emic translation procedure by experienced medical translators, instruments were back-translated into English by a linguist and medical professionals and pre-piloted in the community prior to study commencement. These preliminary validation steps have been used for adaptation of western instruments in other non-western, resource-limited settings. 16

Sample size calculation.

In a U.S. study on the validity of the HDS comparing AIDS patients with and without dementia, asymptomatic HIV patients, and healthy controls, an effect size of 1.35 was identified between groups on scores of the HDS and MMSE.9 Extrapolating this effect size to this population, an ad hoc sample size calculation of 15 patients per group was estimated to be necessary to identify significant differences in mean neuropsychological test scores with α = 0.05 and β = 0.20.

Statistical analysis.

Data was coded and entered into an Excel ® (Microsoft, Redmond, WA) spreadsheet. All statistical analyses were carried out using SPSS version 13.0 (SPSS Inc., Chicago, IL) or SAS version 9.1 (SAS Institute, Cary, NC). Categorical variables, including sex and language of interview, were analyzed using Fisher’s exact test. Mann-Whitney U tests and Student’s t-tests were performed to evaluate continuous variables including age; education; and MMSE, HDS, and CT1 scores. The WHO stage was evaluated as a potential effect modifier of performance on neuropsychological tests by using Kruskal-Wallis and one-way analysis of variance tests. Few patients had evidence of mild HIV disease. Thus, patients with WHO Stage II and Stage III HIV illness were grouped together for analysis.

Because all nonparametric test results supported the results of the parametric tests, only the latter results are reported to maintain the raw data in original scale. Significant CI was defined as scoring > 2 SD below the mean of the comparison group on the MMSE or > 2 SD below the mean of the comparison group on the HDS and CT1, similar to previous investigations. 17,18 The prevalence of CI is reported as the proportion (%) of PLWAs meeting the study criteria for significant CI. A chi-square test for trend in binomial proportions was used to assess the relationship between CI and WHO HIV stage. A significance level of 0.05 was considered statistically significant for all tests.

RESULTS

Seventy-six patients were admitted to the hospice during the study period (Figure 1). The most common reason for not undergoing the study interview was that the patient died or was transferred to another medical facility before enrollment (n = 17, 22%). Ten patients (13%) did not meet WHOCCD criteria for AIDS and were excluded from the analysis. Only one (1%) patient was unable to complete the interview because of acute illness, and no patients were excluded because of a previous history of psychiatric or neurologic disease. Thus, the final study group comprised 48 PLWAs. One patient was currently receiving ART, and none reported previous use of ART. Only one comparison group volunteer (6%) reported having a negative HIV test result. No significant differences were found between PLWAs and healthy participants with regard to age, education, or sex (Table 1). Among all PLWAs, 25 (52.1%) reported noticing changes in memory and 16 (33.3%) reported changes in thinking. No one in the comparison group had these complaints.

Performance on adapted neuropsychological instruments.

Performance on the adapted MMSE for PLWAs and the comparison group are summarized in Table 2. Overall, the MMSE had excellent face validity among comparison group participants. The PLWAs had significant difficulty on items of attention, constructional praxis, and memory recall, consistent with deficits seen in HIV-D.

Performance on the HDS was markedly difficult for PLWAs and the comparison group (Table 3). Ten PLWAs (20.8%) and one (6.7%) comparison group participant were unable to complete the timed number writing task correctly (i.e., omitted numbers, wrote numbers backwards, or were unable to write numbers from 1 to 25). The memory recall task also proved difficult, with only 3 (20%) of 15 comparison participants and 7 of (14.3%) of 48 PLWAs able to correctly recall all four items. The three-dimensional cube drawing was so difficult for comparison group participants and PLWAs to complete that it was dropped from the final analysis.

Color trails 1 was also difficult to administer with 12 (25%) PLWAs and 1 (8.6%) comparison participant unable to complete the task in the allotted 300-second time limit. It is also notable that the need for color copies of test documents resulted in several instances in which copies were unavailable or were poorly copied, resulting in missing data points for analysis.

Neuropsychological comparisons.

Results of neuropsychological tests are reported in Table 4. Overall, three PLWAs (6%) were identified as having WHO stage II disease, 14 (29%) WHO stage III disease, and 31 (65%) WHO Stage IV disease. Overall, PLWAs scored significantly worse as a group compared with comparison participants on the MMSE, with a mean MMSE score of 21.39 versus 28.20 for comparison participants (P < 0.001). Similarly, PLWAs averaged only 2.4 points on the HDS as a group versus 4.2 points averaged by the comparison group (P < 0.001). The PLWAs also performed worse overall on CT1 compared with comparison participants, with a mean time to complete CT1 of 182.69 seconds versus 104.36 seconds for comparison participants (P < 0.003).

After stratifying by WHO stage, the mean MMSE score for WHO Stage IV PLWAs was 20.06 versus a mean of 23.82 for WHO Stage II/III PLWAs and 28.20 for comparison participants. These differences were highly statistically significant for WHO stage IV PLWAs versus comparison participants (P < 0.001), but not between WHO stage IV PLWAs and WHO stage II/III PLWAs (P = 0.078) or between WHO stage II/III and comparison participants (P = 0.081). The PLWAs with WHO stage IV disease performed significantly worse on the HDS than all other groups, with a mean of 1.87 points on the HDS compared with 3.18 (P = 0.011) and 4.20 points for WHO stage II/III and comparison participants, respectively. However, HDS performance was not significantly different between WHO stage II/III PLWAs and comparison participants (P = 0.086). The WHO staging stratification again demonstrated poorer CT1 performance with advanced HIV disease, with WHO stage IV PLWAs having a mean of 195.07 seconds to complete CT1 versus 162.29 seconds for WHO stage II/III PLWAs and 104.36 seconds for comparison participants. However, these differences were only significant between WHO stage IV and comparison participants (P < 0.003).

Prevalence of cognitive impairment.

Twenty-four PLWAs (50%) scored > 2 SDs below the comparison mean on the MMSE, and 8 of those 24 also scored > 2 SD below the comparison mean on the HDS and CT1. No additional cases were identified using the latter criteria alone. Twenty-four PLWAs (50%) scored > 2 SD below the comparison mean on the HDS. Finally, 13 PLWAs (27%) scored > 2 SD below the comparison mean on CT1. Overall, 24 (50%) PLWAs met the study definition for significant CI. Among WHO staging categories, there was 1 stage II (33%), 6 stage III (42%), and 17 stage IV (55%) patients with significant CI but this trend was not statistically significant (P = 0.24).

DISCUSSION

In our pilot study, non-physician healthcare workers used locally adapted screening instruments to identify significant differences in neuropsychological test performance between PLWAs and a healthy comparison group. Although significant between group differences were found by using all instruments, the MMSE was noted to be most easily administered and to have better face validity among comparison participants than the HDS and CT1. It is possible that the frequent errors encountered on items from the HDS and CT1 could be accounted for by poor administration by the non-physician healthcare workers in our study, although no problems were identified during training. These problems are more easily explained by the paper and pencil testing format and the reliance on ability to read and write numbers from 1 to 25 in a population with low educational levels and inexperience with test taking. Such findings emphasize the need for culturally and educationally relevant neuropsychological instruments. An addition to the MMSE of more culturally appropriate tests of psychomotor speed, such as finger-tapping tests, may improve identification of HIV-related CI and should be considered in future investigations. Clinical psychiatry officers in Zambia commonly use MMSE items for cognitive assessments, and therefore the MMSE has the benefit of widespread familiarity. The international HIV dementia scale (IHDS) may also prove to be a useful screening instrument, but was not available at the time of our study.8 We are applying the adapted MMSE and the IHDS in another larger study in a rural Zambian population by using non-physician healthcare workers, which may help elucidate further strengths and limitations of these two instruments for routine clinical assessments.

We found that 50% of all PLWAs and 55% of patients with WHO stage IV HIV disease met our study definition of CI. In addition, the identification of 1 stage II (33%) and 6 stage III (42%) patients with CI suggests that screening is important for all symptomatic HIV patients. Other African investigations have found equally high prevalence estimates in hospitalized patients. 1821 The HIV patients with CI may be overrepresented among hospitalized patients because of the increased dependency and caregiving needs, but our findings suggest that CIs in PLWAs are disorders that consume a great deal of hospital resources in sub-Saharan Africa. Given that delayed treatment may result in irreversible CI, resources should be allocated to enable increased training in identifying and managing such cases, as well as enabling caregiver respite.

This study was limited by the small sample size and the fact that previous normative neuropsychiatric data were not available in this population. Despite our careful screening procedure, some patients in the comparison group may have been asymptomatic HIV cases. However, inclusion of asymptomatic HIV patients in our comparison group should bias our results towards the null. However, we found highly significant differences between groups on neuropsychological test performance.

Screening instruments for cognitive impairment cannot be used alone for HIV-D identification, but may help to narrow the ART access gap for a subset of patients with HIV-D that would not otherwise qualify for ART initiation. HIV-D is the initial AIDS defining illness for 3–4% of antiretrovirally naive patients in the United States and Australia. 22,23 Identification of HIV-D would also benefit patients who do not qualify for ART on the basis of laboratory criteria and those with other undiagnosed stage III or IV HIV illnesses in areas with limited diagnostic abilities. Although little is known about the epidemiology of HIV-D in Africa, a study in Kampala, Uganda reported that 6 of 16 HIV-D patients had CD4 cell counts greater than 200, making a clinical-based diagnosis essential for ART commencement in 37.5% of HIV-D patients identified. 24 In addition, use of such screening instruments may facilitate triage to specialists or diagnosis of other causes of CI in PLWAs. The time to enable clinical identification is now, so that these important disorders can be considered in public health policy planning and resource allocation. Our preliminary findings indicate that simple screening examinations performed by non-physician healthcare workers can identify HIV patients with significant CI.

Table 1

Baseline characteristics of PLWAs and comparison group*

Table 1
Table 2

Number of correct responses (%) to adapted mini-mental state examination items by group and cognitive domain assessed*

Table 2
Table 3

Number of correct responses (%) to human immunodeficiency virus dementia scale items by group and cognitive domain assessed*

Table 3
Table 4

Neuropsychological assessments for PLWAs and comparison group*

Table 4
Figure 1.
Figure 1.

Flow chart for study enrollment. WHOCCD = World Health Organization clinical case definition. Stage is defined by WHO classification criteria. 20

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 6; 10.4269/ajtmh.2009.80.1054

*

Address correspondence to Gretchen L. Birbeck, International Neurologic and Psychiatric Epidemiology Program, Michigan State University, 324 W Fee Hall, East Lansing, MI 48824. E-mail: gretchen.birbeck@ht.msu.edu

Note: An appendix (Zambian Mini-Mental State Examination) appears online at www.ajtmh.org.

Authors’ addresses: Michelle P. Kvalsund and Gretchen L. Birbeck, International Neurologic and Psychiatric Epidemiology Program, Michigan State University, 324 W Fee Hall, East Lansing, MI 48824, E-mails: michelle.kvalsund@ht.msu.edu and Gretchen.birbeck@ht.msu.edu. Alan Haworth, University of Zambia, PO Box 33991, Lusaka, Zambia, E-mail: alan.haworth@yahoo.com. Daniel L. Murman, Department of Neurological Sciences, University of Nebraska, 982045 Nebraska Medical Center, Omaha, NE 68198, E-mail: dlmurman@unmc.edu. Ellen Velie, Department of Epidemiology, Michigan State University, B627 West Fee Hall, East Lansing, MI 48824, E-mail: velie@epi.msu.edu.

Acknowledgments: We thank the administrators at Our Lady’s Hospice for the support and expertise that made this project possible; the healthcare workers at Our Lady’s Hospice in Kalingalinga for assistance with interviewing despite their busy schedules; the translators from Chainama College of Health Sciences for the many long hours spent diligently translating study documents; and, most especially, the patients, families, and community members who participated in the study.

Financial support: This study was supported by a U.S. Student Fulbright Grant and Sigma Delta Epsilon Women in Science Hartley Fellowship.

REFERENCES

  • 1

    World Health Organization, 2006. Towards Universal Access by 2010: How WHO is Working with Countries to Scale-up HIV Prevention, Treatment, Care and Support Page. Available at: http://www.who.int/hiv/pub/advocacy/universalaccess/en/. Accessed March 5, 2008.

  • 2

    Tozzi V, Balestra P, Bellagamba R, Corpolongo A, Salvatori MF, Visco-Comandini U, Vlassi C, Giulianelli M, Galgani S, Antinori A, Narciso P, 2007. Persistence of neuropsychological deficits despite long-term highly active antiretroviral therapy in patients with HIV-related neurocognitive impairment: prevalence and risk factors. J Acquir Immune Defic Syndr 45: 174–182.

    • Search Google Scholar
    • Export Citation
  • 3

    Stringer JS, Zulu I, Levy J, Stringer EM, Mwango A, Chi BH, Mtonga V, Reid S, Cantrell RA, Bulterys M, Saag MS, Marlink RG, Mwinga A, Ellerbrock TV, Sinkala M, 2006. Rapid scale-up of antiretroviral therapy at primary care sites in Zambia: feasibility and early outcomes. JAMA 296: 782–793.

    • Search Google Scholar
    • Export Citation
  • 4

    Muula AS, Chipeta J, Siziya S, Rudatsikira E, Mataya RHK, Ataika E, 2007. Human resources requirements for highly active antiretroviral therapy scale-up in Malawi. BMC Health Serv Res 7: 208.

    • Search Google Scholar
    • Export Citation
  • 5

    Kober K, Van Damme W, 2004. Scaling up access to antiretroviral treatment in southern Africa: who will do the job? Lancet 364: 103–107.

    • Search Google Scholar
    • Export Citation
  • 6

    Clifford DB, Mitike MT, Mekonnen Y, Zhang J, Zenebe G, Melaku Z, Zewde A, Gessesse N, Wolday D, Messele T, Teshome M, Evans S, 2007. Neurological evaluation of untreated human immunodeficiency virus infected adults in Ethiopia. J Neurovirol 13: 67–72.

    • Search Google Scholar
    • Export Citation
  • 7

    Modi G, Hari K, Modi M, Mochan A, 2007. The frequency and profile of neurology in black South African HIV infected (clade C) patients: a hospital-based prospective audit. J Neurol Sci 254: 60–64.

    • Search Google Scholar
    • Export Citation
  • 8

    Sacktor NC, Wong M, Nakasujja N, Skolasky RL, Selnes OA, Musisi S, Robertson K, McArthur JC, Ronald A, Katabira E, 2005. The international HIV dementia scale: a new rapid screening test for HIV dementia. AIDS 19: 1367–1374.

    • Search Google Scholar
    • Export Citation
  • 9

    Power C, Selnes OA, Grim JA, McArthur JC, 1995. HIV dementia scale: a rapid screening test. J Acquir Immune Defic Syndr Hum Retrovirol 8: 273–278.

    • Search Google Scholar
    • Export Citation
  • 10

    Wojna V, Skolasky RL, Hechavarria R, May R, Selnes O, McArthur JC, Melendez LM, Maldonado E, Zorrilla CD, Garcia H, Kraiselburd E, Nath A, 2006. Prevalence of human immunodeficiency virus-associated cognitive impairment in a group of Hispanic women at risk for neurological impairment. J Neurovirol 12: 356–364.

    • Search Google Scholar
    • Export Citation
  • 11

    WHO/UNAIDS, 2004. Epidemiological Fact Sheet on HIV/AIDS and Sexually Transmitted Infections: Zambia Page. Available at: http://www.who.int/globalatlas/predefinedReports/EFS2004/index.asp. Accessed March 5, 2008.

  • 12

    World Health Organization, 1990. Interim proposal for a WHO staging system for HIV infection and disease. Wkly Epidemiol Rec 65: 221–224.

    • Search Google Scholar
    • Export Citation
  • 13

    Miller WC, Thielman NM, Swai N, Cegielski JP, Shao J, Manyenga D, Mlalasi J, Lallinger GJ, 1995. Diagnosis and screening of HIV/AIDS using clinical criteria in Tanzanian adults. J Acquir Immune Defic Syndr Hum Retrovirol 9: 408–414.

    • Search Google Scholar
    • Export Citation
  • 14

    Folstein MF, Folstein SE, McHugh PR, 1975. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12: 189–198.

    • Search Google Scholar
    • Export Citation
  • 15

    Maj M, D’Elia L, Satz P, Janssen R, Zaudig M, Uchiyama C, Starace F, Galderisi S, Chervinsky A, 1993. Evaluation of two new neuropsychologicalal tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: a WHO study. Arch Clin Neuropsychol 8: 123–135.

    • Search Google Scholar
    • Export Citation
  • 16

    Gladstone M, Lancaster G, Jones A, Maleta K, Mtitimila E, Ashorn P, Smyth R, 2007. Can Western developmental screening tools be modified for use in a rural Malawian setting? Arch Dis Child 93: 23–29.

    • Search Google Scholar
    • Export Citation
  • 17

    Maj M, Satz P, Janssen R, Zaudig M, Starace F, D’Elia L, Sughondhabirom B, Mussa M, Naber D, Ndetei D, 1994. WHO Neuropsychiatric AIDS study, cross-sectional phase II. Neuropsychologicalal and neurological findings. Arch Gen Psychiatry 51: 51–61.

    • Search Google Scholar
    • Export Citation
  • 18

    Sebit MB, 1995. Neuropsychiatric HIV-1 infection study: in Kenya and Zaire cross-sectional phase I and II. Cent Afr J Med 41: 315–322.

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