Cognitive and motor deficits associated with HIV-2287 infection in infant pigtailed macaques: A nonhuman primate model of pediatric neuro-AIDS

Journal of NeuroVirology

Volumn 11, Issue 1, 2005, Pages 34-45

  Worlein, Julie M ^a   Leigh, J ^a   Larsen, K ^a   Kinman, L ^a   Schmidt, A ^a   Ochs, H ^b   Ho, R J Y ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

AIDS; Animal model; Cognitive development; Infant; Motor development; Neuro AIDS; Nonhuman primate

Indexed keywords

VIRUS RNA;

AMNION; ANALYSIS OF VARIANCE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY CATHETER; CAROTID ARTERY; CHILDBIRTH; COCULTURE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DEVELOPMENTAL STAGE; DISEASE ASSOCIATION; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; INFANCY; INTRAVENOUS CATHETER; JUGULAR VEIN; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MACACA; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RETROVIRUS INFECTION; REVIEW; STATISTICAL SIGNIFICANCE; THIRD TRIMESTER PREGNANCY; VERTICAL TRANSMISSION;

AIDS DEMENTIA COMPLEX; ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DISEASE TRANSMISSION, VERTICAL; FEMALE; HIV-2; HUMANS; MACACA NEMESTRINA; MONKEY DISEASES; MOTOR SKILLS; PREGNANCY;

EID: 16244367477     PISSN: 13550284     EISSN: None     Source Type: Journal    
DOI: 10.1080/13550280590901732     Document Type: Review

References (89)

1. Abrams EJ, Matheson PB, Thomas PA, Thea DM, Krasinski K, Lambert G, Shaffer N, Bamji M, Hutson D, Grimm K, et al (1995). Neonatal predictors of infection status and early death among 332 infants at risk of HIV-1 infection monitored prospectively from birth. New York City Perinatal HIV Transmission Collaborative Study Group. Pediatrics 96: 451-458.
2. Angelini L, Zibordi F, Triulzi F, Cinque P, Giudici B, Pinzani R, Plebani A (2000). Age-dependent neurologic manifestations of HIV infection in childhood. Neurol Sci 21: 135-142.
3. Aylward EH, Butz AM, Hutton N, Joyner ML, Vogelhut JW (1992). Cognitive and motor development in infants at risk for human immunodeficiency virus. Am J Dis Child 146: 218-222.
4. Belman AL (1990). AIDS and pediatric neurology. Neurol Clin 8: 571-603.
5. Belman AL (1992). Acquired immunodeficiency syndrome and the child's central nervous system. Pediatr Clin N Am 39: 691-714.
6. Belman AL (2002). HIV-1 infection and AIDS. Neurol Clin 20: 983-1011.
7. Belman AL, Diamond G, Dickson D, Horoupian D, Llena J, Lantos G, Rubinstein A (1988). Pediatric acquired immunodeficiency syndrome: neurologic syndromes. Am J Dis Child 142: 29-35.
8. Belman AL, Muenz LR, Marcus JC, Goedert JJ, Landesman S, Rubinstein A, Goodwin S, Durako S, Willoughby A (1996). Neurologic status of human immunodeficiency virus 1-infected infants and their controls: a prospective study from birth to 2 years. Pediatrics 98: 1109-1118.
9. Boivin MJ, Davies AG, Mokili JKL, Green SDR, Giordani B, Cutting WAM (1995). A preliminary evaluation of cognitive and motor effects of pediatric HIV infection in Zairian children. Health Psychol 14: 13-21.
10. Brouwers P, DeCarli C, Tudor-Williams G, Civitello L, Moss H, Pizzo P (1994). Interrelations among patterns of change in neurocognitive, CT brain imaging and CD4 measures associated with anti-retroviral therapy in children with symptomatic HIV infection. Adv Neuroimmuno 4: 223-231.
11. Brouwers P, Tudor-Williams G, DeCarli C, Moss HA, Wolters PL, Civitello LA, and Pizzo PA (1995). Relation between stage of disease and neurobehavioral measures in children with symptomatic HIV disease. AIDS 9: 713-720.
12. Bruck I, Tahan TT, Rodrigues da Cruz C, Martins LTF, Antoniuk SA, Rodrigues M, Mara de Souza S, Regina de Bruyn L (2001). Developmental milestones of vertically HIV infected and seroreverters Children: follow up of 83 children. Arq Neuropsiquiatr 59: 691-695.
13. Burbacher TM, Grant KS, Mottet NK (1986). Retarded object permanence development in methylmercury exposed macaca-fascicularis infants. Dev Psychol 22: 771-776.
14. Chase C, Vibbert M, Pelton SI, Coulter DL, Cabral H (1995). Early neurodevelopmental growth in children with vertically transmitted human immunodeficiency virus infection. Arch Pediatr Adolesc Med 149: 850-855.
15. Chase C, Ware J, Hittelman J, Blasini I, Smith R, Llorente A, Anisfeld E, Diaz C, Fowler MG, Moye J, Kaligh LI (2000). Early cognitive and motor development among infants born to women infected with human immunodeficiency virus. Pediatrics 106: e25.
16. Chougnet C, Kovacs A, Baker R, Mueller BU, Luban NLC, Liewehr DJ, Steinberg SM, Thomas EK, Shearer GM (2000). Influence of human immunodeficiency virus-infected maternal environment on development of infant interleukin-12 production. J Infect Dis 181: 1590-1597.
17. Clerici M, Saresella M, Colombo F, Fossati S, Sala N, Bricalli D, Villa ML, Ferrante P, Dally L, Vigano A (2000). T-lymphocyte maturation abnormalities in uninfected newborns and children with vertical exposure to HIV. Blood 96: 3866-3871.
18. Cooper ER, Hanson C, Diaz C, Mendez H, Abboud R, Nugent R, Pitt J, Rich K, Rodrigues EM, Smeriglio V (1998). Encephalopathy and progression of human immunodeficiency virus disease in a cohort of children with perinatally acquired human immunodeficiency virus infection. J Pediatr 132: 808-812.
19. Coplan J, Contello KA, Cunningham CK, Weiner LB, Dye TD, Roberge L, Wojtowycz MA, Kirkwood K (1998). Early language development in children exposed to or infected with human immunodeficiency virus. Pediatr Electronic 102: e8.
20. Coscia JM, Christensen BK, Henry RR, Wallston K, Radcliffe J, Rutstein R (2001). Effects of home environment, socioeconomic status, and health status on cognitive functioning in children with HIV-1 infection. J Pediatr Psychiatry 26: 321-329.
21. DeMaria MA, Casto M, O'Connell M, Johnson RP, Rosenzweig M (2000). Characterization of lymphocyte subsets in rhesus macaques during the first year of life. Eur J Haematol 65: 245-257.
22. Diamond GW (1989). Developmental problems in children with HIV infection. Mental Retard 27: 213-217.
23. Diamond GW, Kaufman J, Belman AL, Cohen L, Cohen HJ, Rubinstein A (1987). Characterization of cognitive functioning in a subgroup of children with congenital HIV infection. Arch Clin Neuropsychol 2: 245-256.
24. Diamond GW, Gurdin P, Wiznia AA, Bleman AL, Rubenstein A, Cohen HJ (1990). Effects of congenital HIV infection on neuro developmental status of babies in foster care. Dev Med Child Neurol 32: 999-1005.
25. Drotar D, Olness K, Wiznitzer M, Guay L, Marum L, Svilar G, Hom D, Fagan JF, Ndugwa C, Kiziri-Mayengo R (1997). Neurodevelopmental outcomes of Ugandan infants with human immunodeficiency virus type 1 infection. Pediatrics 100: E5.
26. Drotar D, Olness K, Wiznitzer M, Schatschneider C, Marum L, Guay L, Fagan J, Hom D, Svilar G, Ndugwa C, Mayengo RK (1999). Neurodevelopmental outcomes of Ugandan infants with HIV infection: an application of growth curve analysis. Health Psychol 18: 114-121.
27. Eiden LE, Rausch DM, da Cunha A, Murray EA, Heyes M, Sharer L, Nohr D, Weihe E (1993). Aids and the central nervous system. Ann N Y Acad Sci 693: 229-244.
28. Englund JA, Baker CJ, Raskino C, McKinney RE, Lifschitz MH, Petrie B, Fowler MG, Connor JD, Mendez H, O'Donnell K, Wara DW, The Aids Clinical Trials Group Protocol 152 Study Team (1996). Clinical and laboratory characteristics of a large cohort of symptomatic, human immunodeficiency virus-infected infants and children. Pediatr Infect Dis J 15: 1025-1036.
29. Epstein LG (1988). HIV infection in the newborn and child: specific effects on the nervous system. In: AIDS in children, adolescents, and heterosexual adults. Schinazi RF, and Nahmias AJ (eds). New York: Elsevier Science, pp 241-244.
30. Epstein LG, Sharer LR, Joshi VV, Fojas MR, Koenigsberger MR, Oleske JW (1984). Progressive encephalopathy in children with acquired immunodeficiency syndrome. Ann Neurol 17: 488-496.
31. Epstein LG, Sharer LR, Oleske JM, Connor EM, Goudsmit J, Bagdon L, Robert-Guroff M, Koenigsberger MR (1986). Neurologic manifestations of human immunodeficiency virus infection in children. Pediatr 78: 678-687.
32. Esposito S, Musetti L, Musetti MC, Tornaghi R, Corbella S, Massironi E, Marchisio P, Guareschi A, Principi N (1999). Behavioral and psychological disorders in uninfected children aged 6 to 11 years born to human immunoedeficiency virus-seropositive mothers. J Dev Behav Pediatr 20: 411-417.
33. Fox HS, Buchmeier MJ, Lane TE, Stenglein S, Nelson J, Prospero-Garcia O, Henriksen SJ, Gold LH, Bloom FE (1996). Infection of rhesus macaques with neuropathogenic SIV induces cognitive and electrophysiologic abnormalities: viral and host factors lead to CNS dysfunction. J NeuroVirol 2: 13.
34. Fox HS, Gold LH, Henriksen SJ, Bloom FE (1997). Simian immunodeficiency virus: a model for neuroAIDS. Neurobiol Dis 4: 265-274.
35. Gesner M, Papaevangelou V, Kim M, Chen SH, Moore T, Krasinski K, Borkowsky W (1994). Alteration in the proportion of CD4 T lymphocytes in a subgroup of human immunodeficiency-virus-exposed-uninfected children. Pediatr 93: 624-630.
36. Gold LH, Fox HS, Henriksen SJ, Buchmeier MJ, Weed MR, Taffe MA, Huitron-Resendiz S, Horn TF, Bloom FE (1998). Longitudinal analysis of behavioral, neurophysiological, viral and immunological effects of SIV infection in rhesus monkeys. J Med Primatol 27: 104-112.
37. Gurbindo D, Resino S, Sanchez-Ramon S, Leon JA, Munoz-Fernandez MA (1999). Correlation of viral load and CD8 T-lymphocytes with development of neurological manifestations in vertically HIV-1-infected infants. A prospective longitudinal study. Neuropediatrics 30: 197-204.
38. Herz AM, Robertson MN, Lynch JB, Schmidt A, Rabin M, Sherbert C, Agy MB, Anderson D, Hu SL, Greenberg PD, Morton WR (2002). Viral dynamics of early HIV infection in neonatal macaques after oral exposure to HIV-2287: an animal model with implications for maternal-neonatal HIV transmission. J Med Primatol 31: 29-39.
39. Ho RJY, Agy MB, Morton WR, Scheibel M, McClure J, Watson A, Hu SL, Nosbisch C, Dorofeeva N, Unadkat JD (1996). Development of a chronically catheterized maternal-fetal macaque model to study in utero mother-to-fetus HIV transmission: a preliminary report. J Med Primatol 25: 218-224.
40. Ho RJ, Larsen K, Kinman L, Sherbert C, Wang XY, Finn E, Nosbisch C, Schmidt A, Anderson D, Hu SL, Agy M, Ochs H, Morton WR, Unadkat JD (2001). Characterization of a maternal-fetal HIV transmission model using pregnant macaques infected with HIV-2 (287). J Med Primatol 30: 131-140.
41. Holterman L, Niphuis H, Koornstra W, Dubbes R, ten Haaft P, Heeney JL (2000). The rate of progression to AIDS is independent of virus dose in simian immunodeficiency virus-infected macaques. J Gen Virol 81: 1719-1726.
42. Horn TF, Huitron-Resendiz S, Weed MR, Henriksen SJ (1998). Early physiological abnormalities after simian immunodeficiency virus infection. Proc Nat Acad Sci U S A 95: 15072-15077.
43. 287 macaque model of AIDS. AIDS 18: 1363-1370.
44. Knight WG, Mellins CA, Levenson RL Jr., Arpadi SM, Kairam R (2000). Brief report: effects of pediatric HIV infection on mental and psychomotor development. J Pediatr Psychol 25: 583-587.
45. Kuhn L, Coutsoudis A, Moodley D, Mngqundaniso N, Trabattoni D, Shearer GM, Clerici M, Coovadia HM (2001). Interferon-gamma and interleukin-10 production among HIV-1-infected and uninfected infants of HIV-1-infected mothers. Pediatr Res 50: 412-416.
46. Kuhn L, Meddows-Taylor S, Gray G, Tiemessen C (2002). Human immunodeficiency virus (HIV)-specific cellular immune responses in newborns exposed to HIV in utero. CID 34: 267-276.
47. Lifschitz M, Hanson C, Wilson G, and Shearer WT (1989). Behavioral changes in children with human immunodeficiency virus (HIV) infection. International Conference on AIDS: Abstracts, 5, 316.
48. Lindsey JC, Hughes MD, McKinney RE, Cowles MK, Englund JA, Baker CJ, Burchett SK, Kline MW, Kovacs A, Moye J (2000). Treatment-mediated changes in human immunodeficiency virus (HIV) type 1 RNA and CD4 cell counts as predictors of weight growth failure, cognitive decline, and survival in HIV-infected children. J Infect Dis 182: 1385-1393.
49. Lobato MN, Caldwell MB, Ng P, Oxtoby MJ, Pediatric Spectrum of Disease Clinical Consortium (1995). Encephalopathy in children with perinatally acquired human immunodeficiency virus infection. J Pediatr 126: 710-715.
50. Looney DJ, McClure J, Kent SJ, Radaelli A, Kraus G, Schmidt A, Steffy K, Greenberg P, Hu SL, Morton WR, Wong-Stall F (1998). A minimally replicative HIV-2 live-virus vaccine protects M. nemestrina from disease after HIV-2(287) challenge. Virology 242: 150-160.
51. Lucas SB, Hounnou A, Peacock C, Beaumel A, Djomand G, N'Gbichi JM, Yeboue K, Honde M, Diomande M, Giordano C, Doorly R, Brattegaard K, Kestens L, Smithwick R, Kadio A, Ezani N, Yapi A, De Cock KM (1993). The mortality and pathology of HIV infection in a West African city. AIDS 7: 1569-1579.
52. Macmillan C, Magder LS, Brouwers P, Chase C, Hittelman J, Lasky T, Malee K, Mellins CA, Velez-Borras (2001). Head growth and neurodevelopment of infants born to HIV-1-infected drug-using women. J Neurol 57: 1402-1411.
53. Marcario JK, Raymond LAM, McKiernan BJ, Foresman LL, Joag SV, Raghavan R, Narayan O, Cheney PD (1999). Motor skill impairment in SIV-infected rhesus macaques with rapidly and slowly progressing disease. J Med Primatol 28: 105-117.
54. McClure J, Schmidt AM, Rey-Cuille M-A, Bannick J, Misher L, Tsai CC, Anderson DM, Morton WR, Hu SL (2000). Derivation and characterization of a highly pathogenic isolate of human immunodeficiency virus type 2 that causes rapid CD4+ cell depletion in Macaca nemestrina. J Med Primatol 29: 114-126.
55. Mellins CA, Levenson RL Jr, Zawadzki R, Kairam R, Weston M (1994). Effects of pediatric HIV infection and prenatal drug exposure on mental and psychomotor development. J Pediatr Psychol 19: 617-628.
56. Mintz M (1994). Clinical comparison of adult and pediatric NeuroAIDS. Adv Neuroimmunol 4: 207-221.
57. Mintz M (1998). Clinical features of HIV infection in children. In: The neurology of AIDS. Gendelman HE, Liption SA, Epstein L, Swindells S (eds). New York: Chapman & Hall, pp 385-407.
58. Moss HA, Bronwers PL, Wolters PL, Wiener L, Hersh S, Pizzo PA, (1994). The development of a Q-sort behavioral rating procedure for pediatric HIV patients. J Pediatr Psychol 19: 27-46.
59. Moss HA, Wolters PL, Brouwers P, Hendricks ML, Pizzo PA (1996). Impairment of expressive behavior in pediatric HIV-infected patients with evidence of CNS disease. J Pediatr Psychol 21: 379-400.
60. Moss HA, Wolters PL, Eddy J, Weiner L, Pizzo P, Brouwers P (1989). The effects of encephalopathy and AZT treatment on the social and emotional behavior in pediatric AIDS. V International Conference on AIDS: Abstracts, 5, 328.
61. Moss HA, Wolters PL, El-Amin D, Butler K, Brouwers P, Pizzo P (1990). The use of videotaped behavior samples of pediatric AIDS patients to evaluate psychosocial changes associated with encephalopathy before and after treatment. VI International Conference on AIDS: Abstracts, 6, 131.
62. Murray EA, Rausch DM, Lendvay J, Sharer LR, Eiden LE (1992). Cognitive and motor impairments associated with SIV infection in Rhesus monkeys. Science 255: 1246-1249.
63. Nielsen SD, Jeppesen DL, Kolte L, Clark DR, Sorensen TU, Dreves AM, Ersboll AK, Ryder LP, Valerius NH, Nielsen JO (2001). Impaired progenitor cell function in HIV-negative infants of HIV-positive mothers results in decreased thymic output and low CD4 counts. Blood 98: 398-404.
64. Nozyce M, Hittelman J, Muenz L, Duraki SJ, Fischer ML, Willoughby A (1994). Effect of perinatally acquired human immunodeficiency virus infection on neurodevelopment in children during the first two years of life. Pediatr 94: 883-891.
65. Pearson DA, McGrath NM, Nozyce M, Nichols SL, Raskino C, Brouwers P, Lifschitz MC, Baker CJ, Englund JA (2000). Predicting HIV disease progression in children using measures of neuropsychological and neurological functioning. Pediatrics 106: e76.
66. Pollack H, Kuchuk A, Cowan L, Hacimamutoglu S, Glasberg H, David R, Krasinski K, Borkowsky W, Oberfield S (1996). Neurodevelopment, growth, and viral load in HIV-infected infants. Brain Behav Immun 10: 298-312.
67. Pratt RD, Nichols S, McKinney N, Kwok S, Danker WM, Spector SA (1996). Virologic markers of human immunodeficiency virus type 1 in cerebrospinal fluid of infected children. J Infect Dis 174: 288-293.
68. Price RW, Brew B, Sidtis JJ, Rosenblum M, Scheck A, Cleary P (1988). The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239: 586-592.
69. Prospero-Garcia O, Gold LH, Fox HS, Polis I, Koob GF, Bloom FE, Henriksen SJ (1996). Microglia-passaged simian immunodeficiency virus induces neurophysiological abnormalities in monkeys. Proc Nat Acad Sci U S A 93: 14158-14163.
70. Rausch DM, Heyes MP, Eiden LE (1994a). Effects of chronic zidovudine administration on CNS function and virus burden after perinatal SIV infection in rhesus monkeys. Adv Neuroimmunol 4: 233-237.
71. Rausch DM, Heyes MP, Murray EA, Eiden LE (1995). Zidovudine treatment prolongs survival and decreases virus load in the central nervous system of Rhesus macaques infected perinatally with simian immunodeficiency virus. J Infect Dis 172: 59-69.
72. Rausch DM, Heyes MP, Murray EA, Lendvay J, Sharer LR, Ward JM, Rehm S, Nohr D, Weibe E, Eiden LE (1994b). Cytopathologic and neurochemical correlates of progression to motor/cognitive impairment in SIV-infected rhesus monkeys. J Neuropathol Exp Neurol 53: 165-175.
73. Raymond LAM, Wallace D, Marcario JK, Raghavan R, Narayan O, Foresman LL, Berman NEJ, Cheney PD (1999). Motor evoked potentials in a rhesus macaque model of neuro-AIDS. J NeuroVirol 5: 217-231.
74. Ruppenthal GC, Sackett GP (1992). Research protocol and technician's manual: a guide to the care, feeding and evaluation of infant monkeys. Seattle, WA: The Infant Primate Research Laboratory.
75. Schwarcz SK, Rutherford GW (1989). Acquired immunodeficiency syndrome in infants, children and adolescents. J Drug Issues 19: 75-92.
76. Scott GB, Hutto C, Makuch RW, Mastrucci MT, O'Conner T, Mitchell CD, Trapido EJ, Parks WP (1989). Survival in children with perinatally acquired human immunodeficiency virus type I infection. N Engl J Med 321: 1791-1796.
77. Sharer LR, Epstein LG, Cho ES, Joshi VV, Meyenhofer MF, Rankin LF, Petito CK (1986). Pathologic features of AIDS encephalopathy in children: evidence for LAV/HTLV-III infection of the brain. Human Pathol 17: 271-284.
78. Sharer LR, Saito Y, Blumberg BM (1997). Neuropathology of Human Immunodeficiency Virus-1 infection of the brain. In: Aids and the nervous system, 2nd ed. Berger JR and Levy RM (eds). Philadelphia: Lippincott-Raven Publishers, 461-479.
79. Smith R, Malee K, Charurat M, Magder L, Mellins C, MacMillan C, Hittleman J, Lasky T, Llorente A, Moye J (2001). Timing of perinatal human immunodeficiency virus type 1 infection and rate of neurodevelopment. Pediatr Infect Dis J 19: 862-871.
80. Tardieu M, Mayaux MJ, Seibel N, Funck-Brentano I, Straub E, Teglas JP, Blanche S (1995). Cognitive assessment of school-age children infected with maternally transmitted human immunodeficiency virus type 1. J Pediatr 126: 375-379.
81. Tardieu M, Chenadec JL, Persoz A, Meyer L, Blanche S, Mayaux MJ (2000). Hiv-1-related encephalopathy in infants compared with children and adults. Neurol 54: 1089-1095.
82. Terao K, Rose LM, Sackett GP, Clark EA (1988). Development of lymphocyte subsets in pigtailed macaques. Human Immunol 21: 33-48.
83. Tovo PA, de Martino M, Gabiano C, Cappello N, D'Elia R, Loy A, Plebani A, Zuccotti GV, Dallacasa P, Ferraris G, Caselli D, Fundaro' C, D'Argenio P, Galli L, Principi N, Stegagno M, Ruga E, Palomba E, The Italian Register for HIV Infection in Children (1992). Prognostic factors and survival in children with perinatal HIV-1 infection. Lancet 339: 1249-1253.
84. Watson A, McClure J, Ranchalix J, Scheibel M, Schmidt A, Kennedy B, Morton WR, Haigwood NL, Hu SL (1997). Early postinfection antiviral treatment reduces viral load and prevents CD4+ cell decline in HIV type 2-infected macaques. AIDS Res Hum Retroviruses 13: 1375-1381.
85. Westmoreland SV, Williams KC, Simon MA, Bahn ME, Rullkoetter AE, Elliott MW, deBakker CD, Knight HL, Lackner AA (1999). Neuropathogenesis of simian immunodeficiency virus in neonatal rhesus macaques. Am J Pathol 155: 1217-1228.
86. Wilkins JW, Robertson KR, van der Horst C, Robertson WT, Fryer JG, Hall CD (1990). The importance of confounding factors in the evaluation of neuropsychological changes in patients infected with human immunodeficiency virus. J Acquir Immune Defic Synd 3: 938-942.
87. Wolters PL, Brouwers P, Moss HA, Pizzo PA (1994). Adaptive behavior of children with symptomatic HIV infection before and after Zidovudine therapy. J Pediatr Psychol 19: 47-61.
88. Worlein JM, Ha JC, Harris C, Leigh J, Stratton K, Ho JR (in press). Special challenges of rearing infant macaques infected with lentivirus (SIV, HIV, SH1V). In: Developments in primatology: progress and prospects. Sackett GP and Ruppenthal G (eds).
89. Worlein JM, Sackett GP (1997). Social development in nursery-reared infant pigtailed macaques (Macaca nemestrina). Am J Primatol 41: 23-35.