HIV transmission risk through anal intercourse: systematic review, meta-analysis and implications for HIV prevention.
BACKGROUND
The human immunodeficiency virus (HIV) infectiousness of anal intercourse (AI) has not been systematically reviewed, despite its role driving HIV epidemics among men who have sex with men (MSM) and its potential contribution to heterosexual spread. We assessed the per-act and per-partner HIV transmission risk from AI exposure for heterosexuals and MSM and its implications for HIV prevention.


METHODS
Systematic review and meta-analysis of the literature on HIV-1 infectiousness through AI was conducted. PubMed was searched to September 2008. A binomial model explored the individual risk of HIV infection with and without highly active antiretroviral therapy (HAART).


RESULTS
A total of 62,643 titles were searched; four publications reporting per-act and 12 reporting per-partner transmission estimates were included. Overall, random effects model summary estimates were 1.4% [95% confidence interval (CI) 0.2-2.5)] and 40.4% (95% CI 6.0-74.9) for per-act and per-partner unprotected receptive AI (URAI), respectively. There was no significant difference between per-act risks of URAI for heterosexuals and MSM. Per-partner unprotected insertive AI (UIAI) and combined URAI-UIAI risk were 21.7% (95% CI 0.2-43.3) and 39.9% (95% CI 22.5-57.4), respectively, with no available per-act estimates. Per-partner combined URAI-UIAI summary estimates, which adjusted for additional exposures other than AI with a 'main' partner [7.9% (95% CI 1.2-14.5)], were lower than crude (unadjusted) estimates [48.1% (95% CI 35.3-60.8)]. Our modelling demonstrated that it would require unreasonably low numbers of AI HIV exposures per partnership to reconcile the summary per-act and per-partner estimates, suggesting considerable variability in AI infectiousness between and within partnerships over time. AI may substantially increase HIV transmission risk even if the infected partner is receiving HAART; however, predictions are highly sensitive to infectiousness assumptions based on viral load.


CONCLUSIONS
Unprotected AI is a high-risk practice for HIV transmission, probably with substantial variation in infectiousness. The significant heterogeneity between infectiousness estimates means that pooled AI HIV transmission probabilities should be used with caution. Recent reported rises in AI among heterosexuals suggest a greater understanding of the role AI plays in heterosexual sex lives may be increasingly important for HIV prevention.
Baggaley
Rebecca F
RF
Department of Infectious Disease Epidemiology, MRC Centre for Outbreak Analysis and Modelling, Faculty of Medicine, Imperial College London, Paddington, London, UK. r.baggaley@imperial.ac.uk
White
Richard G
RG
Boily
Marie-Claude
MC
D023241:Antiretroviral Therapy, Highly Active; D005260:Female; D015658:HIV Infections / Q000188:drug therapy* / Q000635:transmission*; D006801:Humans; D008297:Male; D011336:Probability; D012306:Risk; D012725:Sexual Behavior; D047568:Unsafe Sex
Sex Transm Dis. 1997 Jan;24(1):11-7
9018778
Arch Sex Behav. 2000 Aug;29(4):357-73
10948725
AIDS Patient Care STDS. 1999 Dec;13(12):717-30
10743535
Lancet Infect Dis. 2009 Feb;9(2):118-29
19179227
Lancet Infect Dis. 2008 Sep;8(9):553-63
18684670
AIDS. 2009 Jul 17;23(11):1397-404
19381076
J Infect Dis. 2007 Dec 15;196(12):1852-9
18190267
Int J STD AIDS. 2000 Jul;11(7):468-73
10919490
Am J Epidemiol. 1997 Aug 15;146(4):350-7
9270414
Sex Transm Infect. 2009 Oct;85(6):411-5
19429569
Int J STD AIDS. 2003 Dec;14(12):856
14678597
Am J Epidemiol. 1999 Aug 1;150(3):306-11
10430236
J Acquir Immune Defic Syndr. 2002 Apr 15;29(5):484-94
11981365
Am J Epidemiol. 1995 Sep 1;142(5):538-47
7677133
AIDS. 1993 Sep;7(9):1247-54
8216983
Sex Transm Infect. 2009 Oct;85(6):408-10
19826062
AIDS Res Hum Retroviruses. 1987;3(4):355-61
3502325
Am J Epidemiol. 1998 Jul 1;148(1):88-96
9663408
Epidemiology. 1994 Nov;5(6):570-5
7841237
J Acquir Immune Defic Syndr (1988). 1990;3(1):55-61
2293643
AIDS. 2008 Oct 18;22(16):2179-85
18832881
J Pediatr Adolesc Gynecol. 2007 Oct;20(5):299-304
17868897
Sex Transm Dis. 1987 Jan-Mar;14(1):44-7
2951878
Sex Transm Dis. 2002 Jan;29(1):44-9
11773878
JAMA. 1987 Aug 14;258(6):788-90
3475478
J Acquir Immune Defic Syndr. 2007 Aug 1;45(4):454-67
17554215
Ann Intern Med. 1987 Nov;107(5):763-6
2821863
AIDS. 1996 Dec;10(14):1749-51
8970705
Health Psychol. 1999 Jan;18(1):37-43
9925044
Am J Public Health. 1990 Apr;80(4):465-6
2316770
J Acquir Immune Defic Syndr (1988). 1992 Dec;5(12):1204-11
1453331
N Engl J Med. 1994 Aug 11;331(6):341-6
8028613
Ann Intern Med. 2007 Apr 17;146(8):591-601
17438318
J Clin Immunol. 1987 Mar;7(2):130-9
3033011
Genitourin Med. 1986 Jun;62(3):177-80
3015772
Int J Epidemiol. 2008 Dec;37(6):1255-65
18664564
Ethiop Med J. 2007 Jan;45(1):103-7
17642165
Lancet. 2009 Jan 3;373(9657):48-57
19038438
J Infect Dis. 2008 Sep 1;198(5):687-93
18662132
AIDS. 1997 Nov 15;11(14):1765-72
9386812
Lancet. 1984 Sep 1;2(8401):477-80
6147546
Int J STD AIDS. 2000 Dec;11(12):804-11
11138916
AIDS. 2006 Jan 2;20(1):123-5
16327330
AIDS. 2008 May 31;22(9):1071-7
18520351
Am J Med. 1993 Jul;95(1):86-100
8328502
Lancet. 1984 Sep 1;2(8401):480-3
6147547
AIDS. 2001 Oct 19;15(15):2057-60
11600841
Am J Health Behav. 2003 May-Jun;27(3):228-34
12751619
AIDS. 2008 Jul;22 Suppl 1:S149-59
18664947
Sex Transm Dis. 2008 Nov;35(11):905-9
18685549
Sex Transm Dis. 2002 Dec;29(12):818-27
12466726
AIDS Care. 1998 Oct;10(5):571-82
9828954
AIDS. 2008 Dec;22 Suppl 5:S69-79
19098481
J Med Virol. 1987 May;22(1):91-8
3108451
JAMA. 2000 Apr 19;283(15):2008-12
10789670
Int J STD AIDS. 2003 Jul;14(7):431-6
12869220
Cult Health Sex. 2008 Jun;10(5):513-27
18568873
Am J Epidemiol. 1993 Apr 15;137(8):899-908
8484381
AIDS. 1989 Jun;3(6):367-72
2502150
J Acquir Immune Defic Syndr (1988). 1994 Nov;7(11):1169-84
7932084
Int J STD AIDS. 2002 Oct;13(10):657-66
12396534
Sex Transm Infect. 2006 Oct;82(5):392-6
16790563
Infect Agents Dis. 1995 Dec;4(4):273-84
8665090
Sex Transm Dis. 2005 Nov;32(11):710-7
16254547
J Acquir Immune Defic Syndr (1988). 1990;3(6):631-43
2338619
AIDS. 1992 Jan;6(1):101-7
1543552
J Clin Epidemiol. 1989;42(9):849-56
2789269
Nature. 1987 Mar 12-18;326(6109):137-42
3821890
AIDS. 2008 Dec;22 Suppl 5:S117-25
19098472
J Acquir Immune Defic Syndr. 2000 Aug 1;24(4):393-8
11015157
Br J Clin Pract. 1992 Winter;46(4):256-7
1290735
N Engl J Med. 2000 Mar 30;342(13):921-9
10738050
Sante. 1999 Mar-Apr;9(2):101-9
10377497
Adv Data. 2005 Sep 15;(362):1-55
16250464
Am J Epidemiol. 1988 Oct;128(4):729-39
3421239
Am J Public Health. 1988 Aug;78(8):944-8
3389432
Lancet. 2008 Nov 22;372(9652):1806-7; author reply 1807
19027479
Lancet Infect Dis. 2008 Nov;8(11):685-97
18992405
Stat Med. 1991 Jan;10(1):131-9
2006351
Lancet. 2002 Sep 28;360(9338):971-7
12383665
Arch Intern Med. 1991 Dec;151(12):2411-6
1684098
Sex Transm Dis. 2007 Oct;34(10):815-9
17551414
Int J STD AIDS. 2004 Jul;15(7):442-52
15228728
Lancet. 2008 Jul 26;372(9635):314-20
18657710
AIDS. 2004 Jan 2;18(1):81-8
15090833
J Infect Dis. 1987 Jul;156(1):189-93
3474298
AIDS Res Hum Retroviruses. 2001 Jul 1;17(10):901-10
11461676
J Acquir Immune Defic Syndr. 2005 Mar 1;38(3):241-53
15735440
Lancet. 2001 Dec 1;358(9296):1835-42
11741621
Am J Public Health. 1998 Aug;88(8):1265-6
9702169
Proc Natl Acad Sci U S A. 2007 Oct 30;104(44):17441-6
17954909
J Infect Dis. 1995 Sep;172(3):691-7
7658060
Lancet. 2008 Dec 6;372(9654):1977-87
19059048
BMJ. 2003 Sep 6;327(7414):557-60
12958120