by Pepin
Following the 1969 Stonewall riots, a gay rights movement emerged in the US, and San Francisco became its focal point where 5,000 homosexuals migrated each year, in search of freedom and tolerance. By 1978, 6% of gay men in San Francisco were HIV-infected. The same year, through some of them who donated blood, HIV entered the local blood supply. The extraordinary level of sexual promiscuity within this population, recently liberated from centuries of repression and stigmatisation, led to an exponential homosexual amplification of HIV-1. Many of the initial cohorts of HIV-1-infected gay men had 100–200 sexual partners per year, most often during anonymous encounters in bathhouses. HIV prevalence among San Francisco gay men increased to 19% in 1979, 33% in 1980 and 44% in 1981. The incidence peaked around July 1981, when 1.4% of gay men acquired HIV infection each month.25,29–31
HIV infections were identified retrospectively among American haemophiliacs starting in 1978, but the virus may have been present at a low prevalence for some years. It was already infecting some British haemophiliacs by 1979. In a cohort of American haemophiliacs, just a few with stored serum going back to 1976, the first case of HIV infection appeared in 1978, with rapid spread in 1981–2. More than half of haemophiliacs in Georgia were HIV-infected by 1981, as were 85% of their Californian counterparts by 1984. The first cases of AIDS among haemophiliacs were recognised in early 1982.32–35
Thus by the late 1970s in the US several modes of HIV transmission acted concomitantly, to a large extent independently of each other but with occasional interconnections. Haemophiliacs who happened to be gay might have sexually infected other gay men and homosexually infected men might have been volunteer blood donors or paid plasma donors. This latter step diversified the sources of HIV-1 which from multiple sites now entered the complex process that led to the production of coagulation factor concentrates made from pools of plasma collected from thousands of donors, by then hugely popular among haemophiliacs and their physicians. The all-male haemophiliacs were otherwise healthy and, if old enough, sexually active. Some infected their female spouses (who in turn could infect their infants) but, because the average number of concomitant sexual partners was low, these became epidemiological dead ends. Although a tragedy with almost half of the 20,000 American haemophiliacs infected, this had only a modest impact on the overall picture. Whole blood transfusions did not contribute much to the overall dissemination of the virus either, because most recipients were sick or elderly individuals undergoing heart surgery or being treated for leukaemia or some other nasty disease, who were not active sexually in the ensuing months. Furthermore, because of the massive infective dose, transfusion recipients developed AIDS and died within just a few years. HIV-1 transmission among drug addicts was more consequential: to generate the income needed for their dope, some addicts sold sexual services or became paid plasma donors, others happened to be gay and infected their sexual partners, and female addicts could infect their offspring.
During the 1970s, there was much dissemination of HIV by gay men visiting other cities where they had unprotected sex. The case of the Air Canada flight attendant, the so-called ‘patient zero’, who was linked to many early cases of AIDS in various American cities, has been described in detail elsewhere. Mobility and promiscuity proved excellent breeding grounds for a sexually transmitted virus, allowing exponential transmission by men who continued having sex with other gay men shortly after they developed a high viraemia during their primary HIV period. Transmission was further facilitated by the high prevalence of other sexually transmitted pathogens within the homosexual community. In this early phase of the epidemic in the US, in all risk groups combined, each HIV-infected person infected another person every year or so. From the United States, the virus was re-exported to many parts of the industrialised world.36,37
Eventually, after an incubation period of roughly ten years during which their CD4 lymphocytes were progressively destroyed, these early American patients developed a variety of opportunistic infections and a new disease was recognised by the physicians who published the landmark MMWR short article in 1981. And thus AIDS was born.
15 Epilogue: lessons learned
Twenty-nine million deaths later, are there any useful lessons that can be drawn from this tragedy? Or was it just an extraordinary confluence of chance events, unlikely ever to be repeated? In retrospect, two factors probably drove the emergence of SIVcpz into HIV-1. Even if their respective contributions will never be fully sorted out, there is little doubt that without them the pandemic would not have developed.
The first was the profound social changes that accompanied the European colonisation of central Africa, eventually leading to sexual behaviours far different from those of traditional societies which had lived there for 2,000 years. A relatively small number of women had sex against remuneration, initially with a few regular clients, and then, after 1960, with a large number of men, a process which amplified the transmission of sexually transmitted pathogens, both the traditional ones (gonorrhoea, syphilis, etc.) and the emerging one, HIV-1. This is just another example of the complex relationships between social changes and diseases. Tuberculosis emerged as an important cause of adult mortality in nineteenth-century Europe, when the industrial revolution brought many poor peasants to the cities where they lived in crowded, unhealthy conditions conducive to the transmission of this respiratory pathogen. More recently, in the last decades of the twentieth century, an unprecedented epidemic of obesity has developed in industrialised countries as a consequence of our sedentarisation, itself driven by the ever-increasing availability of motor vehicles, televisions, video games, the Internet, and so on. Upcoming changes in the lifestyle of future generations will impact on the incidence of various diseases, in a way which is hard to predict and which cannot be avoided. Some of these changes could be detrimental to the human race, while others will represent progress. For instance, the progressive reduction in the use of fossil fuels and their replacement by greener sources of energy should eventually lower the incidence of the respiratory diseases associated with air pollution.
The second factor in the emergence of SIVcpz into HIV-1 was its parenteral amplification through poorly sterilised syringes and needles, re-used on many patients. In central Africa, this may have jump-started the epidemic by increasing the number of infected humans to a level where sexual transmission could thrive. In retrospect, this iatrogenic amplification resulted from a lag of only about fifty years between the development of therapeutic agents that required their IV administration and the realisation that infectious agents, especially viruses, could be transmitted by this route. When humans manipulate nature in a way that they do not fully understand, there is always a possibility that something unpredictable will occur.
This is a reminder that the most dangerous threat to the long-term survival of the human species is the human race itself. Of course, this has been obvious for some time. My generation and the one before us grew up with the fear of a nuclear holocaust. Even though the number of nuclear missiles has been reduced, the list of countries possessing this technology has grown, and with it the probability that one day somebody will push the button. My children’s generation has grown up with the threat of global warming, a process whose consequences could be as destructive, albeit much slower. The human race is not very quick to understand novel threats. Just a few years ago, the president of the United States refused to ratify the Kyoto protocol on the basis that the ‘American way of life is not negotiable’, as if the core of American civilisation and values were the four-wheel drive vehicles produced by three large corporations that barely survived the end of this president’s term in office.
In this context, the one new message that the HIV epidemic, as chronicled in this book, should bring home is that well-intentioned human interventions can have unpredictable and disastrous microbiologic consequences. Mankind has emerged through a process of natural selection over billions of years. Apart from ourselves, there is probably no other living organism on eart
h that could destroy us completely, because if such organisms had existed, we would not have managed to reach our current status in the first place. But as I write these lines, there is renewed interest in sending humans on a wonderful voyage to Mars and back. The kids who watched Neil Armstrong’s small steps on the moon are now engineers, pilots, administrators and politicians. They think that their own generation also needs to push back a new frontier, that this is part of the human experience, and perhaps something that will provide an answer to perennial questions about the meaning of life. For a long time I have thought that space adventures were very unwise. What is the point of setting up a small human colony somewhere in orbit around the earth or even further away, when we are systematically destroying, day in and day out, the only planet which can sustain human life? Would it not be smarter to spend our resources and ingenuity on scientific adventures whose purpose would be to protect our earth rather than taking the risk of importing into our cherished planet a completely different form of microscopic life, perhaps not even based on DNA, and whose innocuous nature has not been proven by billions of years of natural selection and co-evolution with us?
References
Introduction
1. Gottlieb M et al. Pneumocystis carinii pneumonia – Los Angeles. MMWR (1981), 30: 250–2.
2. Shilts R. And the band played on. Politics, people and the AIDS epidemic. New York: Penguin Books, 1987.
3. UNAIDS. Global Report. UNAIDS report on the global AIDS epidemic – 2010. Geneva, 2010.
4. UNAIDS. AIDS epidemic update 2009. Geneva, 2009.
5. Garrett L. The coming plague. Newly emerging diseases in a world out of balance. New York: Penguin Books, 1994.
6. Illiffe J. The African AIDS epidemic. A history. Athens: Ohio University Press, 2006.
7. Fassin D. When bodies remember. Experiences and politics of AIDS in South Africa. Berkeley: University of California Press, 2007.
8. Mukudi E et al. HIV/AIDS in Africa. Challenges and impact. Trenton: Africa World Press, 2008.
9. Nolen S. 28 stories of AIDS in Africa. Toronto: Vintage Canada, 2008.
10. Denis P et al. L’épidémie du sida en Afrique subsaharienne. Paris: Karthala, 2006.
11. Hooper E. The river. A journey back to the source of HIV and AIDS. London: Little Brown and Company, 1999.
12. Pepin J et al. Parenteral transmission during excision and treatment of tuberculosis and trypanosomiasis may be responsible for the HIV-2 epidemic in Guinea-Bissau. AIDS (2006), 20: 1303–11.
13. Schmid GP et al. Transmission of HIV-1 infection in sub-Saharan Africa and effect of elimination of unsafe injections. Lancet (2004), 363: 482–8.
1 Out of Africa
1. Piot P et al. AIDS in a heterosexual population in Zaire. Lancet (1984), 2: 65–9.
2. Van de Perre P et al. Female prostitutes: a risk group for infection with HTLV-III. Lancet (1985), 2: 524–7.
3. Quinn T et al. AIDS in Africa: an epidemiologic paradigm. Science (1986), 234: 955–63.
4. Desmyter J et al. Anti LAV-HTLV-III in Kinshasa mothers in 1970 and 1980. Paris: International Conference on AIDS, June 1985.
5. Nzila N et al. The prevalence of infection with HIV over a 10-year period in rural Zaire. N Eng J Med (1988), 318: 276–9.
6. Byers R et al. Estimating AIDS infection rates in the San Francisco cohort. AIDS (1988), 2: 207–10.
7. Foley B et al. Apparent founder effect during the early years of the San Francisco HIV-1 epidemic (1978–79). AIDS Res Hum Retrovir (2000), 15: 1463–9.
8. Moore JD et al. HTLV-III seropositivity in 1971–72 parenteral drug abusers – a case of false positives or evidence of viral exposure. N Eng J Med (1986), 314: 1387–8.
9. Garrett L. The coming plague. Newly emerging diseases in a world out of balance. New York: Penguin Books, 1994.
10. Anonymous. Ebola haemorrhagic fever in Zaire, 1976. Report of an international commission. Bull World Health Organ (1978), 56: 271–93.
11. Wendler I et al. Seroepidemiology of HIV in Africa. Br Med J (1986), 293: 782–5.
12. Kawamura M. HIV-2 in West Africa in 1966. Lancet (1989), 1: 385.
13. Chiodi F et al. Screening of African sera stored for more than 17 years for HIV antibodies by site-directed serology. Europ J Epidemiol (1989), 5: 42–6.
14. US Census Bureau. HIV/AIDS surveillance data base. Washington, 2006.
15. Otu A et al. Antibody to the AIDS virus in Kaposi’s sarcoma in Nigeria. J Surg Oncol (1988), 37: 152–5.
16. Levy J et al. Absence of antibodies to HIV in sera from Africa prior to 1975. Proc Natl Acad Sci U S A (1986), 83: 7935–7.
17. Tabor E et al. Did HIV and HTLV originate in Africa? JAMA (1990), 264: 691–2.
18. Sher R et al. Seroepidemiology of HIV in Africa from 1970 to 1974. N Eng J Med (1987), 317: 50–1.
19. Piot P et al. Retrospective seroepidemiology of AIDS virus infection in Nairobi populations. J Infect Dis (1987), 155: 1108–12.
20. Vangroenweghe D. The earliest cases of HIV-1 group M in Congo-Kinshasa, Rwanda and Burundi and the origin of AIDS. Phil Trans R Soc Lond B (2001), 356: 923–5.
21. Lyons H et al. Pneumocystis carinii pneumonia unassociated with other disease. Arch Intern Med (1961), 108: 929–36.
22. Hooper E. The river. A journey back to the source of HIV and AIDS. London: Little Brown and Company, 1999.
23. Shilts R. And the band played on. Politics, people and the AIDS epidemic. New York: Penguin Books, 1987.
24. Froland S. HIV-1 infection in a Norwegian family before 1970. Lancet (1988), 1: 1344–5.
25. Jonassen T et al. Sequence analysis of HIV-1 group O from Norwegian patients infected in the 1960s. Virol (1997), 231: 43–7.
26. Bygbjerg I. AIDS in a Danish surgeon (Zaire 1976). Lancet (1983), 1: 925.
27. Nemeth A et al. Early case of AIDS in a child from Zaire. Sex Transm Dis (1986), 13: 111–13.
28. Rogan E et al. A case of AIDS before 1980. Can Med Assoc J (1987), 137: 637–8.
29. Sonnet J et al. Early AIDS cases originating from Zaire and Burundi (1962–1976). Scand J Infect Dis (1987), 19: 511–17.
30. Clumeck N et al. AIDS in African patients. N Eng J Med (1984), 310: 492–7.
31. Motulsky A et al. Population genetics study in the Congo. I. Glucose-6-phosphate deficiency, hemoglobin S, and malaria. Am J Hum Genet (1966), 18: 514–37.
32. Nahmias A et al. Evidence for human infection with HTLV-III/LAV-like virus in Central Africa, 1959. Lancet (1986), 1: 1279–80.
33. Zhu T et al. An African HIV-1 sequence from 1959 and implications for the origin of the epidemic. Nature (1998), 391: 594–7.
34. Worobey M et al. Direct evidence of extensive diversity of HIV-1 in Kinshasa by 1960. Nature (2008), 55: 661–4.
35. Geretti A. HIV-1 subtypes: epidemiology and significance for HIV management. Curr Opin Infect Dis (2006), 19: 1–7.
36. Butler I et al. HIV genetic diversity: biological and public health consequences. Curr HIV Res (2007), 5: 23–45.
37. Los Alamos National Laboratory. The circulating recombinant forms. www.hiv.lanl.gov/content/sequence/HIV/CRFs/CRFs.html.
38. Paleebu P et al. Effect of HIV-1 envelope subtypes A and D on disease progression in a large cohort of HIV-1 positive persons in Uganda. J Infect Dis (2002), 185: 1244–50.
39. John-Stewart G et al. Subtype C is associated with increased vaginal shedding of HIV-1. J Infect Dis (2005), 192: 492–6.
40. Novitsky V et al. Viral load and CD4+ T-cell dynamics in primary HIV-1 subtype C infection. JAIDS (2009), 50: 65–76.
41. Vidal N et al. Distribution of HIV-1 variants in the Democratic Republic of Congo suggests increase of subtype C in Kinshasa between 1997 and 2002. JAIDS (2005), 40: 456–62.
42. Salemi M et al. Different epidemic potentials of the HIV-1 B and C subtypes. J Mol Evol (2005), 60: 598–605.
43. van Harmelen J et al. An association between HIV-1 subtypes and mode of transmission in Cape Town, South Africa. AIDS
(1997), 11: 81–7.
44. Taylor B et al. The challenge of HIV-1 subtype diversity. N Eng J Med (2008), 358: 1590–602.
45. Peeters M et al. Genetic diversity of HIV in Africa: impact on diagnosis, treatment, vaccine development and trials. AIDS (2003), 17: 2547–60.
46. Hemelaar J et al. Global and regional distribution of HIV-1 genetic subtypes and recombinants in 2004. AIDS (2006), 20: W13–W23.
