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6

The Penetration of the West

The penetration of HIV-1 from the equatorial region into West Africa differed markedly from its expansion to the east and south. Except in Côte d’Ivoire, it was more gradual and less complete, reaching in the early 2000s prevalences only one-fifth or one-sixth of the highest elsewhere. The reasons for this are unclear but probably include obstacles to overland mobility from east to west, the wider economic opportunities open to West African women in towns, widespread male circumcision, relatively low HSV-2 prevalences, and the barriers to infection presented by Islamic moral and marital patterns. Another difference, of less certain relevance, was that when the HIV-1 virus entered West Africa, it found HIV-2 already established.

As a human disease, HIV-2 was probably older than HIV-1. It was closely related to the simian immunodeficiency virus found in sooty mangabey monkeys (SIVsm) living only in the West African forest region between the Casamance River in Senegal and the Sassandra River in Côte d’Ivoire, which was also the endemic location of the human virus. HIV-2 shared some 70 per cent of its genome with SIVsm but only about 42 per cent with HIV-1. Indeed, some of the eight groups of HIV-2 known in 2004 were more like SIVsm than they were like one another. This was because SIVsm was very widespread and diverse (although completely harmless) in sooty mangabey monkeys and because each HIV-2 group was probably the result of a separate transmission from a monkey.¹ Of the eight groups, six had failed to establish themselves in human beings, having infected only seven known cases between them. Of the two more successful, group A was the more common throughout the coastal region west of Côte d’Ivoire, while group B was found chiefly in Côte d’Ivoire and Ghana, although scattered cases of both existed elsewhere.² A study using molecular clock techniques estimated that the most recent common ancestor of group A existed in 1940±16 and of group B in 1945±14.³ Yet, given the high prevalence of SIV among sooty mangabeys, their close interaction with human beings, and the frequency of twentieth-century transmissions, similar transmissions had probably taken place in earlier centuries.

This was more likely with HIV-2 than HIV-1 because HIV-2 was a less virulent and visible disease in human beings, possibly because its progenitor was so fully adapted to monkeys. HIV-2 was about three times more difficult than HIV-1 to transmit through sexual intercourse and at least ten times more difficult to pass from mother to child.⁴ Mortality from HIV-2 may have been only about one-third of that from HIV-1, for viral loads were generally lower, those infected were often older, and progression to Aids might take on average as much as 25 years, so that many of those infected never reached that stage, although if they did the final illness was similar.⁵ Given that the opportunistic infections fatal to Aids patients were often those common to the local disease environment, it was understandable that HIV-2 passed unnoticed until 1985, when researchers investigating the existence of HIV-1 in Senegal discovered the other virus almost by chance.⁶ This probably explains why HIV-1 and HIV-2 appear to have emerged virtually simultaneously: the appearance is an optical illusion.

Once the discovery was made, retrospective testing of the earliest stored blood for HIV-2 antibodies revealed an intriguing pattern.⁷ Apart from one obscure reference to an alleged case in Mali in 1957, the earliest may have been a Portuguese man who had lived in Guinea-Bissau between 1956 and 1966. Other infections there during the 1960s are also recorded. Five cases were found in Côte d’Ivoire during the 1960s. Stored blood taken in 1967 also revealed two cases each in Nigeria and Gabon, both outside the range of sooty mangabeys and presumably infected through travel. They were followed in the 1970s by infections from Mali, Senegal, and Angola, the last probably transmitted through the movement of Portuguese troops from Guinea-Bissau. By the 1980s scattered cases were reported from many parts of western Africa, often from the countryside, suggesting a low-intensity disease much like HIV-1 in its pre-epidemic days in western equatorial Africa. In Guinea-Bissau, however, the liberation war of 1960–74, the presence of Portuguese troops, the movement of refugees, and perhaps especially the widespread use of injections by Portuguese military doctors appear to have bred a localised and probably unique epidemic.⁸ Hospitals in Portugal later treated many cases contracted in Guinea-Bissau at this time. A study in Bissau town in the late 1990s showed that levels of infection peaked among men in their sixties and women in their fifties who would have been sexually most active during the 1960s. Prevalence there among men who had served in the Portuguese army was 23 per cent; among the nineteen women who had had sex with white men it was 37 per cent. This wartime legacy gave Guinea-Bissau much the highest prevalence of HIV-2. In the mid 1980s, 26 per cent of paid blood donors there tested positive, as did 8.6 per cent of Bissau’s pregnant women and 36.7 per cent of its sex workers in 1987.⁹ Ten years later HIV-2 infected 13.5 per cent of people over 35 living on the outskirts of the town. High levels were also reported in rural areas and spilled over (largely through migrant sex workers) to southern Senegal and The Gambia.¹⁰ Yet the epidemic never spread beyond this region. That would presumably have required a virus more infectious than HIV-2.

HIV-1 was such a virus. Its arrival in West Africa (as distinct from western equatorial Africa) is difficult to trace but possibly took place in about 1980, slightly after its appearance in East and Central Africa. A claim to have discovered one case in stored blood taken in Burkina in 1963 can almost certainly be dismissed. A Malian migrant who had never visited equatorial Africa died in Paris in 1983 with Aids-like symptoms, although this could as well have been HIV-2 as HIV-1. Ghanaian doctors came to believe that they had seen Aids cases as early as 1981, but no details are available and HIV-2 would again have been possible.¹¹ Otherwise, the earliest evidence comes from Côte d’Ivoire. Retrospective tests on stored blood taken there between 1970 and 1983 all proved negative. Adult mortality in Abidjan declined until 1985, the year when its first Aids cases were diagnosed, and then began to increase rapidly. In 1985, 38 of 79 sex workers were found to be infected there, together with 10 of 71 in the northern Ivoirian town of Korhogo. A year later HIV-1 prevalence was 3.0 per cent among pregnant women and 4.9 per cent among hospital staff in Abidjan. French researchers concluded that the first HIV infections there probably took place in about 1980.¹² Observers suggested at the time that the city’s sex workers might have been infected by European tourists, but this is unlikely because the B subtype of HIV-1 prevalent in Europe did not become established in Abidjan or elsewhere in West Africa. Rather, the dominant strain came to be CRF02_AG, the circulating recombinant form rare in the DR Congo but common in Cameroun and Gabon, implying a northward diffusion comparable to the eastward diffusion of subtypes A and D into East Africa – a diffusion that in West Africa could have been carried in the first instance along the coast by sex workers and their clients moving between Libreville, Douala, and Abidjan. CRF02_AG became dominant among West Africa’s coastal sex workers, throughout Côte d’Ivoire (where in the late 1990s it was responsible for over 90 per cent of HIV-1 infections), in southern Nigeria (causing 70 per cent of the entire country’s infections), and in most coastal areas as far west as Senegal.¹³ In some inland savanna regions, including northern Nigeria, another recombinant form, CRF06_cpx, was sometimes more common (cpx signifying a complex of more than two subtypes).¹⁴

Map 4 West Africa

There were several reasons why Abidjan and Côte d’Ivoire should have become the focus of West Africa’s HIV-1 epidemic. Neglected until late in the colonial period but endowed with vast areas of virgin tropical forest, Côte d’Ivoire experienced rapid development during the first two decades of independence, with a 6.8 per cent annual growth rate of real Gross Domestic Product between 1965 and 1980.¹⁵ Sparsely populated, its prosperity attracted immigrants both from economically faltering neighbours like Ghana and from the poorer savanna countries to the north. By the late 1980s some two million migrants from Burkina, over one million from Mali, and large numbers from Niger were present in Côte d’Ivoire at any time. Although many migrants worked in agriculture, over half lived in cities, especially in Abidjan, whose development as a major port increased its population between 1955 and 1984 from 120,000 to nearly 1,800,000. In 1975 some 40 per cent were non-Ivoirian immigrants. In older West African cities the control of retail trade by women fostered a rough equality of numbers between the sexes, but Abidjan, alone in West Africa, had the large male majority among adults that in East African cities like Nairobi led to highly commercialised sex, although in Abidjan it led also to more sophisticated forms of courtesanship, owing to the greater economic independence of women in West Africa and the region’s less constrained sexual traditions.¹⁶ Like Nairobi, Abidjan was a primate city on which the whole of Côte d’Ivoire’s excellent transport system focused. And as Vinh-Kim Nguyen has shown,¹⁷ two other features of Abidjan helped to make it an epicentre of HIV infection. One was an aspiration to modernity that bred individualistic choice, extreme differences of wealth, sexual adventurism – the median age of sexual debut was fifteen¹⁸ – and complex, disassortative networks through which HIV could pass. In 1994, 51 per cent of Abidjan’s men aged 20–24 said they had casual sex and 56 per cent never used a condom.¹⁹ The other circumstance favouring an epidemic was the economic crisis that struck Côte d’Ivoire during the 1980s as the world economy faltered and the easy growth opportunities of the 1970s were exhausted. This bred unemployment, sexual commercialisation, weakened health services, and resort to Abidjan’s 800 informal dispensaries ‘that sprout like mushrooms after rain’.²⁰

When HIV-1 prevalence was first measured in Abidjan in 1985, the city was on the verge of an epidemic more explosive than those in Kinshasa or even New York, with an annual incidence of new infections of over 3 per cent in 1989.²¹ The core were the city’s sex workers and their male clients. Between 1986 and 1993 HIV prevalence among sex workers rose from 38 to 86 per cent; at the latter date 50 per cent had HIV-1, 2 per cent HIV-2, and 34 per cent both. Studies showed that contact with sex workers was the chief risk factor for men, largely explaining why in 1988 men outnumbered women by nearly five to one among HIV-positive patients admitted to city hospitals and why 83 per cent of the 24,735 people estimated to have died of Aids-related diseases in the city between 1986 and 1992 were men. Deaths were most common among informal sector workers in the older working-class quarters.²² By 1991, however, as the Minister of Health put it, the epidemic ‘is in the process of passing from populations at risk to the general population,’ as HIV-positive men infected their wives and other partners, creating a second peak of incidence. By 1993, the ratio of men to women infected had fallen to less than two to one.²³ Antenatal prevalence rose between 1986 and 1989 from 3.3 to 9 per cent. During the mid 1990s it fluctuated around 15 per cent. As in southern Africa, good transport and high levels of mobility ensured an unusually narrow difference between urban and rural prevalences. In 1994 an estimated 41 per cent of all West Africa’s Aids cases were in Côte d’Ivoire.²⁴

Abidjan was not only the place where HIV-1 and HIV-2 met, it was also the epicentre of infection for the entire eastern half of West Africa. This infection spread along two routes. One was the network of migrant sex workers who left their rural homes for a few years to work in the cities of neighbouring countries, seeking to bring home enough to set up a small business or finance their siblings’ schooling, without revealing their occupation to their families or potential future husbands. Like sex workers everywhere in the continent, these women were invariably blamed for expanding the epidemic, although almost all must themselves have contracted the disease from infected men resident in the towns where they came to work. West African sex workers were extraordinarily mobile. Of those attending a clinic in Abidjan in 1992, 82 per cent were from Ghana, 9 per cent from Côte d’Ivoire, and 2 per cent from Nigeria, but by 1998 only 9 per cent were from Ghana, 29 per cent from Côte d’Ivoire, and 56 per cent from Nigeria. Recovery in the Ghanaian economy and recession in Côte d’Ivoire and Nigeria probably shared the explanation with numerous Aids deaths among Ghanaian women and violence towards the Ghanaian community in Abidjan following a soccer match in 1993.²⁵

Ghana was the first country to which Abidjan’s epidemic spread. Testing facilities became available there late in 1985 and were immediately deployed on sex workers. Of those tested in Accra early in 1986, only 5 of 236 were found HIV-positive, but when attention switched to women returning from Abidjan, 74 of 151 were found infected and many already gravely ill. At the end of 1987 the doctor in charge reported that Ghana had 276 known HIV cases, of whom 242 were women, 199 were sex workers returned from Côte d’Ivoire, and 145 came from Ghana’s Eastern Region, where the patrilineal Krobo people allowed women no rights over land and young women had long been engaged in commercial sex. ‘There is no work here,’ a woman from the area explained at that time. ‘In Abidjan I can earn 10,000 CFAs a day. . . . I have about 12 men a day. Since I heard about AIDS I always make them use condoms . . . I don’t know anyone who has it.’²⁶ Although Ghanaians habitually blamed HIV on these women, it was plainly an oversimplification, for they had been singled out for testing and their predominance among those with HIV demonstrated that they had seldom transmitted the virus, which many were probably too sick to do. Transmission was clearly more diffuse. Nevertheless, by 2001, as national adult prevalence hovered around 3 per cent, Eastern Region was still the most heavily infected area and commercial sex was still central to the epidemic. HIV prevalence in Accra at that time was 5.9 per cent among men who bought sex and 0.5 per cent among those who did not. Among men aged 15–19, 84 per cent of cases were attributable to commercial sex.²⁷

This combination of relatively low general prevalence and high infection rates among mobile sex workers and their clients was widespread within the region of West Africa focused around Abidjan. In Benin, for example, HIV prevalence among pregnant women in Cotonou rose slowly from 0.4 per cent in 1990 to 3.4 per cent in 1997–8, while prevalence among the city’s commercial sex workers rose from 3.3 per cent in 1986 to 58.0 per cent in 1997–8. It was calculated in the early 2000s that 76 per cent of male HIV infection in the city was contracted through commercial sex. Benin was unusual in that HIV prevalence in the general population was higher in some provinces than in the capital city, partly because commercial sex, a long-established practice there, was also widely dispersed, with a close correlation between infection in sex workers and in the general public.²⁸ The remarkable point, as in Ghana, was that high infection among commercial sex workers did not precipitate the explosive epidemic seen in Kigali, Nairobi, and Abidjan. One reason was probably the equal gender balance in West African cities other than Abidjan. Another was that condoms had come to be quite widely used in commercial sex: by 54 per cent of clients in Cotonou in 1997–8, so they claimed, and by 90 per cent in Accra in 2001. In Cotonou the age at first sex was relatively high and women in the general population reported few sexual partners. Most important, perhaps, were the two contrasts emphasised by a study in 1997–8 that compared Cotonou and Yaounde in western Africa with Kisumu and Ndola in the east: the high levels of male circumcision in West African cities (almost 100 per cent in Cotonou) and the relatively low levels of HSV-2 in the general population (12 per cent among men and 30 per cent among women in Cotonou).²⁹

Away from the coast, in the savanna hinterland of Côte d’Ivoire, the network of commercial sex remained an important means for the diffusion of HIV, but it was supplemented by a second network of male migrant labour. The effects of migration were especially strong in Burkina, where Aids was often known as ‘the Côte d’Ivoire disease’, ‘a disease of people who move around, who travel and cannot keep still’, as an elder put it.³⁰ ‘From Spring 1990 to Christmas 1992,’ an anthropologist wrote of his village, ‘a score of young-old migrants returned from Côte d’Ivoire, dreadfully bent, with their sticks, without bicycles or suitcases. They had simply come to die in Kampti and its environs.’³¹ At first the national hospital in Ouagadougou admitted seven male cases for every female, but by October 1987 HIV prevalence among pregnant women in the city was 7.5 per cent and it appears to have hovered around that figure during the 1990s, although rising to 57 per cent among sex workers in 1994.³²

Further north, in Niger and Mali, these patterns were repeated but at lower levels of disease and with larger proportions of locally born sex workers. In Niger, for example, 62 per cent of the first 40 Aids cases diagnosed at Niamey hospital were former migrants to the south; their risk factors were listed as ‘prostitution, contact with prostitutes, blood transfusions and histories of visits to coastal countries’. Nearly three-quarters were men, a balance that shifted during the 1990s as infection spread more broadly, although still at relatively low levels. In 2003 adult prevalence was just over 1 per cent, but with 38 per cent among sex workers in Maradi.³³ Prevalence was somewhat higher in Mali, averaging 1.7 per cent in adults aged 15–49, according to a population survey in 2001, but with 30 per cent infection among sex workers and significant concentrations in Bamako and in towns like Sikasso and Mopti on migration routes to the south. Some 63 per cent of sex workers in Mali’s four main towns at that time came from outside the country.³⁴ Low overall prevalence characterised other Sahelian regions like Mauritania and northern Chad, where, as in Sudan, levels of infection were higher in the south.³⁵

The pattern suggests that the savanna region’s Islamic social order may have limited the transmission of disease. In Niger, for example, a population survey in 2002 showed exceptionally low infection among young people, only about 0.3 per cent for men and 0.1 per cent for women. Women in this region married very young – a median age of sixteen in Mali – to men nine or ten years older. Often secluded, only 0.1 per cent of women in Niger reported more than one sexual partner in the last twelve months when surveyed in 1998. Most of the 11 per cent of men who reported paying for sex during that year were unmarried. Moreover, whereas women in West African coastal countries practised postpartum abstinence for 10–19 months, during which their husbands often sought other partners, in Mali and Niger the average was only 4–8 months.³⁶ The data suggest that in this Islamic region non-marital sex was to an unusual degree confined to commercial sex workers and young, unmarried, circumcised men, where it was least likely to spread infection to the general population. The same seems generally to have been true in North Africa, where, except in Sudan, official prevalence figures at age 15–49 were generally 0.1 per cent or less and about 100,000 people were thought to be infected in 2005. Although many of the earliest cases there were introduced from Europe by returning migrants, tourists, or injecting drug users, infection during the 1990s appears to have taken place mainly within indigenous but narrow sexual networks, both heterosexual and homosexual, with expansion into the general population confined by the Islamic marital and social order, although it was under increasing strain.³⁷

The spread of HIV in Nigeria needs to be seen in this context. It was often described as a delayed epidemic, ‘with a potential for rapid increase’, but in fact it fitted logically into broader West African patterns. Nigeria experienced two infections by HIV-1, one in the south caused mainly by CRF02_AG and the other in the north caused by CRF06_cpx. Both revealed their first HIV cases in 1986, in sex workers, among whom and their partners much of the early proliferation took place.³⁸ In 1993 the first widespread sentinel survey showed prevalence of about 1.9 per cent among pregnant women. During the next six years it rose gradually to 5.4 per cent and the variation between different states widened, but those most affected were scattered broadly across the country. The highest prevalence (16.7 per cent in 1999) emerged in Benue state, in central Nigeria, where Aids was known as ‘the Abuja disease’. ‘No one suffers from this sickness in our village here,’ it was said, ‘but these women who go to Abuja [for commercial sex] suffer from it. They come home almost dead.’ Of 40 people with Aids studied in that village, only one did not have a history of ‘life abroad’. The next highest prevalence was 12.5 per cent in Akwa-Ibom state in the extreme south-east, where cross-border traffic coincided with great female independence and exceptionally high levels of commercial sex.³⁹

Three reasons may help to explain why Nigeria did not suffer an explosive epidemic like that in Côte d’Ivoire. One was that Nigeria was too big and diverse, with many local epidemics but no primate city to transmit disease throughout the country. Rural prevalence was higher than urban in some states in the early 2000s. The second reason was that sex workers were mostly Nigerians and only marginally involved in the wider West African sex trade, at least until the later 1990s, so that even in 1994 only 13 per cent of sex workers in Lagos were infected. The third reason was the restraint imposed by the culture of the Muslim north, where women were commonly secluded and average HIV prevalence was significantly lower than in the centre and south-east.⁴⁰ It is more difficult to explain why prevalence was even lower in the south-west, where extra-marital sex had long been common among the Yoruba and had become increasingly so among the young in the course of the twentieth century, unless perhaps the very diffuseness of partnerships rather than their concentration around high-risk sex workers gave protection.⁴¹ On the other hand, one factor encouraging the spread of disease was the mediocrity of Nigeria’s health system, rated by the World Health Organisation as one of the worst in the world. In 1995 the Federal Ministry of Health estimated that 10 per cent of HIV transmission was by blood transfusion, a problem still unresolved ten years later.⁴²

In 1995, also, Nigeria’s health authorities estimated that at least 24 per cent of the country’s HIV infections were by HIV-2, although the country lay well outside the range of the sooty mangabey.⁴³ The virus had probably entered Nigeria from the west at much the same time as HIV-1 was spreading from the east and south. Further west along the Guinea coast and in Senegambia, however, HIV-1 had to penetrate a region where HIV-2 was already endemic, if generally at low prevalence. The first search for HIV-1 in Senegal in 1985–6 chiefly revealed cases of HIV-2, both among sex workers in Dakar and especially in the southern Casamance region bordering the epicentre of the disease in Guinea-Bissau. Almost all were Senegalese who had never left the country, whereas the first HIV-1 cases identified were predominantly foreigners or Senegalese men who had travelled elsewhere in West or Equatorial Africa and often had histories of homosexuality or drug use. In 1990 Senegal’s national prevalence of HIV-2 was reckoned to be nine times that of HIV-1, but the greater virulence of the latter enabled it to overtake HIV-2 in 1996–7. By 2004 HIV-1 in Senegal was sixteen times more prevalent than HIV-2, which was of equal importance only in the Ziguinchor region on the Guinea-Bissau border.⁴⁴ During the 1990s this reversal took place everywhere in the western coastal region except Guinea-Bissau, where the differential between the two infections narrowed but did not close, chiefly because of continuing (although declining) high levels of HIV-2 infection among older women.

Senegal gained international renown by limiting its national HIV prevalence at age 15–49 to little more than 1 per cent. Much of its infection was concentrated among the Jola people close to the southern border with Guinea-Bissau, where prevalence was two or three times the national average.⁴⁵ Young, infected Jola migrants began to return from Côte d’Ivoire during the late 1980s to die at home. Like the Yoruba and many other young people throughout the continent, they had during the twentieth century adopted risky patterns of pre-marital sex in response to the commercialisation of the economy, the need to migrate for urban employment, the declining status of women consequent on the spread of Islam, the increasing difficulty of marriage, the collapse of customary sexual restraints, the spread of sexually transmitted diseases, the marginalisation of the region within independent Senegal, the destructive impact of structural adjustment policies, and their continuing anxiety to bear children at the peak of fertility.⁴⁶ Elsewhere in Senegal, however, Muslim culture provided greater protection. There the median age of sexual debut was high, at about 19 years for both sexes during the late 1990s, levels of non-marital sex were low outside the capital, and condoms were quite widely used with casual partners. The government’s important part in containing disease will be considered later, but Senegal’s experience, like Nigeria’s, fitted closely into the wider patterns of West Africa, where the great regional variations in HIV prevalence witnessed to an epidemic that had penetrated but not conquered.⁴⁷