Although they contribute little to the overall burden of AIDS in the world, the other HIVs (HIV-1 groups O, N and P, and HIV-2) can provide useful insight into the events that led to the emergence of pandemic HIV-1 group M. How was it possible for HIV-2, a different virus that originated from a different simian host, to spread in a different region of Africa at roughly the same time (give or take a few decades) as HIV-1, only to disappear quietly thereafter? And why was HIV-1 group M so successful compared to the others?
HIV-1 groups O, N and P
Highly divergent strains of HIV-1 were described in the 1990s. The first, now known as HIV-1 group O (‘O’ for outlier), has only 50–65% homology in nucleotide sequences compared to HIV-1 group M, which is why it is considered as a different ‘group’ rather than a different ‘subtype’ (subtypes differ by about 20%; in other words, they have 80% homology). The original isolates of HIV-1 group O had been obtained from two Cameroonians living in Belgium, a young woman and her husband. Additional cases were documented among Cameroonians living in France, and in Cameroon itself. Further studies confirmed that Cameroon was the epicentre of HIV-1 group O, where it accounted for 2% of all HIV-1 infections, versus 1% in adjacent Gabon and Nigeria. A few cases were found in other African countries. Within Cameroon, regional variations were noted, with group O representing 6% of all HIV-1 positive sera in Yaoundé but only 1% in northern provinces. When stored sera were tested, group O represented 21% of all HIV-1 positive sera in 1986–8, 9% in 1989–91, 3% in 1994–5 and only 1% in 1997–8. It then remained rather stable at 1–2%.
We have just seen how HIV and other blood-borne viruses can be transmitted through injections. Here we will examine the history of colonial medicine in the French territories of central Africa, where remarkable public health interventions ultimately proved successful in reducing the burden of tropical diseases, but at the same time caused the parenteral transmission of HCV, the HTLV-1 retrovirus and presumably SIVcpz/HIV-1 as well. The core of the problem was that since the early drugs against infectious diseases were not very effective, they all had to be administered by injections, often IV, so as to maximise the drug concentration in the blood and in other tissues. As we will see now, tens of millions of IV injections were administered within the crucible of HIV-1, at exactly the right time.
A remarkable peculiarity of French colonial history is the way medicine was organised: as part of the military. Young Frenchmen interested in a medical career in the colonies would usually get their degree at a medical school run by the armed forces in Bordeaux, before moving on to the tropical medicine institute in Marseilles, known as Le Pharo, after the name of the park where it is located near the old port. Overseas, they would start as a médecin-lieutenant and progressively, for the more talented, patient or motivated, move up the ladder to become perhaps a médecin-colonel or médecin-général at the end of their careers. Very few of them would be posted to the barracks to provide care for the colonial armed forces. Instead, they were posted to the hospitals and disease control units, working among civilians but remaining military doctors so that a strict hierarchy was maintained. Disease control interventions and modes of healthcare delivery would be decided at the top of the pyramid, by the médecin-général, and implemented in a similar fashion throughout the colony following detailed protocols. There were precise definitions of what had to be reported and in what form, and the reports from each hospital or district would be merged into an annual report for the colony, containing an extraordinary number of tables, maps and graphs about the diseases of interest, their distribution, the treatments administered, the exact number of injections for each drug, and so on. Some of these annual reports contained 800 pages. Their format was the same for all colonies, so that they could be consolidated into an annual summary of the health status of overseas France.
Prostitution facilitates the spread of all sexually transmitted microbial agents. There is no doubt that it played a crucial role in the dissemination of HIV-1 in many parts of the world, including during the first few decades of the emerging epidemic in central Africa. In this chapter, we will review what is known about the development of prostitution (or sex work, as some prefer to call it) in the burgeoning cities located close to the natural habitat of the P.t. troglodytes source of SIVcpz/HIV-1, a process that was intimately related to the urbanisation we have just examined.
The core group
Immediately after the African HIV epidemic was recognised in the mid-1980s, prostitutes and their clients were identified in many countries as the core group within which the virus is exponentially transmitted in the early stages, a process facilitated by the extraordinary prevalence of STDs among these women, which increase the efficacy of heterosexual HIV transmission. Eventually, male clients infect their subsequent female partners not involved in the sex trade, enabling the virus to move out of the core group and into the general adult population. From a concentrated epidemic, it becomes a generalised one.
In this chapter, we will examine the possibility that, during the early stage of the Haitian epidemic, a commercial enterprise in Port-au-Prince exponentially and parenterally amplified the number of HIV-1-infected individuals and allowed the virus to thrive. More generally, we will review the role of the blood trade in the globalisation of HIV-1. But first, we need to understand how viruses can be transmitted, not only from donor to recipient, but also from one donor to another during the handling required to prepare certain blood products. The word ‘donor’ is somewhat misleading here because we are talking mostly about people paid for their ‘donations’.
Blood is made of cells (red blood cells, white blood cells and platelets) and plasma, its liquid component. Plasma is made of water and proteins: antibodies, clotting factors and albumin. When a donation is made, the various components are separated to maximise their use. Patients with anaemia or acute blood loss need only receive the red blood cells, those with a low platelet count will be given the platelets and so on. Plasma is highly valuable as it contains many proteins. Therapeutic use of plasma started during WWII as an expander of intravascular volume, to increase quickly blood pressure in patients with serious bleeding. Subsequently, other uses of plasma components were developed, which required the selective processing of specific proteins: albumin (to expand intravascular volume or to patients with low albumin levels), coagulation factors (haemophilia or other coagulation disorders) and immunoglobulins (patients with immune deficiencies or to protect travellers against hepatitis A).
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.
Ex Africa semper aliquid novi
Out of Africa, there is always something new, wrote historian Pliny the Elder more than 2,000 years ago. He was quite right. As early as 1984, just three years after the first description of the new disease, it was suspected that HIV, its recently discovered aetiological agent (then known as human T-cell lymphotropic virus (HTLV)-III in the US, LAV (lymphadenopathy-associated virus) in Europe), originated in central Africa. This was mainly because the first studies in Africa, conducted in Zaire and Rwanda, showed that AIDS was common in Kinshasa and Kigali, where nearly 90% of sex workers were infected. These field studies were prompted by the observation that of the first few hundred cases of AIDS diagnosed in Europe, about half occurred among patients coming from central Africa, mostly from Zaire. Over the following years, the epidemiology of HIV-1 infection in Kinshasa would be described in great detail by a group of American, Belgian and Congolese researchers known as Projet Sida, based at Hôpital Mama Yemo (Mama Yemo was dictator Mobutu’s mother, a former sex worker, and she suffered the same fate as the Belgian colonists after her son was overthrown: this institution is now called Hôpital Général de Kinshasa). Projet Sida came to an abrupt end in 1991, when the whole of Kinshasa was looted by the city’s poor people. During the same period and until the 1994 genocide, similar epidemiological work was conducted in Kigali, 1,500 kilometres east of Kinshasa.
In retrospect, this early vision of central Africa as the source of HIV-1 was rather naive. Researchers assumed that since this was at the time the region with the highest prevalence (i.e. the proportion of the population that is infected) among groups representative of the general adult population, the virus must have originated there. There were at least two problems with this assumption.
The early spread
Here we will review how, from its central African crucible, HIV managed to disseminate throughout Africa, at the same time as it did so across the Atlantic. But first we need to review two epidemiological terms. As explained in Chapter 1, ‘incidence’ is a measure of new cases of HIV that occur among previously uninfected subjects over a period of time. The same individuals have to be tested repeatedly: this is time-consuming, expensive and rarely used. ‘Prevalence’ is the proportion of individuals who have HIV at some point in time, a snapshot that indicates the current distribution. As the median interval between HIV infection and death in Africa is about ten years, measures of HIV prevalence reflect an accumulation of individuals infected from as little as a few weeks ago to more than ten years earlier. Over time, prevalence in a population increases if the number of new infections since the previous survey was greater than the number of individuals who died from HIV or other causes. Prevalence decreases when the reverse occurs, i.e. the number of deaths is higher than the number of new infections.
Ten years ago, a group of scientists argued that unsterile injections played a role in the emergence of HIV in Africa (and that serial passage of the virus within syringes altered it in a way that made it more virulent and/or more transmissible, something which remains debated among virologists until now). As mentioned in the introduction, after studying this question for some time I came to the conclusion that they were right, that a substantial part of the early amplification of HIV-1 in central Africa occurred through the re-use of improperly sterilised syringes and needles, and that this mechanism was probably as important as the sexual amplification which we just reviewed. It will be impossible to prove this directly. But like a crown prosecutor who has not found the exact gun used in a crime, in the next three chapters we will assemble circumstantial evidence that would ultimately convince any jury. We will first examine how HIV but also HBV and HCV can be transmitted through injections.
Parenteral or iatrogenic
Parenteral is synonymous with injectable; it literally means to bypass the gut, by administering a drug (therapeutic or recreational) or blood product as an injection, either into a vein (IV), muscle (IM), the tissues underneath the skin (SC) or the skin itself (intradermal (ID)). Iatrogenic means during health care; the transmission of pathogens between intravenous drug users is not included in this latter definition, but non-injection modes of healthcare transmission are (for example, during an organ transplant or some other invasive procedure). In sub-Saharan Africa, there is much overlap between these two terms, parenteral and iatrogenic, because the continent has few drug addicts (such a habit is far too expensive) and few patients undergo invasive medical procedures during which a virus could be transmitted.
Having identified the source of HIV-1, the next question is: when did the virus manage to cross species from chimps to humans? It has often been said that AIDS was a new disease on the African continent. Apart from the published cases mentioned in Chapter 1, clinicians working in central Africa, for instance Dr Bila Kapita, chief of internal medicine at Hôpital Mama Yemo in Kinshasa, reported that, at least since the mid-1970s, they started seeing cases that in retrospect were very likely to have been AIDS. This would be consistent with some degree of dissemination of the virus during the mid-1960s, given the average ten-year interval between infection and symptomatic disease. But could the disease have been present even earlier?
In most district or regional hospitals of countries inhabited by P.t. troglodytes, the diagnostic facilities during the colonial era (and even now) were so minimal that it would have been difficult, even for astute and experienced clinicians, to recognise the emergence of a new disease characterised by intermittent fevers and profound wasting. Most such institutions did not have any kind of half-decent microbiology laboratory. No cultures were done, either for common bacterial pathogens or the agent of tuberculosis, and diagnoses were based on stains made directly on the specimens, or solely on the combination of symptoms and signs found during the clinical examination. Fifty years later, I found the same situation at the Nioki hospital in Zaire: nothing had changed. This approach was relatively effective for diagnosing parasitic diseases (malaria, sleeping sickness, filariasis, intestinal parasites) but very insensitive for most bacterial diseases. Little radiological investigation was available either; only in the best hospitals was it possible to get something as elementary as a chest x-ray. The first x-ray machine in Brazzaville was installed in 1931, two years before one became available in Léopoldville.
For readers unfamiliar with virology, this section reviews a few concepts, which are summarised in the table. HIV-1 and HIV-2 are the two human ‘retroviruses’ that cause AIDS. To replicate, retroviruses transcribe RNA into DNA, which is then integrated into the DNA genome of the human host cells. This process is the reverse of what normally happens (DNA transcripted into RNA), hence their name. Retroviruses are further subdivided into ‘lentiviruses’ (HIV-1 and HIV-2), ‘oncoviruses’ (HTLV-I, the first retrovirus isolated from humans, which does not cause AIDS but sometimes cancer or paraplegia) and ‘spumaviruses’ (not pathogenic).
Of course, the pandemic is caused by HIV-1. HIV-2 differed enough, genetically, from HIV-1 to be considered a distinct virus. It remained confined to West Africa, is less transmissible and less pathogenic than HIV-1 and slowly disappeared while HIV-1 spread throughout the world. HIV-1 infection is 100 times more common than HIV-2; when authors use the term HIV, in practice it generally means HIV-1.
While France was busy running the health systems of more than twenty-five territories in Africa, around the Indian Ocean, in south-east Asia and the Americas, Belgium could concentrate its efforts on its three African colonies, the largest of which by far was the Belgian Congo. Belgium was justifiably proud of its achievements in the Congo, whose health system soon acquired the reputation of being the best in tropical Africa. This led to a substantial improvement in the health of the Congolese people, but also to numerous opportunities for the transmission of blood-borne microbial agents. What happened in and around Léopoldville will be especially relevant, as this is the area where ultimately HIV-1 spread and diversified.
For this part of the story, the best sources of information are in Belgium. Since 1960 the ministry of foreign affairs has kept the archives of the Belgian Congo, which are accessible to researchers. The Royal Library and the university libraries of Brussels, Louvain and Louvain-la-Neuve hold impressive collections of books and journals relating to the country’s former colonies. In Antwerp, the tropical medicine institute has made available online the Annales de la Société Belge de Médecine Tropicale, in which Belgian medical officers working in the tropics used to publish their findings. More detailed articles were published through the Académie Royale des Sciences Coloniales.
This background chapter aims to describe the settings in which the rest of the story took place. Africans understandably resent and reject as arrogant, or at least Eurocentric, historical accounts of their continent which consider the European penetration as the starting point and describe this process as discovery rather than what it really was: a military conquest for the purpose of economic exploitation. However, since the events relevant to the emergence of HIV-1 occurred during the colonial occupation of central Africa, and were facilitated by the profound social and economic changes brought about by colonisation, especially around the pool on the Congo River, we will focus on this period, but after a short detour which will enable us to examine how history confirms the molecular clocks of Chapter 3.
The slave trade and the exportation of infectious diseases to the Americas
The arrival of the Bantus in central Africa is, on the scale of human history, relatively recent, having occurred about 2,000 years ago, when migrants from around Lake Tchad managed to dominate the truly indigenous pygmy populations and for the first time introduced various forms of agriculture. In some areas, organisation was limited to small tribes that occupied geographically limited territories. Elsewhere, kingdoms were established, such as the Kongo kingdom, a loose confederation of tribes which corresponded to parts of current day Congo-Brazzaville, DRC, Angola and Gabon. These societies were not technologically advanced, which made it easy for Europeans to conquer the heartland of Africa once they found solutions to the health problems (mostly malaria) that decimated their early soldiers and settlers, many of whom died within two years of their arrival. But central African people had strong values, beliefs and traditions centred on the extended family, the clan. And there was already a fair amount of trading between ethnic groups within the Congo basin.
June 1981 is the official birth date of the AIDS epidemic. In a short article published in the Centers for Disease Control’s Morbidity and Mortality Weekly Report (MMWR), American clinicians described a cluster of five cases of Pneumocystis carinii pneumonia, an infection of the lungs hitherto seen only in patients with severe impairment of their immune system. These five initial cases had been diagnosed in 1980–1 among gay men, all living in Los Angeles, who had been previously healthy and were not receiving drugs that suppressed the body’s immune response. At the time, the standard treatment for Pneumocystis pneumonia was an old drug called pentamidine, developed during WWII for the treatment of sleeping sickness, which happened to be highly active against Pneumocystis. Pentamidine was not commercially available and had to be distributed centrally from the CDC in Atlanta. An astute CDC technician found it strange to have received several requests for pentamidine within a short period of time from hospitals in California and, a bit later, from New York as well. This became the first step in the identification of the new syndrome by this federal agency.
We saw in Chapter 1 how geopolitical events, in that case the Cuban intervention in Angola, had a measurable effect on the dissemination of HIV-1 into this Caribbean island. Here, we will see how earlier historical circumstances had even more dramatic impacts on the spread of HIV-1, first in its crucible of central Africa, and then across the Atlantic, by finally creating conditions propitious to the successful dissemination of the virus, after decades of quiescence. Although the next few pages may seem a little bit of a detour, these incidents lie at the heart of our story.
A botched decolonisation
Fifty years later, it is astonishing to read some of the colonial and early post-colonial writings about the Belgian Congo which is described as ‘our Congo’ or its inhabitants as Nos Noirs, our blacks. Belgium exploited this huge country, much to the profit of its banks and large corporations, but the Congolese benefited from the development of the infrastructure. Good roads were built, an impressive health system was put in place and primary school education was offered to many. It was cheaper for the colonial government to subsidise Catholic (and, after WWII, Protestant) missions to take care of the teaching, and its expenditures on education were modest. In contrast with their French and British counterparts, Belgian colonialists elected not to train any Congolese elite, presumably for fear that these educated few would sooner or later challenge the colonial order. Only a tiny proportion would be able to enter secondary schools, and very few apart from Catholic priests would have access to post-secondary education. In 1957–8, out of 494 Congolese students attending post-secondary education, 376 were future priests enrolled in the seminaries. Throughout Africa, the Belgian Congo had the second highest proportion of its population that had attended primary school but the lowest with regard to post-secondary education. Among adults aged twenty and over, 1.7% of men and 0.1% of women had received at least one year of post-primary education, and respectively 0.5% and 0.04% had completed secondary school.
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