Chapter 3


AIDS spreads silently, 1960-81

 

 

During 1960-81, the HIV epidemic expanded geographically, reaching more countries in Africa and also in the Americas and Europe. In parts of Central Africa, the epidemic grew slowly if at all. Infections multiplied much faster in some of the countries with newer epidemics both in and outside Africa. The contribution of HIV transmission through blood exposures to Africa’s epidemic during this period remains a matter for speculation and investigation.

 

HIV-1 expansion in Africa, 1960-81       

 

The HIV-1 M (main) group apparently began with SIV passing from a chimpanzee to a human in southeast Cameroon. Low HIV prevalence in Cameroon at the beginning of the 1980s testifies to decades of slow or no epidemic expansion in that country. During 1960-81, the most intense epidemics in Africa developed in DRC and in DRC’s neighbors to the east.

More than 24,000 stored blood samples collected in Africa before 1982 have been tested for HIV.[i] From these samples, the highest rates of HIV-1 prevalence have been found in DRC and Burundi. In Kinshasa, tests of stored blood found 0.25 percent of ‘healthy mothers’ to be HIV-positive in 1970, increasing to 3 percent in 1980.[ii] Tests of stored blood collected in 1976 from rural children and adults in north-central DRC found 0.8 percent to be HIV-positive (the blood was collected after an outbreak of Ebola hemorrhagic fever, which is discussed later in this chapter).[iii] In Burundi, testing of blood samples collected in 1980-81 from a ‘healthy population’ including some children found 8.1 percent HIV prevalence in urban areas and 2.8 percent in selected rural areas (these and other results from stored blood are based on too few samples to give more than a rough idea about HIV prevalence before 1981).[iv]

More than a half-dozen pre-1980 HIV infections and suspected AIDS deaths in Europeans linked to Africa have been traced to DRC, Rwanda, and Burundi in the 1960s and 1970s.[v]  During 1960-81, doctors in DRC and in neighboring countries reported unusual numbers of patients with cryptococcal meningitis[vi] and Kaposi’s sarcoma (including some with infected lymph nodes, and some children). After 1981, these conditions have been associated with AIDS. Tests of blood collected in Kinshasa in 1972 from four patients with Kaposi’s sarcoma found that two were HIV-positive.[vii] Experts disagree about how often pre-1980 cases of Kaposi’s sarcoma in Africans were associated with AIDS.

When HIV testing began in the mid-1980s, some of the highest rates of HIV prevalence were found in Rwanda and in communities west of Lake Victoria in northwest Tanzania and southwest Uganda. A 1974 study reports ‘a definite concentration of cases [of Kaposi’s sarcoma] in western Uganda…which seems…to extend into Tanzania to the west and south of Lake Victoria and possibly across Rwanda and Burundi into the eastern [DRC].’[viii] When I visited northwest Tanzania in 2000, a Canadian missionary told me that when he arrived in the early 1970s, people already recognized slim disease, which was later found to be AIDS. Hooper in The River reports Kaposi’s sarcoma and other often AIDS-related infections during the 1960s in immigrants from Rwanda and Burundi in Uganda.[ix] Hooper speculates that refugees fleeing genocide in Rwanda around 1960 brought HIV to Tanzania and Uganda,[x] but there was a lot of normal cross-border traffic which could have done so as well. Unfortunately, not much information is available from tests of stored blood on pre-1980s HIV infections in those regions.

Before 1981, HIV had very likely passed south from DRC into Zambia, but there is no information from stored blood to show when HIV began to circulate there. In Zimbabwe, tests of several hundred blood samples from around 1970 found no HIV infections. HIV-1 no doubt reached West Africa before 1981, but infections were rare. Tests of more than 4,000 blood samples collected in West Africa in the 1960s and 1970s found no confirmed HIV-1 infections.[xi]

 

Molecular evidence

 

DRC’s HIV epidemic appears to have grown over time, rather than with a concentrated late growth spurt. The evidence for this is that the HIV circulating in DRC established new major branches, such as clades, sub-clades (or sub-subtypes) and CRFs, progressively over time.[xii] All clades in the HIV-1 M group began to multiply from parent (founder) viruses in or near DRC (except for clade B, for which the founder virus appears to have reached Haiti before multiplying). All clades, with a few possible exceptions, circulate across DRC, all former French colonies in Central Africa (Cameroon, CAR, Congo, Chad, and Gabon), and Angola. High clade diversity is evidence for slow epidemic growth over decades – with HIV-infected people moving around the region, introducing divergent strains from distant places, but with subsequent slow multiplication of infections, so that no one virus type overwhelmed others. Within this diversity, the percentage of HIV infections from each clade varies across the region. For example, the C clade is more common in several southern cities in DRC than in north DRC.[xiii]

On the other hand, HIV-1 samples from countries east and southeast of DRC and in West Africa show less clade diversity, suggesting rapid expansion from one or a handful of introduced viruses, so that later, divergent virus introductions subsequently account for small percentages of total infections. For example, the C clade, which has been estimated to begin in the mid- to late 1960s,[xiv] accounts for most infections in Burundi[xv] and Zambia.[xvi] Tanzania’s epidemic shows a bit more diversity, with three clades, A, C, and D, accounting large percentages of infections.

 

Sex exposures in Africa

 

Many AIDS experts suppose that urbanization and other social changes in Africa during this period accelerated heterosexual transmission of HIV. According to Chin,[xvii]

 

During the 1960s, concomitant with the attainment of independence for some African states, there were significant political and social upheavals, along with major movements of young adults, mostly males, to the growing urban centers in SSA [sub-Saharan Africa]. These population changes increased the introduction of HIV infections from relatively stable rural societies to the newly expanding urban centers where a more open and liberal social/sexual environment fostered the transmission of HIV. The patterns and high prevalence of heterosexual HIV risk behaviors in many SSA cities provided the fertile environment for HIV epidemic spread.

 

This picture fits some evidence. By 1980 at least 25 percent of the residents of CAR, Congo, and DRC lived in cities.[xviii] Adult HIV prevalence had reached several percent in Kinshasa by 1980, and HIV was circulating across the river in Brazzaville (the capital of Congo), in Bangui (the capital of CAR), and no doubt also in other urban areas in DRC.

On the other hand, African countries where HIV ‘sparks’ found the driest tinder during 1960-81 were not consistently distinguished by urban agglomerations or sexual behavior. Although only 4 percent of Burundians lived in urban areas in 1980, the country appears to have had one of the worst HIV epidemics at the beginning of the 1980s. Because the C clade, whose founder virus has been dated to the mid- to late 1960s, accounts for most HIV infections in Burundi, the country’s epidemic must have grown faster during the 1970s than older epidemics in Cameroon, Gabon, DRC, Congo, and CAR. This rapid growth occurred even though sexual behavior in Burundi is relatively conservative. In a 1990 survey among urban Burundian adults aged 15-49 years, only 10 percent of men and 3 percent of women reported sex with a non-regular partner in the past 12 months. This was far less than percentages reporting non-regular sex partners in seven of eight other African countries with comparable 1989-90 surveys.[xix]

In contrast, HIV prevalence among adults in Yaounde, the capital of Cameroon, the country with the world’s oldest HIV-1 epidemic, was 0.3 percent only when this was first measured in 1987.[xx] Neither lack of urbanization nor conservative sexual behavior explains Cameroon’s low HIV prevalence. In 1980, 31 percent of Cameroon’s population lived in urban areas, and in a 1997-98 survey, 67 percent of men and 44 percent of women in Yaounde reported one or more non-regular sex partners in the past 12 months.[xxi]

 

Blood exposures in Africa

 

In Cameroon and several neighboring Central African countries, much higher prevalence of hepatitis C in persons born before vs. after 1960 suggests a sharp drop in blood exposures around that year (see Chapter 2). If so, why? Future research might clarify what happened.

In any case, over the next several decades, blood exposures throughout Africa generally increased with expanding foreign aid, national health systems, and private healthcare. National governments and donors continued to channel a lot of resources through mobile teams and special programs, but over time shifted more efforts into hospitals and clinics. In addition, private formal and informal providers administered injections and other invasive procedures.

 

Mobile teams and special programs

 

From 1949, WHO promoted mobile teams to treat yaws. During 1950-66, yaws treatment programs administered one or more injections of long-acting penicillin to 20 million Africans[xxii] – at that time, approximately 1 in 12 Africans.

In 1967, WHO launched an Intensified Smallpox Eradication Program. The program used mobile teams to vaccinate people and to survey for cases. Depending on the country, these teams often provided BCG vaccinations (against tuberculosis) and/or other health care inspections and treatments as well. In Central, West, and East Africa, the number of smallpox vaccinations by country during the program generally exceeded the population, as some people were vaccinated more than once. The program identified the last naturally occurring smallpox infection in Somalia in 1977. Smallpox has been eradicated, except for frozen samples of the virus retained in several laboratories.

The Smallpox Eradication Program used needles with a split tip to place a drop of vaccine on the skin, and to administer shallow jabs to get the vaccine under the skin. Instructions to vaccinators prescribed sterilization of needles between clients by boiling or flaming. For flaming, which was common, the instructions read: ‘the needle is passed through the flame of a spirit lamp. It should not remain in the flame for more than three seconds.’[xxiii] This upper time limit was set to prolong the life of the needle. Notably, the instructions did not prescribe a minimum time required to sterilize the needle. After flaming and cooling, the vaccinator dipped the needle in vaccine to pick up a drop for the next client. To contain costs, program managers pushed staff to vaccinate more people per day. Staff in Africa commonly vaccinated over 500 people per day. During one month in Rwanda the average was over 1,500 vaccinations per day per vaccinator.[xxiv]

For other vaccines, health staff often reused injection equipment without sterilization. For example, a description of BCG vaccination in Sudan around 1970 reports that ‘needles had to be flamed after each inoculation and the syringes repeatedly refilled from the vaccine vial.’[xxv] At the time, changing needles and reusing syringes remained common in the UK. As late as 1978 doctors in the UK injected children with BCG ‘using a separate syringe for every 10 injections and a new needle for each child.’[xxvi]

From 1974, WHO launched the Expanded Program on Immunization (EPI), which promoted immunizing children throughout the world against six diseases (tetanus, tuberculosis, polio, diphtheria, whooping cough, and measles), and immunizing women against tetanus, both to protect them during childbirth, and to protect their children from neo-natal tetanus. Before EPI, BCG vaccination was common in much of Africa, but coverage of the other vaccines was limited. In Africa, the program took time to get started, so that almost all the expansion in immunization coverage under EPI occurred in the 1980s and later.

 

Hospitals, clinics, and other healthcare providers

 

During 1950-70, governments and donors put a lot of effort into expanding Africa’s hospitals. Whereas population grew by about 60 percent over these two decades, the number of hospital beds almost doubled. Thereafter, hospital expansion slowed. In the 1970s, public health experts increasingly recognized that Africa’s hospitals absorbed an inordinate share of health budgets, and did not reach healthcare services to rural people. This realization led to a shift of emphasis towards primary healthcare delivered through local clinics.[xxvii] In 1978, most governments in the world took part in the International Conference on Primary Health Care in Alma Ata, Kazakhstan. The conference declaration asked governments ‘to launch and sustain primary health care as part of a comprehensive national health system,’ promoted immunizations and maternal and child healthcare, and asked donors to give more money.[xxviii]

As African medical schools produced more doctors, an increasing number went into private practice, opening their own clinics. In addition, pharmacists, traditional practitioners, and people with little or no training offered injections and other invasive healthcare in formal and informal settings. Because medical equipment – including syringes and needles – and injectable drugs were widely available without prescription, virtually anyone could provide an injection.[xxix]

Due in part to the dramatic cures seen with injections against yaws and other diseases, injections were popular.[xxx] Patients often expected or even demanded injections. During this time, common treatment for tuberculosis was 60 daily injections of streptomycin, and common treatment for syphilis was 10 daily injections of short-acting penicillin.

Unsterile practices were common. During the 1970s, recognized health consequences from using unsterile instruments included bacterial abscesses, viral diseases, and tetanus. In Yaounde’s Central Hospital in 1974-75, ‘14% of the tetanus cases reviewed…had an identifiable iatrogenic source of infection.’[xxxii]

Some authors link an increase in reuse of syringes without sterilization during 1950-80 to the spread of plastic syringes intended for single use.[xxxiii] Because the high temperatures required for sterilization damaged or destroyed plastic syringes, they were often reused without sterilization. However, reuse without sterilization was common with glass syringes as well, both before and after plastic syringes came into common use.

 

Blood transfusions

 

Although blood transfusions can save lives, blood has always been dangerous to use, with known as well as unknown risks (such as unknown viruses). During the early 20th century, doctors learned how to overcome some of the short-term dangers due to mismatched blood types and clotting. Blood transfusions became common in rich countries before World War II. In Central Africa, transfusions were available from at least one site in DRC by 1924.[xxxiv]

The expansion and development of transfusion services to treat soldiers during World War II led to large post-war increases in the frequency of transfusions in Africa as well as in Europe and the US. Transfusion services expanded to at least 19 countries in Africa by 1955. The number of transfusions administered per decade in Africa (except South Africa and North Africa) has been estimated at 680,000 in the 1940s, increasing to 1.4 million in the 1950s, 5.2 million in the 1960s, and 12 million in the 1970s.[xxxv] Doctors administered transfusions to treat not only people with acute blood loss, but also people with chronic anemia, such as from parasite infection. In addition, doctors used blood transfusions (convalescent serum) to treat people with infectious disease, injecting blood from someone who had recovered from the disease.

Blood transfusion was not limited to cities or to major hospitals. In 1951, a doctor working in a rural hospital in DRC reported transfusing blood to treat anemia from malaria in more than 5,000 infants beginning in 1943. He collected fresh blood for each transfusion from a parent, relative, or member of the clinic staff. For children with mild anemia, he reported intramuscular injections of blood. He recommended that ‘all dispensaries, even small ones, should be able to manage ordinary blood transfusions’ and that ‘medical assistants…can be trained to transfuse infants’ and can do so ‘in the bush in an emergency and with minimum material support…’[xxxvi]

Because blood banks were not well-developed – due in part to lack of or unreliable refrigeration – doctors often transfused fresh blood after simple tests to match blood type. Most blood was collected from replacement or paid donors. Relying on replacement donors ‘could rapidly degenerate into a system of unofficially paid donors, recruited on behalf of the relatives by “Captain Blood” operating in the local lorry-park.’[xxxvii] Repeat donors could transmit bloodborne pathogens to other donors if needles and tubes used to withdraw blood were reused without sterilization. In this way, one HIV-infected donor could infect not only the patients to whom he or she donated (sold) blood, but also other donors and, indirectly, other patients.

When HIV testing started in the 1980s, blood donors in Central Africa were often found to have higher HIV prevalence than adults in the general population. Very likely this was the situation in the 1970s as well. From their history of transfusions in Africa, Schneider and Drucker conclude that ‘transfusions may have played a significant role in the origins of the disease.’[xxxviii]

 

Collecting blood plasma

 

For donors, selling plasma – blood with the cells removed – is more dangerous than selling blood. The procedures to separate plasma from cells and to re-inject the cells provide opportunities to transmit HIV from donor to donor. Moreover, people can sell plasma more often than blood. Careless procedures to collect plasma have infected donors in many countries (see Chapters 5 and 9).

From the 1960s, US and European companies that produce blood products (such as albumin, gamma globulin, and factor VIII to stop bleeding in hemophiliacs) imported plasma from developing countries.[xxxix] During the 1970s, Kinshasa in DRC was ‘one of the main centres’ extracting and exporting plasma.[xl] Other African countries and Haiti also exported plasma. Wherever HIV was circulating, plasma collection could have spread HIV among donors. Unfortunately, no one has looked for HIV infections among 1970s plasma donors in countries with early HIV epidemics.

(Almost all HIV infections in Europe and the US belong to the HIV-1 B clade, and can be traced to a parent virus which left Africa around 1966. No one has identified any link between 1970s plasma exports from Africa and early HIV epidemics in Europe and the US. Because plasma from Africa was a recognized risk to transmit hepatitis B, companies may have used it for products for which processing killed the hepatitis B virus – and also the unknown HIV.)

 

Recognizing bloodborne pathogens: Hepatitis B virus

 

By mid-century, doctors recognized that liver cancer was unusually common among Africans. In 1958, a liver specialist speculated that infections that cause hepatitis might be important contributors to liver cancer and cirrhosis in Africa.[xli] Because scientists had not yet identified the viruses that cause most hepatitis, this was a guess.

In 1963, Blumberg and Alter discovered an antigen (a protein that stimulates the body to produce antibodies) in the blood of someone who had received multiple transfusions. By 1966, Blumberg and colleagues showed that what they had discovered was part of the virus that caused jaundice after blood exposures.[xlii] The antigen they discovered is currently known as the hepatitis B virus surface antigen, which is part of the hepatitis B virus. People with the antigen have the virus. All over the world, hepatitis B was found to be a major cause of liver cancer. Blumberg received a Nobel Prize for discovering the virus.

From the late 1960s, scientists used tests for the hepatitis B virus surface antigen to measure the percentages of people infected in different communities, and to investigate risks. In the US, Europe, and Australia, infections were rare in the general population – only between 1-3 in 1,000 were infected. In rich countries, hepatitis B was, as expected, linked to recognized blood exposures, including IDU and needlestick accidents among healthcare workers.[xliii]

By 1970, researchers had also found that ‘in many tropical areas’ 3-20 percent of people carried the hepatitis B virus surface antigen.[xliv] This surprising finding required not only urgent changes in medical practice, but also research to explain how it could be so. Unfortunately, at this point, medical practice and medical research in Africa both took a wrong turn.

 

Wrong turn in medical practice          

 

New information that large percentages of African patients carried the hepatitis B virus meant that unsterile medical procedures were a threat to transmit hepatitis B from patient to patient. Despite this new information, ministries of health and organizations providing health aid did not revise their activities to ensure use of sterile instruments, but rather extended programs with invasive procedures that were widely known to be unsafe.

In 1978, Zuckerman, at the WHO Collaborating Centre for Reference and Research on Viral Hepatitis at the London School of Hygiene and Tropical Medicine criticized careless injection practices:[xlv]

 

…in some parts of Africa and Asia as many as 20 percent of the population may be carriers [of the hepatitis B virus]. The risk of transmitting hepatitis by the multidose-syringe technique [i.e., filling a syringe with multiple doses, then changing needles between patients] is therefore considerable and it is imperative that an adequately sterilized or a disposable syringe and needle should be used for each individual patient.

 

Laird, who had demonstrated in the 1940s that using sterile syringes and needles prevented jaundice after syphilis treatments, seconded the warning.[xlvi] These warnings had no apparent impact on public health programs in Africa.

 

Wrong turn in research

 

Calculating that tens of millions of residents of tropical countries were infected with the hepatitis B virus, Blumberg and co-authors opined in 1970 that ‘Very few of these would have received blood transfusions or needle injections.’[xlvii] This ignored what was generally recognized among public health experts and doctors in Africa and other tropical regions: that injections were common. Instead, hepatitis experts speculated that some populations were genetically susceptible to infection, and that the virus might transmit through mosquitoes or other insects, poor sanitation, etc.[xlviii] Such speculations guided decades of often fruitless research.

Early research in Africa found high prevalence of hepatitis B infection among children. In a 1972 study in Senegal, for example, 12 percent of children aged less than 1 year had active infections, increasing to 16 percent by age 7-8 years.[xlix] Because a large proportion of children who are infected with hepatitis B in their first five years of life develop chronic, lifetime infections, high prevalence of infection among children largely explained the observed high percentages of African adults with active infections. In contrast, almost all adults who contract a hepatitis B infection are able to defeat the virus within months, and are left only with antibodies and lifetime immunity. But why were so many African children infected with hepatitis B?

Ignoring blood exposures in healthcare, research on risks for hepatitis B in African children found no answers. Mother-to-child transmission explained only a small minority of infections. For example, in a study reported in 1973, in Kenyan families with one or more children infected with hepatitis B, only 2 of 49 mothers were infected.[l] Researchers in Cote d’Ivoire found evidence of hepatitis B virus in blood from mosquitoes, but whether mosquitoes spread the virus was another matter.[li] More informative research in Papua New Guinea published in 1972 showed that presence or absence of mosquitoes in a community had no impact on prevalence of hepatitis B infection.[lii]

Some studies reported suggestive evidence pointing to healthcare risks. A 1973 paper from Kenya reported a near absence of hepatitis B infection among children aged less than 2 years in a community where ‘childhood immunization is not routinely available.’[liii] A study in Ibadan, Nigeria, in 1974 found that hepatitis B infection was associated with injections and frequent blood tests among adults living in the inner city, but not among residents of the wealthier suburbs.[liv] But no one followed the clues.

After discovering the hepatitis B virus, scientists soon developed tests for prior infection – for antibodies to hepatitis B that persist in the blood after people have defeated the virus. With these tests, studies during the 1970s and later found that 70-95 percent of African adults had past or current infections, of which 8-20 percent had current infections.

Failure on the part of public health managers in Africa to stop practices that transmitted hepatitis B was linked to parallel failure by researchers to investigate whether healthcare procedures transmitted the virus. Did researchers not look because they were influenced by public health managers who did not want anyone to find and report  nosocomial infections? Or did researchers on their own avoid obvious questions?

 

Recognizing bloodborne pathogens: Ebola      

 

In 1976, the first two recognized outbreaks of a frightening new disease, Ebola hemorrhagic fever, made world news. The first began in southern Sudan in August and continued into November. The largest part of the outbreak centered on a hospital in Maridi. A member of the WHO team that investigated the outbreak described the hospital as an ‘epidemic amplifier.’[lv] Contaminated injection equipment may have infected some patients. Hospital staff who nursed patients contracted the virus. (Research during a later Ebola outbreak found virus in blood, saliva, feces, and several other bodily fluids, but not urine.)[lvi] People who stayed home with Ebola passed the disease to family care-givers, but not so often that this could sustain the epidemic. The disease was deadly and fast: 150 of 299 recognized cases died.[lvii] Characteristically, case patients fell ill a week after exposure, and died a week later.

The first recognized death in the second outbreak occurred in Yambuku, a town in north-central DRC, on 5 September 1976. The amplifier of this outbreak was a Catholic mission hospital. Every morning, the hospital allocated five syringes and needles to the nursing staff, which they reused without sterilization throughout the day to inject outpatients and inpatients. The hospital had 120 beds and an average of 200-400 outpatients per day.

Injections accounted for most of the transmissions in the first several weeks of the Yambuku outbreak. At the same time, the virus attacked nurses caring for inpatients. The hospital closed on 30 September after most of its staff fell sick. According to WHO’s International Commission that investigated the outbreak, closing the hospital was ‘likely…the single event of greatest importance in the eventual termination of the outbreak.’[lviii] Transmission occurred less frequently during home-based care, and the last death was recorded on 5 November. From September to November 1976, this outbreak killed 211 out of 237 recognized cases.[lix] The Commission noted: ‘All ages and both sexes were affected, but women 15-29 years of age had the highest incidence of disease, a phenomenon strongly related to attendance at prenatal and outpatient clinics at the hospital where they received injections.’[lx]

During the Yambuku outbreak, ‘no person whose contact was exclusively parenteral [skin-piercing] injection survived the disease.’ The Commission recommended ‘a national campaign to inform health personnel of the proper methods for sterilizing syringes and needles,’ more reliance on oral medication, and controls on ‘the activities of itinerant nurses who treat all diseases by injection.’[lxi]

In 1979, Ebola re-emerged in southern Sudan. As in 1976, a hospital amplified the outbreak. As before, ‘The staff do not routinely practice barrier nursing and often do not sterilize needles, syringes, or other instruments used on the wards.’[lxii] Most infections occurred in family members of people with hospital-acquired infections. Twenty-two of 34 cases died.

 

HIV-2 epidemic in Guinea-Bissau linked to blood exposures       

 

During the several decades before 1981, small numbers of people across West Africa lived with HIV-2 infections. Guinea-Bissau likely had the highest HIV-2 prevalence. Tests of stored blood collected from rural communities in Guinea-Bissau during a 1980 yellow fever survey found that 11 (0.9 percent) of 1,245 children and adults were infected.[lxiii] From Guinea-Bissau, HIV-2 reached Portugal as well as Angola and Mozambique, which were Portuguese colonies until 1975.

A study reported in Chapter 2 linked HIV-2 infections in persons born before 1955 in Guinea-Bissau to three blood exposures (injections to treat sleeping sickness and tuberculosis, and female circumcision).[lxiv] Two studies published in 2006 link HIV-2 infections in adults born before 1973 with other – and more recent – blood exposures. Both studies found that HIV-2 infection was more common in people with scars from smallpox vaccination than in people who had not been vaccinated (smallpox vaccination was discontinued in 1980).[lxv] Healthcare workers remembered that ‘hygiene was not always optimal in the smallpox vaccination campaigns.’ The study team concluded: ‘These campaigns could have contributed to the transmission of blood-born [sic] infections like HIV-2.’[lxvi] Moreover, in one of these studies, people with scars from BCG vaccination – which has continued – were more than twice as likely to be HIV-2-positive as people without such scars.

A review of patients treated for HIV-2 in a Portuguese hospital during 1997-2002 (most of whom were from former Portuguese colonies Guinea-Bissau and Cape Verde) reported that the concentration of infections in older age groups was[lxvii]

 

not compatible with predominant sexual transmission, which would result in a more even distribution through all age groups. These facts point to parenteral exposure (increased use of injections, vaccination campaigns, blood and its derivatives, nosocomial infection, and some traditional practices) as the principle route for the spread of this virus during the epidemic period.

 

Thus, findings from multiple recent studies support the view that many if not most HIV-2 infections have been from blood exposures.

 

HIV-1 spreads out of Africa           

 

During the 1970s, probably the fastest growing HIV epidemics in the world concentrated in IDUs and MSMs in major cities in North America. What was required to ignite these epidemics was that HIV reach an IDU who shared injection equipment or an MSM with multiple sex partners. Once HIV began to circulate among either of these groups, it would reach the other, because many MSMs were also IDUs.[lxviii]

More than a half dozen instances have been documented in which people contracted HIV infections in Africa and returned to Europe or North America before 1981.[lxix] Infected returnees include the Norwegian sailor already mentioned, a pilot transfused in Kisangani in 1976, and a Belgian living in DRC, who retired to Belgium in 1968. All of these known infections, and no doubt many others that are unknown, did not reach IDUs or MSMs, and died out without igniting or contributing to HIV epidemics.

Analyses of HIV sequences provide information about the chain of infection that led from Africa to North American and European IDUs and MSMs. Most HIV in North America, Europe, and Haiti belongs to the HIV-1 B clade. From sequences of B clade HIV collected in North America, two estimated dates for the last common ancestor are 1968 and 1969.[lxx] Including HIV from Haiti, the estimated date recedes to 1966. These analyses present strong evidence that B clade HIV-1 began to spread within Haiti around 1966, and reached North America from Haiti around 1969.

After the chaotic end of Belgian rule in DRC in 1960, UNESCO arranged for educated French-speaking Haitians to work in DRC.[lxxi] If HIV could infect Europeans and North Americans in Africa before 1981 – as it did – it could certainly infect Haitians. This could have occurred through blood or sexual exposures. Similarly, the multiplication of HIV infections in Haiti, as in Africa, occurred through an unknown mix of blood and sexual exposures.

Many people have speculated that HIV passed from Haiti to North America and Europe through MSMs visiting Haiti for low-cost commercial sex. However, if HIV reached North America in the late 1960s, this probably did not occur through MSM sex tourism to Haiti, which did not develop until the 1970s. In the late 1960s, an alternate scenario for the beginning of North America’s HIV epidemic is that a Haitian immigrant IDU shared syringes and needles with other IDUs in Miami, New York, or elsewhere. Supporting this scenario, there is some evidence that HIV had already infected substantial numbers of IDUs in the US as early as 1971-72.[lxxii] Another possibility is that plasma imported from Haiti (before Haiti blocked plasma exports in the early 1970s)[lxxiii] might have gone into blood products that infected an MSM or IDU.

Testing of stored blood samples collected from MSMs in San Francisco reveal 4.9 percent to be HIV-positive in 1978, increasing to 13.5 percent in 1979.[lxxiv] This observed rate of epidemic expansion – doubling in 8 months – roughly agrees with an estimated date of 1969 for the introduction of B clade HIV to the US. If, for example, the number of B clade infections in North America and Europe doubled every 8 months, starting from one infection in 1969, there would have been 1,000 in 1975, and 250,000 in 1981 – which is not far from the estimated number of infections in North America and Europe at that time.

With this scenario one could expect several hundred AIDS cases in North America and Europe before 1981. The US Centers for Disease Control and Prevention (CDC) – looking back from 1981 and later – identified 100 AIDS cases in the US before 1981.[lxxv] The earliest well-established AIDS case in North America, Europe, and Haiti that is not directly linked to Africa was reported in a bisexual musician from Cologne, Germany, whose symptoms began in 1976.[lxxvi] Many cases may have been missed. For example, early AIDS cases among IDUs may have been diagnosed as tuberculosis or otherwise overlooked.

From the US and Europe, the B clade spread not later than the early 1980s to Australia, Japan, South Africa, South Korea, Thailand and elsewhere through IDUs, MSMs, and blood products (especially factor VIII for hemophiliacs).

 

Unsterile healthcare, unresolved questions       

 

Healthcare procedures contributed to HIV transmission in Africa and Haiti during this period. Recent research has been able to identify blood exposures before 1980 as risks for HIV-2 infection. Healthcare procedures that spread HIV-2 would have been even more likely to spread HIV-1. But was healthcare a major or minor factor in HIV-1’s epidemic expansion? New information from sequencing, from stored blood, and from other sources can be expected, over time, to fill in more of the picture of the HIV epidemic during this period.

 



[i] Low-Beer D. ‘The distribution of early acquired immune deficiency syndrome cases and conditions for the establishment of new epidemics’, Phil Trans R Soc Lond B, 2001, 356: 927-31.

[ii] Desmyter J, Goubau P, Chamaret S, et al. ‘Anti-LAV/HTLV-III in Kinshasa mothers in 1970 and 1980 [abstract]’, 2nd Int Conf AIDS, Paris, 23-25 June 1986, abstract s17g.

[iii] Nzilambi N, De Cock KM, Forthal DN, et al. ‘The prevalence of infection with human immunodeficiency virus over a 10-year period in rural Zaire’, N Eng J Med, 1988, 318: 276-9.

[iv] Morvan J, Carteron B, Laroche R, et al. ‘Enquete sero-epidemiologique sur les infections a HIV au Burundi entre 1980 et 1981’, Bull Soc Pathol Exot, 1989, 82: 130-40.

[v] Sonnet J, Michaux J-L, Zech F, et al. ‘Early AIDS cases originating from Zaire and Burundi (1962-1976)’, Scand J Infect Dis, 1987, 19: 511-7; Vangroenweghe D. ‘The earliest cases of human immunodeficiency virus type 1 group M in Congo-Kinshasa, Rwanda and Burundi and the origin of acquired immune deficiency syndrome’, Phil Trans Roy Soc Land B, 2001, 356: 923-5. Hooper E. The River. London: Penguin, 2000.

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[viii] Cook PJ, Burkitt DP. ‘Cancer in Africa’, Br Med Bull, 1971, 27: 14-20. p. 19.

[ix] Hooper E. The River. pp. 762-7.

[x] Hooper E. The River.

[xi] US Census (US) Bureau. HIV/AIDS Surveillance Data Base, June 2003 Release. Washington, DC: US Census Bureau, 2003.

[xii] Rambaut A, Robertson DL, Pybus OG, et al. ‘Phylogeny and the origin of HIV-1’, Nature, 2001, 410: 1047-8; Archer J, Robertson DL, ‘Understanding the diversification of HIV-1 groups M and O’, AIDS, 2007, 21: 1693-700.

[xiii] Vidal N, Mulanga C, Bazepeo SE, et al. ‘Distribution of HIV-1 variants in the Democratic Republic of Congo suggests increase in subtype C in Kinshasa between 1997 and 2002’, J Acquir Immune Defic Syndr, 2005, 40: 456-62.

[xiv] Travers SAA, Clewley JP, Glynn JR, et al. ‘Timing and reconstruction of the most recent common ancestor of the subtype C clade of human immunodeficiency virus type 1’, J Virol, 2004, 78: 10501-6.

[xv] Vidal N, Niyongabo T, Nduwimana J, et al. ‘HIV type 1 diversity and antiretroviral drug resistance mutations in Burundi’, AIDS Res Hum Retroviruses, 2007, 23: 175-80.

[xvi] Los Alamos National Laboratory. HIV Sequence Database. Available at: http://www.hiv.lanl.gov/content/hiv-db (accessed 26 August 2007).

[xvii] Chin J. The AIDS Pandemic. Abingdon, UK: Radcliffe Publishing, 2007. p. 37.

[xviii] World Bank. African Development Indicators 1998/99. Washington DC: World Bank, 1998.

[xix] Carael M. ‘Sexual behavior’, in: Cleland D, Ferry B (eds), Sexual Behavior and AIDS in the Developing World. London: Taylor and Francis, 1995. pp. 75-123.

[xx] Merlin M, Josse R, Trebucq A, et al. ‘Surveillance epidemologique du syndrome d’immunodepression acquise dans six etats d’Afrique centrale’, Med Trop, 1988, 48: 381-9.

[xxi] Auvert B, Buve A, Ferry B, et al. ‘Ecological and individual level analysis of risk factors for HIV infection in four urban populations in sub-Saharan Africa with different levels of HIV infection’, AIDS, 2001, 15 (suppl 4): S15-30.

[xxii] Guthe T. ‘Clinical, serological and epidemiological features of Framboesia tropica (yaws) and its control in rural communities’, Acta Derm Venereol, 1969, 49: 343-68.

[xxiii] Fenner F, Henderson DA, Arita I, et al. Smallpox and its Eradication. Geneva: WHO, 1988. p. 574.

[xxiv] Ibid., pp. 967-8.

[xxv] Ibid., p. 935.

[xxvi] Gordon H. ‘Syringe-transmitted hepatitis [letter]’, Brit Med J, 1978, 2: 953.

[xxvii] Van Lerberghe W, de Bethune X, De Brouwere V. ‘Hospitals in sub-Saharan Africa: Why we need more of what does not work as it should’, Trop Med Int Health, 1997, 2: 799-808.

[xxviii] Declaration of Alma-Ata International Conference on Primary Health Care, Alma-Ata 6-12 September 1978. Available at:

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[xxix] Van der Geest S. ‘The illegal distribution of Western medicines in developing countries: pharmacists, drug peddlers, injection doctors and others. A bibliographic exploration’, Med Anthrop, 1982, 6: 197-219.

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[xxxi] Beheyt P. ‘Contribution a l’etude des hepatites en Afrique: L’hepatite epidemique et l’hepatite par inoculation’, Ann Soc Belge Med Trop, 1953, 33: 297-338. p. 335. Gisselquist translated the quote.

[xxxii] Guyer B, Candy D. ‘Injectable antimalarial therapy in tropical Africa: Iatrogenic disease and wasted medical resources’, Trans R Soc Trop Med Hygiene, 1979, 73: 230-2.

[xxxiii] Drucker E, Alcabes PG, Marx PA. ‘The injection century: massive unsterile injections and the emergence of human pathogens’, Lancet, 2001, 358: 1989-92.

[xxxiv] Schneider WH, Drucker E. ‘Blood transfusions in the early years of AIDS in sub-Saharan Africa’, Am J Pub Health, 2006, 96: 984-94.

[xxxv] Ibid.

[xxxvi] Pieters G. ‘Service de transfusion sanguine pour nourrissons congolais en zone rurale’, Ann Soc Belge Med Trop, 1951, 31: 661-81. pp. 679-80. Gisselquist translated the quote.

[xxxvii] Fleming AF. ‘HIV and blood transfusion in sub-Saharan Africa’, Transfus Sci, 1997, 18: 167-79. p. 168.

[xxxviii] Schneider WH, Drucker E. ‘Blood transfusions’. p. 993.

[xxxix] WHO. ‘Utilization and supply of human blood and blood products: Information provided by the Director-General’, Geneva: WHO, 1975. Doc. no. A28/WP/6.

[xl] Jones P. ‘AIDS: The African connection? [letter]’ Br Med J, 1985, 290: 932.

[xli] Steiner PE. ‘Some aspects of infectious hepatitis’, Ann Soc Belge Med Trop, 1958, 38: 359-64.

[xlii] Blumberg BS, Sutnick AI, London WT, et al. ‘Australia antigen and hepatitis’, N Eng J Med, 1970, 283: 349-54.

[xliii] Cherubin CE, Hargrove RL, Prince AM. ‘The serum hepatitis related antigen (SH) in illicit drug users’, Am J Epidemiol, 1970, 91: 510-17; Koff RS, Isselbacher KJ. ‘Changing concepts in the epidemiology of viral hepatitis’, N Eng J Med, 1968, 278: 1371-80.

[xliv] Blumberg BS et al. ‘Australia antigen and hepatitis’. p. 353.

[xlv] Zuckerman AJ. ‘Syringe-transmitted hepatitis [letter]’, Brit Med J, 1978, 2: 696.

[xlvi] Laird SM. ‘Syringe-transmitted hepatitis [letter]’, Brit Med J, 1978, 2: 953.

[xlvii] Blumberg BS et al. ‘Australia antigen and hepatitis’. p. 351.

[xlviii] Prince AM. ‘Prevalence of serum-hepatitis-related antigen (SH) in different geographic regions’, Am J Trop Med Hyg, 1970, 19: 872-9; Szmuness W, Prince AM, Diebolt G, et al. ‘The epidemiology of hepatitis B infections in Africa: Results of a pilot survey in the Republic of Senegal’, Am J Epidemiol, 1973, 98: 104-10.

[xlix] Szmuness W et al. ‘The epidemiology of hepatitis B infections in Africa’.

[l] Bagshawe A, Nganda TN. ‘Hepatitis B antigen in a rural community in Kenya’, Trans R Soc Trop Med Hyg, 1973, 67: 663-70.

[li] Brotman B, Prince AM, Godfrey HR, ‘Role of arthropods in transmission of hepatitis-B virus in the tropics’, Lancet, 1973; i: 1305-8.

[lii] Hawkes RA, Vale TG, Marshall ID, et al. ’Contrasting seroepidemiology of Australia antigen and arbovirus antibodies in New Guinea’, Am J Epidemiol, 1972, 95: 228-37.

[liii] Bagshawe A, Nganda TN. ‘Hepatitis B antigen’. p. 668.

[liv] Olumide EA. ‘The distribution of hepatitis B surface antigen in Africa and the tropics: Report of a population study in Nigeria’, Int J Epidemiol, 1976; 5: 279-89.

[lv] Garrett L. The Coming Plague. New York: Penguin, 1995. p. 148.

[lvi] Bausch DG, Towner JS, Dowell SF, et al. ‘Assessment of the risk of Ebola virus transmission from bodily fluids and fomites’, J Infect Dis, 2007, 196 (suppl 2): S142-7.

[lvii] ‘Viral haemorrhagic fever’, Wkly Epidemiol Rec, 1977, 52: 177-80.

[lviii] International Commission. ‘Ebola haemorrhagic fever in Zaire, 1976’, Bull WHO, 1978, 56: 271-93. p. 280.

[lix] ‘Viral haemorrhagic fever’.

[lx] International Commission. ‘Ebola haemorrhagic fever in Zaire, 1976’. p. 271.

[lxi] Ibid. pp. 280, 290.

[lxii] Baron RC, McCormick JB, Zubeir OA. ‘Ebola virus disease in southern Sudan: Hospital dissemination and intrafamilial spread’, Bull WHO, 1983, 61: 997-1003. p. 997.

[lxiii] Piedade J, Venenno T, Prieto E, et al. ‘Longstanding presence of HIV-2 infection in Guinea-Bissau (West Africa)’, Acta Trop, 2000, 76: 119-24.

[lxiv] Pepin J, Plamondon M, Alves AC, 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.

[lxv] Jensen ML, Dave S, Schim van der Loeff M, et al. ‘Vaccinia scars associated with improved survival among adults in rural Guinea-Bissau’, PLoS ONE, 2006, 1: e101; Aaby P, Gustafson P, Roth A, et al. ‘Vaccinia scars associated with better survival for adults: An observational study from Guinea-Bissau’, Vaccine, 2006, 24: 5718-25.

[lxvi] Aaby P et al. ‘Vaccinia scars associated with better survival for adults’. p. 5722.

[lxvii] Gomes P, Abecasis A, Almeida M, et al. ‘Transmission of HIV-2’, Lancet Infect Dis, 2003, 3: 534-6. p. 535.

[lxviii] CDC. ‘Update: acquired immunodeficiency syndrome – United States,’ MMWR, 1986, 35: 757-66.

[lxix] Sonnet J et al. ‘Early AIDS cases’; Hooper E. The River.

[lxx] Robbins KE, Lemey P, Pybus OG, et al. ‘U.S. human immunodeficiency virus type 1 epidemic: Date of origin, population history, and characterization of early strains’, J Virol, 2003, 77: 6359-66; Gilbert MTP, Rambaut A, Wlasiuk G, et al. ‘The emergence of HIV/AIDS in the Americas and beyond’, Proc Nat Acad Sci USA, 2007, 104: 18566-70.

[lxxi] Vangroenweghe D. ‘The earliest cases’; Molez J-F. ‘The historical question’.

[lxxii] Moore JD, Cone EJ, Alexander Jr SS. ‘HTLV-III seropositivity in 1971-1972 parenteral drug abusers – A case of false positives or evidence of viral exposure? [letter]’, N Eng J Med, 1986, 314: 1387-8.  

[lxxiii] Starr D. Blood: An epic history of medicine and commerce, New York: HarperCollins, 2000.

[lxxiv] Foley B, Pan H, Buchbinder S, et al. ‘Apparent founder effect during the early years of the San Francisco HIV type 1 epidemic (1978-1979)’, AIDS Res Hum Retroviruses, 2000, 16: 1463-9.

[lxxv] CDC. HIV/AIDS Surveillance Report, 2001, 13(1).

[lxxvi] Sterry W, Marmor M, Konrads A, et al. ’Kaposi’s sarcoma, aplastic pancytopenia, and multiple infections in a homosexual (Cologne 1976) [letter]’, Lancet, 1983; i: 924-5.