Chitnis, A., Rawls, D. & Moore, J. (2000). Origin of HIV-1 in colonial French Equatorial Africa? AIDS Res. Hum. Retroviruses. 16: 5-8.


About this paper, and comments on "The River"

Because this topic is important and controversial, and because the background of this paper is unusual, I (Jim Moore) thought it worth writing a brief account of how it came to be written. Brevity has never been my strong suit; to ignore this history, skip to the paper.

Edward Hooper's response to Chitnis et al. and this preamble
New material from Edward Hooper, summer 2001
Press release from Edward Hooper, 9/28/01: New evidence

25 September 2000: I've added some material;
if you've already seen this preamble (or don't care),
skip ahead to the new bits.

One important new bit: this link to the Safe Injection Global Network (SIGN) homepage at http://www.injectionsafety.org/. Whether HIV originated with OPV (as Hooper has argued), with colonial-era policy (including dirty needles, as we suggest here), or with the re-use of "disposable" needles in the 1950s (as Preston Marx suggests), there can be no question that continued use of non-sterile needles represents a serious risk factor for this and other (known and unknown) diseases.

10 May 2001
Another "new bit" -- there have been several developments re the debate over HIV's origins.

First, a series of papers reporting the absence of any HIV, SIV, or chimpanzee DNA in the remnants of Koprowski's OPV
These have been heralded as "disproving" the OPV hypothesis; since there is always the possibility that SIVcpz contaminated some batch that didn't happen to be preserved, the results do not disprove anything. They do further reduce the likelihood that the OPV hypothesis is correct.
  • Berry, N. et al. (2001). Analysis of oral polio vaccine CHAT stocks. Nature. 410: 1046-1047.

  • Blancou, P. et al. (2001). Polio vaccine samples not linked to AIDS. Nature. 410: 1045-1046.

  • Poinar, H., Kuch, M. & Paabo, S. (2001). Molecular Analyses of Oral Polio Vaccine Samples. Science. 292: 743-744.

  • Rambaut, A., Robertson, D. L., Pybus, O. G., Peeters, M. & Holmes, E. C. (2001). Phylogeny and the origin of HIV-1. Nature. 410: 1047-1048.

Second, Preston Marx & colleagues have published a detailed presentation of the theory that HIV originated post-WWII via unsterile disposable needles
Marx, P. A., Alcabes, P. G. & Drucker, E. (2001). Serial human passage of simian immunodeficiency virus by unsterile injections and the emergence of epidemic human immunodeficiency virus in Africa. Phil. Trans. R. Soc. Lond. B. 356: 1-9.
Marx et al. point out that the probability of spontaneous mutation from SIV to HIV is a function of viral population size, and that since "[n]ormally, human host defences would suppress poorly adapted SIV strains", some mechanism must be found to permit the SIV to remain at high levels in the new host for long enough that such a spontaneous mutation might occur (where "long enough" is on the order of months, and normal immune suppression of unfit virus is on the order of 1-2 weeks). Visually, in (a) SIV titres have to be high for a long time (red curve) to have a realistic chance of mutating to HIV, but normally they are suppressed (black curve) too soon.

The suggested mechanism is serial passaging of virus via unsterile needles, which they tie to the postwar introduction of disposable syringes. High viral population levels are maintained (through a series of bottlenecks) in a series of different individual hosts (figure b).

Chitnis et al. postulate a slightly different mechanism, that of immune suppression due to chronic stress associated with colonial labor camps etc. plus a much lower rate of serial passage via unsterile needles or arm-to-arm vaccination (figure c).

The two papers (Marx et al. and Chitnis et al.) postulate similar mechanisms for the origin of HIV but place the critical events and immediate causes in two very different time periods. In this connection there is a glaring discrepancy between our papers concerning the history of injections in Africa during the colonial period. I do not fully understand the basis for the discrepancy, so only note it here.

Marx et al. provide a table of "History of injectable medications and needle reuse in Africa, 1900-1998", in which the only entry prior to 1920 is for treatment of syphilis, 1900-1920, and it is stated that this "antedates awareness of transmission of infectious diseases by unsterile injections". They also state that prior to WWII injectable drugs were administered "on site and under medical supervision, while closely controlling access to the relatively costly drugs and injecting equipment (UNICEF 1987), using sterile injecting procedures and with access to sterilization equipment on hand. There is little evidence of injection-related transmission of disease in the pre-WWII colonial period (Alland 1970)." [p. 6]. The only indications they list prior to 1952 are syphilis, diabetes and VD.

In total and complete contrast, Headrick (1994) presents tables of numerous specific vaccination campaigns against smallpox and other diseases prior to 1920. For example, Table 3.8 (p. 65) lists 19 separate documented smallpox vaccination campaigns in French Equatorial Africa between 1893 - 1912; the total vaccinated in the 15 for which numbers are available is 82,091. She then states, "In addition, continual vaccination of recruits and porters went on and doctors, missionaries, and sometimes administrators carried out informal, small-scale vaccination tours in their immediate surroundings. Compared to French West Africa, where 1,003,000 vaccinations were performed in 1911 alone, the figures for French Equatorial Africa are not impressive (Delrieu 1914, 375)." [p. 66]. In addition there were (according to Headrick) massive campaigns against sleeping sickness and bacillary dysentery during the 1920s. As to the qualifications and supervision of people administering injections, see Headrick pp. 241-253. One illustrative quote: "Most white missionaries, administrators, company agents, army nurses, agents sanitaires, and hygienistes adjoints went well beyond what their occupations permitted. All dispensed drugs, gave injections, made diagnoses, or performed minor surgery without the direct supervision of a doctor." [p. 244]. As to awareness that unsterile injections could carry disease, Headrick notes e.g. that in 1920, nurses (local technicians) in the sleeping sickness campaigns were trained in "concrete operations: sterilizing water, instruments, and the skin, cleaning slides and ... giving injections. These courses lasted from 4 to 8 weeks." [p. 246; she notes this was the only formal training course for local nurses given at the time.] See also Copeman (1899) for a contemporary discussion of the importance of sterile instruments.

I have no idea how to reconcile these two images of colonial medical practice. For the interested reader, here are the references cited above:

  • Alland, A. (1970). Adaptation in cultural evolution: an approach to medical anthropology. New York: Columbia University.

  • Copeman, S. M. (1899). Vaccination, its natural history and pathology. London: Macmillan.

  • Delrieu. (1914). Organisation du Service de sante en Afrique occidentale francaise (Extrait de Rapport medical annuel 1911). Annales d'hygiene et de medecine colonialies. 17: 349-375.

  • Headrick, R. & Headrick, D. R. E. (1994). Colonialism, Health and Illness in French Equatorial Africa, 1885-1935. Atlanta: African Studies Association Press.

  • UNICEF. (1987). UNICEF in Africa south of the Sahara: a historical perspective. UNICEF History Series, monograph VI.. UNICEF.

End of the May 2001 "new bits"; following is the promised narrative behind our paper.

In late 1998/early 1999, several seemingly unrelated elements came together for me:

  • Because of my participation in the work that made possible genetic identification of chimpanzee subspecies (Morin et al. 1994) I became involved in an email discussion with Beatrice Hahn, Karl Amman and others concerning the conservation implications of linking HIV-1 with central African chimpanzees.

  • A UCSD undergrad, Amit Chitnis, arrived at my door interested in doing an independent study project hopefully related to epidemiology in some way.

The obvious way to link these was for Amit to do a paper reviewing what was known about the origins of HIV-1, and how the new chimpanzee data fitted into it. Then...

  • A visiting colleague, Richard Nisbett, loaned me his copy of "King Leopold's Ghost" by Adam Hochschild, a history of the Congo region between about 1880 - 1930.

  • I happened on a short piece about AIDS in Discover magazine that read in part:
    "Simon Wain-Hobson, a British virologist and AIDS researcher at the Pasteur Institute in Paris, believes that the disruption and migration that characterized post-colonial Africa may have played a key role in the spread of HIV. "The English and the French kept people ruthlessly under control," says Wain-Hobson. They didn't let them move, they didn't let them travel. And what happened finally when the English pulled out was a free-for-all. There were pogroms, there was corruption, there was blackmail, there were movements of populations, the introduction of the motorcar. There was the beginning of the urbanization of Africa, which is a postwar event." These developments, he believes, may have helped HIV expand beyond the narrow range it occupied after it first emerged.
    (January 1999, page 40-41)

  • A recent graduate of UCSC's anthropology department, Diana Rawls, contacted me asking about volunteer opportunities here.

King Leopold's Ghost" made a huge impact on me. According to Hochschild, at one stage those in charge of enforcing colonial rule were required to account for every spent cartridge with proof of a dead African; a severed hand was acceptable. Because cartridges often went astray, it became standard practice to cut the hand from a living person and turn that in; photographs of amputees that were (eventually) distributed in Europe played a role in the "Red Rubber" movement against the abuses of Belgian colonial rule -- the first international human rights campaign. Reading the Discover passage quite frankly infuriated me; the colonial governments did not prevent travel, they regulated it -- those impressed into forced labor camps, or as porters, certainly traveled widely. And post-colonial pogroms need to be viewed in context of the up to 10 million people who died during this period as a result of colonial policies. Not to mention that the urbanization of e.g. Brazzaville and Leopoldville/Kinshasa began well prior to WWII.

Thus it seemed to me (and Amit and Diana) that while the end of colonial rule certainly brought with it the risk factors Wain-Hobson mentions, there was an apparent ignorance of comparable risk factors present during the half-century preceding WWII as well. The purpose of our paper is to bring these factors to the attention of the HIV/AIDS research community. We make no claim to having "demonstrated" an origin scenario for HIV, but we hope to have pointed to a plausible, but seemingly ignored, place to look.

The River

Which brings me to Edward Hooper's book, "The River". This came out after we had written our paper, and what with one thing and another I wasn't able to finish it until December 1999.

First off, I realize now that we are not the first to suggest an HIV origin in colonial, rather than postcolonial, times. The scenario was new to us and reviewers found it acceptable without pointing us to a canonical reference, so there we are. I hope we have added something of real value, at least (e.g., calling attention to the lack of epidemiological information for Guinea may lead to something).

Only after reading Hooper's book do I realize (only partially, I'm sure) the nature of the controversy into which we have wandered. Broadly speaking, there are currently two main scientific schools regarding the origin of HIV (see Hooper, chapter 10):

natural transfer
SIVcpz was transferred to humans in the course of 'normal' contact - butchery, hunting accident, pet bite, etc. To explain the obvious problem of "why now?" the natural transfer school appends the "lost tribe" qualifier: such natural transfers have been going on in remote villages for millennia, but for demographic reasons the virus never spread until this century.

human error
The transfer took place in the course of deliberate or more likely accidental introduction of [chimpanzee-derived] materials into humans. While there have been a number of candidates proposed, Hooper makes a strong case that the only likely one is via contamination of oral polio vaccine (OPV) given to many thousands of Africans in poorly-documented campaigns ca. 1957-58.

To the extent that our paper is seen as supporting one school or the other it is participating in a controversy, so I want to be clear where I personally stand on this (Amit and Diana have moved, and I will update this note as appropriate when I reach them). My stance is developing as I learn about the issues involved; feedback is welcome.

Hooper's book represents a magnificent effort and is a persuasive analysis. I would feel ridiculous comparing it with our brief sketch, but need to at least address points of conflict. Let me be explicit: at this point in time, I suspect that the OPV hypothesis is less likely to be correct than is something along the much vaguer lines we propose -- but this is a weak suspicion only. Hooper does not offer proof, but his argument cannot be dismissed.

Arguments against 'natural transfer' (and rebuttals)

As I see it, the main arguments against the natural transfer/lost tribe scenario are that

The absence of HIV in the New World demonstrates that the transfer didn't occur prior to about 1860 (or the slave trade would have carried it over).
This is evidence against 'natural transfer' only insofar as no 'events' other than e.g. OPV administration occurred since 1860 that might account for the origin of the epidemic. Our paper suggests alternatives.

The absence of recorded AIDS in Africa prior to the 1960s or so demonstrates that it did not exist much earlier, or doctors would have detected it (see e.g. Hooper, p. 163).
This is a critical argument. I am less sanguine about early detection, and note that according to Hooper, AIDS was not officially recognized in Africa until 1983, in Lusaka (p. 89). This means that doctors in the Ruzizi Valley region (site of major OPV distribution) failed to detect AIDS for over 20 years, despite the fact that a 1986 seroprevalence study in Rwanda found 17.8% of urban residents and 1.3% of the rural population HIV-1 positive (Hooper, p. 92). The population of Rwanda in 1980 was roughly 5,000,000, so [very roughly] those 1986 percentages translate into well over 50,000 carriers of HIV. If there were more than 50,000 infected people in 1986, there must have been many thousands in the 1970s; it is hard to see how there might not have been hundreds, probably thousands, of cases of AIDS. Given that doctors missed these, it does not seem implausible (to me) that pre-WWII doctors throughout Africa would have missed the disease as well. See also Hooper, p. 751. For a simplistic look at why it might be easy to miss the early years, click here.

AIDS/HIV-1 among "pygmy" tribes such as the Baka and Efe, among the most plausible candidates for natural transfer (as they live in ape habitat, eat apes, etc.), appears to postdate the origin of the epidemic.
Our paper suggests that in fact it was not "traditional" styles, techniques or circumstances of hunting that were responsible for the origin of the current epidemic, but rather the results of villagers forced to flee into and subsist upon the forest, often with new weapons, that resulted in the initial ape-human transfer[s]. One could argue that under a natural transfer model one would expect forest gatherer/hunters to have adapted, biologically or culturally, to the threat of such zoonoses. I won't make such an argument, but note here a personal observation made while working (briefly) in the R. P. Congo: local bushmeat hunters, after shooting a monkey, would break its bones with the edge of a machete and then cook it prior to skinning/gutting (at least some of the time). The result was that they were totally unfamiliar with the sight of a skinned monkey; when I skinned one (for a taxonomically inclined colleague) the hunters I was with were horrified at its resemblance to a human child. Because the expedition I was with forbade hunting of apes by anyone working for us, I have not seen how chimpanzees are handled (though I understand that in Cote d'Ivoire and probably elsewhere they are usually cut up, as being too large for other handling; Pascal Gagneux, pers. communication). While they did not explicitly avoid contact with blood, their handling of the carcasses did have the result of minimizing such contact (see Durham 1991 for discussion of cultural evolution; I wrote on one aspect of such issues in Moore 1983).

The distribution of Central African chimpanzees (P. t. troglodytes) (in Gabon/Cameroon/CAR/RP Congo) does not match the distribution of early high HIV seroprevalences (in Rwanda/Burundi/Tanzania/Uganda) (Hooper, Postscript).
Anyone moving southeast from the P. t. t. range would hit the Congo River (or its tributary the Ubanji). Steamboat traffic linked Kinshasa/Brazzaville with Kisangani starting in the 1890s, so the connection was well established in the early part of this century. The Ruzizi Valley area, according to Hooper the epicenter of HIV-1 seroprevalence, was affected by ethnic violence in the region that began in 1959 and has continued intermittently ever since (see The International Response to Conflict and Genocide: Lessons from the Rwanda Experience (1996) for a history of the conflict in Rwanda). The role of warfare and conflict in exacerbating the spread of STDs is well-known (see e.g. Hooper pp. 638-640; 767-771). Because it would be easy for the infection to reach Kisangani (and then points east), and the sociopolitical setting was much more conducive to spread of STDs in the Ruzizi region, this distributional objection seems readily answerable.

It is of course critical to determine whether any eastern chimpanzees (P. t. schweinfurthii) carry an SIVcpz that could be ancestral to any of the three known HIV-1 lineages. This should be doable with noninvasive methods; I am sure the work is ongoing.

Whose side are we on? [sic]

While the hypothesis we set out is not consistent with the OPV hypothesis, I do not know in what sense it can really be considered a version of the "natural transfer" school, either. Scenario:
a fisherman flees his small village to escape a colonial patrol demanding their rubber quota, as he runs grabbing one of the unfamiliar shotguns recently arrived in the area. While hiding for several days, he shoots a chimpanzee and, unfamiliar with the process of killing and preparing it, is infected with SIVcpz. On return to the village he finds his family massacred and the village disbanded; he wanders for miles, dodging patrols, until arriving at a distant village. The next day he is seized by a railroad press gang and marched for days to the labor site, where he (along with several hundred others) receives an injection (for reasons he does not understand). During his months working on the railroad, he has little to eat and is continually stressed, susceptible to any infection. He finds some solace in one of the camp prostitutes (themselves imported by those in charge), but eventually dies of an undiagnosed wasting illness -- the fate of hundreds in that camp alone.

Question: What part of that is "natural"?

Why might we care about the origin of HIV?

There are at least four possible reasons why someone might be interested in discovering the origin of HIV. In my opinion, not all are equally "good" and I list them here to cover possibilities, not to endorse all of them. In particular, in the case of HIV origins I do not believe #2 represents a productive goal.
  1. There is a human desire to understand "why", rooted in cognitive science/evolutionary psychology.

  2. If the origin lies in preventable human action, then determining that origin would be tantamount to establishing blame and could be used in a legal action.

  3. the answer might give perspective on other only quasi-related topics. For example, if Africans base refusal to accept public health recommendations on seeing AIDS as a myth invented by former colonial powers (or as an attack on indigenous cultural practices), then an origins account that excludes these might help win over some people and save lives.

  4. "Those who forget the past are condemned to repeat it" -- there may be useful lessons for us that can be derived from understanding the origin of the disease.

I believe that our scenario and Hooper's OPV account differ with respect to the first two reasons, but do not differ at all with respect to the latter two. Neither scenario seems likely to be provable beyond a shadow of legal doubt, but both are plausible enough that to ignore the implications or lessons of either would be foolish. Hooper convinces me that the OPV scenario could have happened, and in my opinion that possibility is the important thing.

And maybe it did, with a different virus. See The Virus and the Vaccine (Atlantic Monthly, Feb. '00), an account of SV40.

References

  1. Durham, W. H. (1991). Coevolution: Genes, Culture, and Human Diversity. Stanford: Stanford University Press.

  2. Hochschild, A. (1998). King Leopold's Ghost : a story of greed, terror, and heroism in Colonial Africa. Boston: Houghton Mifflin.

  3. Hooper, E. (1999). The River: A Journey to the Source of HIV and AIDS. Boston: Little, Brown.

  4. Moore, J. (1983). Carrying capacity, cycles and culture. J. Hum. Evol. 12: 505-514.

  5. Morin, P. A., Moore, J., Chakraborty, R., Jin, L., Goodall, J. & Woodruff, D. S. (1994). Kin selection, social structure, gene flow, and the evolution of chimpanzees. Science. 265: 1193-1201.

ADDITIONAL references on forced labor practices in the region, recommended by Adam Hochschild in response to this website:

"...there are some good sources that detail the continuation of the forced labor system after this, and the vast migrations and flights of refugees that accompanied it. This was particularly severe in the French Congo and the Belgian Congo up until 1930--when the Great Depression, paradoxically, brought some relief for conscripted Africans."
ADDITIONAL references to early vaccination campaigns that may have employed arm-to-arm methods for carrying vaccine to the interior regions of French Equatorial Africa (taken from Headrick 1994; I have not consulted the originals -- I hope that some Francophone interested in this issue will do so!

  • Conan 1913. Organisation du Service de sante en Afrique equatoriale francais. Annales d'hygiene et de medecine coloniales 16: 27-52.

  • Heckenroth, F. 1909. La Vaccine dans la Haute-Sangha Congo francais. Annales d'hygiene et de medecine coloniales 12 402-414.

  • Marque, E. 1911. Tournee de vaccine dans le Chari-Logone. Annales d'hygiene et de medecine coloniales 14: 119-124 and 353-362.

  • Roques. 1902. Variole et vaccine dans la region de Loango (Congo francais) de Novembre 1893 a Septembre 1899. Annales d'hygiene et de medecine coloniales 5: 116-122.


I recently came across the following items.

Merfield, F. G. [with Miller, H.] (1956). Gorillas Were My Neighbours. London: Longmans, Green & Co.
[I have no knowledge of the person or subject outside this book; came across it in a used-book store.] Fred Merfield was an animal collector/hunter who lived in French Cameroons and this is his book about his experiences. It is not structured chronologically, but most of the action takes place shortly after WWI. He states that he lived for 15 years in gorilla country, and 35 years in French Cameroons. While gorillas are not chimpanzees, (a) the two species are similar, and (b) to my knowledge, we have no data on the possible existence of "SIVgor" nor how similar it might be to HIV-1 (if it exists).

Of interest:

He states of the Mendjim Mey tribe [located about halfway between Doume and Youkadouma on his map] that they are the only tribe in Cameroon to regularly hunt gorillas for food [p. 56]; "...among them, it is considered a disgrace to be injured by a gorilla. Should a hunter return with such injuries he is laughed at as a coward, for the people know that the gorilla would not have attacked if the man had not taken fright and run away" [but on p. 170: "They were often injured, but I never heard of one being killed"]. Then, on p. 162-3, he writes: "The Mendjims were a desperately poor people. During the rubber boom of the '20's they had earned a little money to pay their taxes and to buy knives and cloth by selling meat to the native rubber tappers who entered their country. When the boom ended they had nothing to fall back on. They produced only enough food for themselves and their men knew no other art than hunting." They were at this time using primarily or exclusively spears [p. 170].
---This is certainly consistent with the idea that prior to the rubber boom, hunting gorillas was unusual and that colonial pressure for taxes and rubber created an expanded market for hunting bushmeat.

Writing of the village of N'Vonde Manga (apparently about 35 miles east of Yaounde): "The villagers had little skill as hunters and lived mainly by agriculture. The chief, however, possessed a gun and a 'shootman' who knew how to use it. In this he was favored by the Government. ... those who kept their people well-behaved and their plantations productive were allowed to purchase one twelve- or sixteen-bore shotgun."
---This is evidence that guns, and hunting game difficult to get without them, were uncommon under colonial rule. WWI must have put some into circulation, and certainly the supply has been increasing. Point is, while shotguns may have been known in the region for centuries, they were not available. [Interestingly, he tells of being threatened by Maka "cannibals" (just north of Avebe) and astonishing them by shooting a flying parrot with his shotgun; they knew only about rifles and so thought him a supernatural marksman (p. 39).]

"Taxes were collected by native soldiers who toured the forest ... once a year, under a native officer, for no European official ever entered the Mendjim Mey. Even medical missionaries and Government doctors never went beyond Meyoss on the very fringe of the territory" [p. 169].
---This seems relevant to the idea that if HIV-1 had existed in the interior prior to 1960, it would have been reported by Colonial doctors.

Copeman, S. M. (1899). Vaccination, its natural history and pathology. London: Macmillan.
The main thing I gained from this was an understanding of the difference between "variolation" and "vaccination". Variolation, the deliberate inoculation of a healthy person with material from a smallpox pustule, was known for a long time (it was introduced to England in 1721). As I understand it (the book is not explicit) a benign strain could be serially passaged from one person to the next on about an 8-day cycle, with inoculations being done as long as the strain was maintained. One team of brothers claimed to have inoculated 20,000 people with no fatalities [p. 24]. The word "variolation" appears to be used almost synonymously with "inoculation"; inoculation was made illegal in England in 1840.

Vaccination was introduced by Jenner in 1796, and consists of substituting cowpox (vaccinia) for smallpox. The benefits of not using smallpox itself are obvious.

All that is old hat. What may be significant regarding the HIV origins debate is that for a long time, the mechanism of transfer of the culture (variola or vaccinia) was the same. When Copeman writes of vaccination rather than inoculation, at least at times he appears to be distinguishing between the content of the pustules, no more. Vaccinia strains were carried serially from child to child (p. 52), starting with a strain Jenner originated in 1798. See pages 67 through 72. Reference is made to a strain of "humanized lymph [which] was obtained from Birmingham [in 1892], where, to the best of my belief, the same strain has been continuously carried on by means of arm-to-arm vaccination for the past thirty-eight years" (p. 131). This does not necessarily imply a continuous 8-day cycle; it was known from 1853 that lymph could be stored for up to 6 months between host passages (p. 156). Arm-to-arm methods were known to carry risks of transmitting e.g. syphilis (p. 151). The method was abandoned slowly (as best as I can tell, over a period of > 30-50 years), first on the continent and then in England in the late 19th century (p. 149). France was the last country to give it up on the continent.

Copeman and his colleague Richard Thorne Thorne did a survey of methods used on the continent that started in December 1896; Thorne Thorne wrote the report which is appended in the book. Of note:
"It will be noted that in each of the countries concerned, vaccination with calf lymph has become the habitual, if not the universal practice. In some, indeed, we were informed that, although vaccination with humanized lymph is not definitely prohibited under any statute or regulation, yet resort to such lymph by any medical practitioner having official responsibility to the Government is altogether discouraged.
In only one of the places visited -- namely, Paris -- did we find that vaccination was carried out under official sanction with crude calf lymph, and even there the process was limited to vaccination direct from calf to arm, all lymph stored for distribution being glycerinated calf lymph" (p. 190). (Glycerin was found to kill most of the bacterial contaminants of crude lymph.)

The report then goes on to explain that in Paris, "certain classes" were so suspicious of lymph delivered to a vaccination site in tubes -- thinking it derived from humans, and so potentially carrying syphilis, tuberculosis, etc -- that vaccination could only be done by bringing a tethered calf to the site and "vaccinating" people with lymph material scraped directly from the calf.

---Clearly, while arm-to-arm methods had fallen from favor in Europe by 1900, the pace of medical change was slow and doctors practicing in the late 19th century would have been educated (and often practiced) when it was an acceptable if second-choice method. One can also read the suspicion among "certain classes" of Parisians as evidence that vaccine stocks could not always be trusted. Note that it appears to have been somewhat difficult to grow lymph in calves, and (I am speculating here) it may have been that human-passaged lymph was simply easier to obtain--wherever one wants fresh vaccine, there are by definition plenty of humans but not always young calves.

This is relevant to the discussion of HIV-1 origins in two ways. First, arm-to-arm serial passaging would have seemed an acceptable second choice in a region where cattle were scarce and people available. Second, it suggests that one needs to be very careful of the word "vaccination" in the context of the period; it appears initially to have meant only "use of vaccinia" and only later gained generic secondary implications of batch-tested stocks, sterile methods, etc.

Back to list of publications


Origin of HIV Type 1 in Colonial French Equatorial Africa?

Amit Chitnis, Diana Rawls, Jim Moore*
University of California, San Diego
AIDS Research and Human Retroviruses 16(1): 5-8

*to whom correspondence should be addressed:
Anthropology Dept.
University of California, San Diego
9500 Gilman Drive
La Jolla CA 92093-0532
jjmoore@ucsd.edu

ABSTRACT Sociocultural factors during the postcolonial period have been implicated as paramount in generating conditions that promoted both the origin and subsequent epidemic spread of HIV-1 in Africa. We suggest, however, that the origin of the disease may lie in the interaction between colonial practices (e.g., labor camps, non-sterile vaccination campaigns) and traditional bushmeat hunting in French Equatorial Africa. Both the epidemiology of HIV-2 and the colonial history of West Africa appear more complex, but similar conditions existed there and may have contributed to the origin of HIV-2. Focusing the search for the origins of HIV-1 and HIV-2 on this earlier time period may contribute to understanding the evolution of the HIV viruses and the dynamics of emerging diseases.


Human Immunodeficiency Virus Type 1 (HIV-1) seems to have originated in at least three zoonotic transmissions of SIVcpz from chimpanzees (Pan troglodytes troglodytes) to humans, 1 placing the origin of the disease in Central Africa (Cameroon, Gabon, R. P. Congo, lower Central African Republic, and Rio Muni [Equatorial Guinea]). This most probably occurred in the course of hunting and butchering apes for food. Because such hunting is traditional, an obvious question is, "Why now?"

The earliest direct evidence of HIV-1 comes from a blood sample collected in Kinshasa in 1959, 2 and this has led some to concentrate attention on post-World War II (WWII) social changes connected with the end of European colonial power in the region (basically, urbanization combined with "breakdown of colonial control" leading to increased opportunities for transmission of sexually transmitted diseases [STDs]). However, while the post-WWII period did bring many changes to Central Africa that have probably played a role in the origin of the current epidemic, the origin of the disease must lie some years earlier. We suggest that the origin of the disease may have occurred prior to WWII, during the period of French colonial administration of French Equatorial Africa (see Table 1 for chronology). What factors might have contributed to the initial zoonosis and to its subsequent spread during this period, in the absence of evidence of endemic HIV-1?

It seems likely that transmission of SIVcpz to humans has taken place regularly at some low frequency for thousands of years; previously either strains were nonpathogenic in humans (and lost owing to random factors), nontransmissible between humans, or infected individuals died without spreading the virus (owing either to low population density or to [hypothetical] traditional practices limiting sexual promiscuity). We are thus looking for factors associated with the colonial period that would do the following:

  1. Increase exposure risk (i.e., increased reliance on chimpanzee bushmeat and/or changes in hunting or butchery practices resulting in increased risk of blood-blood contact)

  2. Increase the probability of virus transmission (via sexual or blood- blood routes)

  3. Increase the probability of adaptation of the virus to humans, increasing the probability that it would be transmitted.

1) EXPOSURE RISK: Colonial authorities conscripted people for work as porters and as forced labor on railroads and other infrastructure projects; during WWI, they also required villagers to harvest large quantities of rubber. 3-5 All these led to (a) some people fleeing villages to live in the forest, and (b) those conscripted having little time, energy, or opportunity to devote to agriculture. It may be conjectured that both would have led to significant increases in reliance on bushmeat. In addition, increasing access to guns would have played a role in obtaining large animals like chimpanzees.

2) VIRAL TRANSMISSION: There was a massive influx of people into the major cities following WW II, constituting "... movement of previously isolated people into the newly expanding cities" 6 (e.g., the population of Kinshasa increased almost 10-fold from 49,000 in 1940 to 420,000 in 1961; Fig. 1 7). Whatever role this influx may have had in the development of the epidemic, it should be kept in mind that the cities were not "newly" expanding; the population of Kinshasa (and Brazzaville) also increased about 10-fold between 1905 and 1940 (Fig. 1). This earlier period of urbanization would have created conditions favorable to the initial establishment of the disease.

In addition, the social turmoil associated with forced resettlements and labor undoubtedly disrupted traditional sexual practices and networks. More directly, some of the labor camps (of thousands of men) encouraged the presence of women for "recreational" purposes. 5 Finally, massive vaccination campaigns were carried out with limited resources (e.g., six syringes used to screen and treat nearly 90,000 people for sleeping sickness in 1917-19) 8. An unknown proportion of nearly 100,000 smallpox vaccinations prior to 1914 employed arm-arm direct inoculation with material from pox vesicles5, 9 (containing a high concentration of lymphocytes, the primary target of HIV-1).

3) VIRAL ADAPTATION: Arm-arm inoculation may have resulted in passaging of virus through a series of hosts over a relatively short period of time, a process that can select for more virulent pathogen strains. 10 Without knowing more about the details of the arm-arm campaigns (how many successive "donors" were used in the course of a campaign? how many people vaccinated?) the importance of this possible serial passaging cannot be evaluated.

It is not clear whether understanding the origins of HIV-1 will make a difference in treating AIDS, and the above scenario presents only plausible risk factors--it is not clear how or if any of them can be confirmed as playing a role in the origin of AIDS. However, to the extent that it is useful/interesting to understand the origin of HIV-1, if this scenario is correct it suggests that investigation should be concentrated in French archives pertaining to French Equatorial Africa between 1890 and 1930, with special reference to

  1. The details of techniques used during medical campaigns against smallpox and sleeping sickness, particularly those involving Moyen Congo and Gabon, heart of P. t. troglodytes' range),

  2. The prevalence of bushmeat as an alternative food source for porters and laborers (analogous to modern reliance on bushmeat by logging companies 11), and

  3. Changes in the availability of guns (including locally-made muzzle- loaders) and the role such changes may have played in making apes easier to hunt. While there is some literature on the impact of firearms on West African wars and slaving 12, we have found nothing on their early history in bushmeat hunting.

We have not dealt in detail with conditions in West Africa that might have been associated with the origin of HIV-2 from SIVsm carried by sooty mangabeys (reviewed in Ref. 13). Unlike the comparatively sudden impact of colonialism on small-scale societies in French Equatorial Africa, in the west European contact began in the 15th century and interacted in a complex way with existing kingdoms through some 400 years of trade and exploitation--prominently including the slave trade 14. In addition, in West Africa (but apparently not in French Equatorial Africa) smallpox inoculation (variolation) was either indigenous or introduced early 15. These differences make it more difficult to point to a specific time and place as the likely site of the origin of the disease.

It is, however, worth noting that while the highest reported seroprevalence of HIV-2 is in Guinea-Bissau, the greatest diversity of subtypes is in Sierra Leone 13, 16-18. These countries straddle Guinea, a country for which there seems to be relatively little information published about HIV seroprevalence. Northwestern Guinea includes the heart of the 19th century state of Fouta Djalon, which played a major role in the slave trade and did not fall to the French until 1895, not long after the rubber boom began in the area 14 Entire districts were depopulated, and then repopulated, as Fouta fell and antislavery laws were slowly enforced over the next decade. Because it took time to re-clear fields and rebuild abandoned villages, many of these returning people were forced to live by hunting bushmeat. Over 50,000 porters were used per year to headload rubber from the interior to the coast by 1906; a railroad was under construction from 1899 through 1913, mostly with slave labor. The "[d]iversion of labor was so great that food was in short supply and had to be imported" and if laborers sickened they received no rations, having to scavenge in the forests 14. Finally, the French army of the Sudan operating in the late 19th century (mostly in what is now northeastern Guinea and western Mali) made extensive use of slaves for both labor and sex; officers regularly got their choice of slave women and promiscuity was high 14.

In short, similar risk factors were present. They peaked slightly earlier (the turmoil was greatest roughly in 1880-1910) and less sharply (e.g., indigenous variolation was practiced for hundreds of years), but they were present. While spread throughout the region, the combination of clashing states and intensive forced labor was slightly greater in the region of Fouta Djalon and neighboring Wasulu, both located primarily within the modern nation of Guinea.

The widespread occurrence of these epidemiologically-relevant factors prior to WWII suggests that HIV-1, and possibly HIV-2, emerged as infectious human pathogens earlier than generally believed, a conclusion consistent with recent and ongoing genetic analyses. 19

We thank Kathy Creely, David Ho, Bette Korber and Richard Nisbett for their help and encouragement.


REFERENCES
[eprint note: formatting is not that of the journal]

  1. Gao, F., Bailes, E., Robertson, D. L., Chen, Y., Rodenburg, C. M., Michael, S. F., Cummins, L. B., Arthur, L. O., Peeters, M., Shaw, G. M., Sharp, P. M. & Hahn, B. H. (1999). Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature. 397: 436-441.
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  2. Zhu, T. F., Korber, B. T., Nahmias, A. J., Hooper, E., Sharp, P. M. & Ho, D. D. (1998). An African HIV-1 sequence from 1959 and implications for the origin of the epidemic. Nature. 391: 594-597.
    back to text

  3. Hartwig, G. W. & Patterson, K. D. (Eds.) (1978). Disease in African History. Durham (NC): Duke University Press.
    back to text

  4. Headrick, R. (1994). Colonialism, Health and Illness in French Equatorial Africa, 1885-1935. Atlanta: African Studies Association Press.
    back to text

  5. Hochschild, A. (1998). King Leopold's Ghost : a story of greed, terror, and heroism in Colonial Africa. Boston: Houghton Mifflin.
    back to text

  6. Essex, M. E. (1997). Origin of Aquired Immunodeficiency Syndrome. pp. 3-14 IN DeVita Jr., V. T., Hellman, S. & Rosenberg, S. A. (Eds.), AIDS: Etiology, Diagnosis, Treatment and Prevention (4th Edition). Philadelphia: Lippincott-Raven.
    back to text

  7. Hance, W. A. (1970). Population, Migration, and Urbanization in Africa. New York: Columbia University Press.
    back to text

  8. McKelvey, J. J. (1973). Man Against Tsetse: Struggle for Africa. Ithaca (NY): Cornell University Press.
    back to text

  9. Copeman, S. M. (1899). Vaccination, its natural history and pathology. London: Macmillan.
    back to text

  10. Ebert, D. (1998). Experimental evolution of parasites. Science. 282: 1432-1435.
    back to text

  11. Robinson, J. G., Redford, K. H. & Bennett, E. L. (1999). Wildlife harvest in logged tropical forests. Science. 284: 595-596.
    back to text

  12. Inikori, J. E. (1977). The import of firearms into West Africa 1750- 1807: a quantitative analysis. J. Afr. Hist. 18: 339-368.
    back to text

  13. Schim van der Loeff, M. F. & Aaby, P. (1999). Towards a better understanding of the epidemiology of HIV-2. AIDS. 13 (suppl. A): S69-S84.
    back to text

  14. Klein, M. A. (1998). Slavery and Colonial Rule in French West Africa. Cambridge: Cambridge University Press.
    back to text

  15. Herbert, E. W. (1975). Smallpox inoculation in Africa. J. Afr. Hist. 16: 539-559.
    back to text

  16. De Cock, K. M., Brun-Vézinet, F. & Soro, B. (1991). HIV-1 and HIV-2 infections and AIDS in West Africa. AIDS. 5 (suppl. 1): S21-S28.
    back to text

  17. Chen, Z., Luckay, A., Sodora, D. L., Telfer, P., Reed, P., Gettie, A., Kanu, J. M., Sadek, R. F., Yee, J., Ho, D. D., Zhang, L. & Marx, P. A. (1997). Human immunodeficiency virus Type 2 (HIV-2) seroprevalence and characterization of a distinct HIV-2 genetic subtype from the natural range of simian immunodeficiency virus-infected sooty mangabeys. J. Virol. 71: 3953-3960.
    back to text

  18. Gao, F., Yue, L., Robertson, D. L., Hill, S. C., Hui, H., Biggar, R. J., Neequaye, A. E., Whelan, T. M., Ho, D. D., Shaw, G. M., Sharp, P. M. & Hahn, B. H. (1994). Genetic diversity of human immunodeficiency virus Type 2: evidence for distinct sequence subtypes with differences in virus biology. J. Virol. 68: 7433-7447.
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  19. Korber, B., Theiler, J. & Wolinsky, S. (1998). Limitations of a molecular clock applied to considerations of the origin of HIV-1. Science. 280: 1868-1871.
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TABLE 1: CHRONOLOGY

1892:
Start of steamboat service upriver from Kinshasa/Brazzaville to Kisangani. Riverboat traffic regular and significant from this point onward, connecting areas and people who had previously had little contact.

1893 - 1912:
Smallpox vaccination campaigns prior to development of dry vaccine in 1914. The cowpox virus used in vaccinations was difficult to transport into the interior, and so arm-arm vaccinations were used. More than 78,000 people in present-day Gabon, R. P. Congo, Central African Republic and Chad were vaccinated during this period, with at least 35,000 of these being in interior regions where arm-arm methods were most likely to be used.a

late 1890s - 1908:
Period of intense rubber demand. In the Belgian Congo (now Democratic Republic of the Congo), associated with draconian quota system resulting in social disruption and dislocation. From 1908 into 1920s less severe methods were used to force collection.b

1920 - 1935:
French campaign against sleeping sickness -- mobile clinics. Procedure involved (1) examination of blood and lymph to identify carriers, followed by (2) treatment with intravenous drugs. Based on work of Dr. Eugène Jamot who treated > 89,000 people in Ubangi Shari (now Central African Republic) in 1916 using 6 syringes and two hand centrifuges (number of needles and methods of sterilization not known). From 60,000 to 600,000 people treated per year.

1921 - 1930+:
Construction of railroad connecting Brazzaville with the coast (estimated 20,000 deaths), and other infrastructure projects requiring large labor pools. Labor was generally forced and involved concentration of workers from wide (and non-local) areas into camps. The sex ratio in the camps was highly skewed (498 women and 6173 men in one camp, 1929).a

1960:
Independence
----------------------------------
a See Ref. 5.
b See Ref. 6.

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The initial draft of our paper included a simple numerical 'model' to illustrate how long it might take for HIV/AIDS to be detected in Africa. Reviewers all thought it went beyond "simple" to simplistic, and it got pulled. Since webspace isn't as expensive, and since it might help some people, here is a very slightly improved version.

Suppose: a single person is infected, and on average transmits the virus to 2 people over the next 5 years. Given obvious uncertainties about sexual practices, infectability etc. this is very rough; I am assuming here that if the virus originally transferred during a hunting/butchery episode, the early years are in rural, small-village settings; prostitution was not a factor early on. Basically, I'm postulating a doubling every 5 years. What does that look like?

In about 1930, the population of French Equatorial Africa was very roughly about 1.2 million adults (Headrick, 1994). The figure shows the number of "cases" as a percent of 1.2 million, starting with N = 1 in 1900 and doubling every 5 years. Note the vertical axis goes only up to 5.5%.

IMPORTANT Please note that these numbers are not intended to accurately model HIV seroprevalence in Africa. Really the ONLY point here is the trivial--but often forgotten--power of nonlinear processes to (a) appear nonexistent at first, and then (b) suddenly "burst" into being. In the case above, all I intend to show is that even with no change in human behavior, given a disease having relatively low infectivity one would expect a period of years/decades with prevalence too low to be detected (without extraordinary, well-focussed effort or astounding good luck)to precede a "sudden" appearance. For an interesting discussion of this issue applied to a very different problem--the apparently discontinuous acquisition of vocabulary by human infants--see chapter 4 of

Elman, J. L., Bates, E. A., Johnson, M. H., Karmiloff-Smith, A., Parisi, D. & Plunkett, K. (1996). Rethinking Innateness: A Connectionist Perspective on Development. Cambridge: MIT Press.

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since 5 Jan 00
Last update: 24 Jan 2000