Bloodborne HIV: Don't Get Stuck!

Protect yourself from bloodborne HIV during healthcare and cosmetic services

Covid-19 provides an opportunity to challenge lies about HIV in Africa


This website is about bloodborne HIV in Africa, not Covid-19 (hereafter: C19). However, because debates about C19 policies include charges of lies, misinformation, and unethical research, C19  debates have parallels with mismanagement of HIV in Africa. Recognizing these parallels could not only call attention to long-term mismanagement of HIV in Africa but also strengthen debates about C19. For example:

1. Government health agencies and critics charge each other with misinformation about C19 issues. Are health  agencies always reliable? Critics could strengthen their case by calling attention to decades of well-documented lies about HIV in Africa. For example:

Lying about bloodborne risks: For decades foreign and international public health agencies have assured Africans they won’t get HIV from health care even though the same agencies warned their employees they could get HIV from clinics serving the African general public (and arranged special, safe facilities for foreigners). All along evidence was available to show that bloodborne risks were a major contributor to Africa’s HIV epidemics (see Chapters 3 and 6 in [1]). We can quibble about the percentages of HIV from health care, but not about the lies and inadequate response to unexplained infections (no investigations to find and stop their source).

Lying that evidence shows sex accounts for most HIV-positive adults: Yes, evidence shows some adults got HIV from sex penile-vaginal sex. But evidence has never been available to show most infections come from sex. To the contrary: the best evidence says only a minority of HIV-positive Africans got it from sex (see Chapters 3 and 6 in [1]). The long-standing lie that most HIV in Africa comes from sex has led to millions of avoidable bloodborne infections, stigmatized HIV-positive adults with changes of sexual misbehavior, and endorsed long-standing racist stereotypes.

Lying to say Depo is safe: WHO and other public health agencies have lied to Africans about Depo-Provera injections for birth control, dismissing evidence they increase risk for women to get HIV by 40%-50% (for evidence and references, see menu on the right of this page).

2. Critics charge that the US National Institute of Health (NIH), Anthony Fauci, and Gates supported unethical research. These charges could be strengthened by noting long-term and repeated foreign support for unethical HIV-related research in Africa. For example (see also Appendix 2 in [1] or the menu on the right of this page):

Following HIV-positive adults who are unaware of their infections (but researchers know!) to watch them infect spouses, get sick, and die.

Following HIV-positive new mothers who are unaware of their infections (but researchers know!) to watch them infect their babies through breastfeeding.

Giving African women a drug known to increase their risk for HIV and following them to see how fast they get HIV.

Following and testing young African women twice per week in a community where young women get HIV at high rates to study immune responses to very new infections, but without identifying the sources of the new infections, which could protect women in the community.

Where are we going?

Critics of C19 policies challenge official C19 statements and recommendations. Are critics right or wrong? I expect time will tell. But in the meantime, debates  about C19 present an opportunity to recognize and challenge dangerous and demeaning HIV-related public health lies and unethical research afflicting Africans.

Is this a parallel?

After WWII, German Pastor Martin Niemoller confessed that his silence about early government abuses led to more widespread abuses[2]. Here’s a paraphrase of his famous confession – linking HIV lies to current C19 debates:

First they lied to Africans that they would not get HIV from healthcare, and we didn’t complain – because we didn’t take health care in Africa.

Then they followed HIV-positive Africans without telling them they were infected to watch infect their spouses and children, and we didn’t complain — because we didn’t live in Africa.

Then they didn’t warn African women about Depo injections increasing their risk to get HIV, and we didn’t complain -– because we didn’t live in Africa.

Then they asked people in rich countries to believe whatever they said about C19 – and who will help us challenge unreliable official data, analyses, and public health messages (behavior change communications)?

References

1. Gisselquist D. Stopping Bloodborne HIV: investigating unexplained infections. London: Adonis & Abbey, 2021. Available for free download at: https://sites.google.com/site/davidgisselquist/stoppingbloodbornehiv (accessed 28 January 2021).

2. Marcuse H. Martin Niemoller’s famous quotation: “first they came for the communists…” Niemoller Quotation Page [internet] 22 April 2021.  Available at: https://marcuse.faculty.history.ucsb.edu/niem.htm (accessed 18 December 2021). Niemoller’s confession: First they came for the socialists, and I did not speak out — because I was not a socialist. Then they came for the trade unionists, and I did not speak out — because I was not a trade unionist. Then they came for the Jews, and I did not speak out — because I was not a Jew. Then they came for me — and there was no one left to speak for me.

Please don’t bother me with facts, I like my sex fantasies!


Sex, sex, sex. Beginning in the late 1980s, several years after HIV was recognized in Africa, health bureaucrats, staff, and researchers have peddled salacious and racist fantasies that almost HIV-positive adults got it from sex.

But what about facts?

One way to see how people in a community have been getting HIV is to see who has viruses that are similar. Because HIV changes over time as it multiplies in anyone it infects, when two people are found to have very similar HIV (similar components in a similar order), one likely infected the other. Studies that look for people with similar HIV in African communities provide facts to test the fantasy that male-female sex accounts for almost all HIV-positive adults.

Here’s an example: During 2011-15, research staff drew blood from 25,882 people in 40 communities in Rakai District in Uganda.[1] More than 5,000 were HIV-positive. Researchers were able to describe HIVs (what components, what order) from 2,552 HIV-positive adults. Among the 2,552 HIV, researchers found 537 pairs with very similar HIV (“highly supported phylogenetic linkages”[page 5 in reference 1]), indicating that one person in the pair likely infected the other.

What do those pairs tell us about sexual fantasies?

1. Setting aside 176 spouse pairs with similar HIV (more on spouses below), there were 361 (=537-176) very similar non-spouse pairs. Here’s where the fantasy runs afoul of facts: 161 (45%) of those 361 non-spouse pairs were same-sex pairs, linking a man with a man, or a woman with a woman. Since the sex of whoever infected anyone seems to have been irrelevant (near equal numbers of same-sex pairs as male-female pairs), the obvious conclusion is that most transmission had nothing to do with sex. Most infections likely came from bloodborne risks such as unsterilized needles, syringes, catheters, saline bags, razors, lancets, etc., not from a sex partner. What about the 200 (=361-161) unmarried male-female pairs? Since the study says nothing about the sexual behavior of anyone in those non-spouse pairs, supposing sexual transmission is based on sex fantasy, not evidence.

2. What about spouses with similar HIV? The study collected and described HIV from 331 husband-wife couples. Only 176 (53%) of the 331 couples had similar HIV. Almost half of the couples (155 of 331) had non-matching HIV, which means husbands and wives likely got HIV from other blood or sex risks, not from their partners. In other words: Sexual transmission seems to be inefficient and slow in Africa as it is elsewhere in the world.

Instead of acting like scientist (respecting evidence), the research team that reported the above facts simply rejected same-sex pairs as mistakes: We don’t like the facts, so we ignore them! Let’s stick with sex fantasies! For example:

Example  1: In a 2021 sub-study, the research team used male-female pairs previously identified to fantasize about the ages of men and women having sex, ignoring same-sex pairs.[2] Because the average HIV-positive man is older than the average HIV-positive woman, one could expect pairs to include older men and younger women no matter how one infected the other (sex, or shared skin-piercing instruments). Duh! But the study team opted for sex fantasies: Hah, older men chasing younger women!  

Example 2: To estimate direction of HIV transmission between Rakai’s lakeshore communities and inland communities, the study team rejected 200 same-sex pairs as misleading (not agreeing with sex fantasies). Then, “[w]e further analysed the … male−female linkages to infer the direction of transmission”[page 6 in  reference 3]. Even so, what they found did not agree with sex fantasies – HIV was going from inland communities with lower percentages of adults infected to lakeshore communities with higher percentages infected. If it was going by sex, that doesn’t make a lot of sense – in sex partnerships across communities, the transmitting (HIV-positive) partner would more likely come from the lakeshore, where adults were more likely to be HIV-positive. On the other hand, if it were going by bloodborne risks in clinics and cosmetic services in inland communities along main roads, then the direction of transmission makes sense if, as seems likely, people from lakeshore communities visit facilities along major roads. Hence, it’s likely many male-female pairs were linked not by sex but by reused and unsterilized skin-piercing instruments.

Peddling sex fantasies about Africa’s HIV epidemic is not a victimless lie 

1. Sex fantasies distract everyone’s attention from bloodborne risks that people face in clinics and cosmetic services. That leads to infections.

2. Sex fantasies stigmatize HIV-positive Africans. Consider, for example, a woman who tests HIV-positive during antenatal care, and then her husband tests negative. Here’s what those who peddle sex fantasies are, in effect, saying to the husband: “Your wife had a boyfriend and lied about it!” What about a teenage boy or girl testing HIV-positive, or a husband? All slimed with abusive fantasies.

3. Health pros who push these fantasies suffer as well. If they know it’s a lie, how do they live with themselves? If they are too scared to investigate unexplained infections to find and stop unsafe practices in healthcare, how can they respect themselves and their profession?

References

1. Ratmann O, Grabowski MK, Hall M, et al. Inferring HIV-1 transmission networks and sources of epidemic spread in Africa with deep-sequence phylogeneetic analysis. Nat Commun 2019; 10: 1411. Available at: https://www.nature.com/articles/s41467-019-09139-4.pdf (accessed 13 December 2021).

2. Xi X, Spencer SEF, Hall M. Inferring the sources of HIV infection in Africa from deepsequence data with semi-parametric Bayesian Poisson flow models. arXiv [internet] 29 October 2021. Available at: https://arxiv.org/pdf/2110.12273.pdf (accessed 6 December 2021).

3. Ratmann O, Kagaayi J, Hall M, et al. Quantifying HIV transmission flow between high-prevalence hotspots and surrounding communities: a population-based study in Rakai, Uganda. Lancet HIV 2020; 7: e173-e183. Available at: https://www.ncbi.nlm.nih.gov/labs/pmc/articles/PMC7167508/ (accessed 13 December 2021).

Ignoring children’s HIV risks – is there any good excuse?


In Mozambique, a national survey in 2015 found that a third of HIV-infected children age 6-23 months had HIV-negative mothers.[5] In a national survey in eSwatini in 2006-7, 22% of tested mothers of HIV-positive children age 2-12 years were HIV-negative.[4]

With evidence like that, why does UNAIDS say that 100% of HIV-positive children age 0-14 years got HIV from their mothers?[2] Why do health experts from US and African estimate that 97% of HIV-positive children aged 10-14 years in five countries in southern Africa got HIV from their mothers?[1]

Ignoring unexplained infections — not finding and stopping risks – allows risks to continue and to infect others. Too many foreign and national experts have been doing just that – ignoring unexplained infections.

How do children with HIV-negative mothers get HIV? The answer to that question depends on the time and place. Answers come with on-site investigations to find and stop specific risks. Where people have looked – in countries outside sub-Sahara Africa – investigations have found hundreds to thousands infected from health care procedures. Investigations found and stopped risks – and, most importantly, protected others (see “outbreaks and unexpected infections” in the menu on the right).

Here’s a letter recently rejected by Clinical Infectious Diseases (below).Because UNAIDS, health experts, and journal editors are not warning Africans to find and stop blood-borne HIV risks, it’s up to people at risk to begin informal investigations and to push their governments to join. Africans at risk have been waiting decades for health experts to discover their hearts and to do the right thing.  

REJECTED LETTER: Unexplained HIV infections in children and adolescents in Africa

TO THE EDITOR – In a recent paper, Low and colleagues[1] use data from national surveys in five countries during 2015-17 (eSwatini, Lesotho, Malawi, Zambia, and Zimbabwe) to examine HIV in adolescents aged 10-19 years. Survey data are sufficient to describe short-comings in finding and treating cases: among 707 identified HIV-positive adolescents, 39.1% had not been diagnosed before the survey, and only 47.1% had suppressed viral loads.

On the other hand, survey data are insufficient to determine sources of infections. For example, setting aside 22 adolescents with recent infections, Low and colleagues estimate 71% (485) of the remaining 685 got HIV from their mothers even though only 35% (= 242/685) of their mothers tested HIV-positive. The only other risk identified from the survey was having had sex, which was reported for 22% (= 150/707) of infected adolescents (without attention to partners’ HIV status). Unspecified behavioral risk was reported for 10% (= 72/707) of infections; surveys did not ask about skin-piercing health care or cosmetic services.

Focusing  on children, Low and colleagues’ estimate 97% of infections in children aged 10-14 years came from mothers. Similarly, UNAIDS assumed all infections in children aged 0-14 years came from mothers.[2] On the other hand, Ng’eno and colleagues, with data from a 2012 national survey in Kenya, identified no risk for 4 of 9 HIV-positive children aged 10-14 years.[3]

Table 1: Attributed risks for HIV infections in Africans aged 0-14 years

Source of estimatecountriesages (years)% of infections attributed to mother-to-child transmission
UNAIDS[2]all0-14100%
Low et al[1]eSwatini, Lesotho, Malawi, Zambia, Zimbabwe10-1497%

Low and colleagues’ and UNAIDS’ low estimates of  the percentages non-vertical HIV infections in children disregard relevant evidence. For example: in a 2006-7 national survey in eSwatini, 22% of mothers of HIV-positive children aged 2-12 years tested HIV-negative (among tested mothers only)[4]; and in a 2015 national survey in Mozambique, 33% of mothers of HIV-positive children aged 6-23 months tested HIV-negative.[5] Moreover, many mothers surveyed in eSwatini and Mozambique likely got HIV from infected children (in two studies with relevant data, breastfeeding children infected from health care infected 40% to 60% of their mothers[6]). If Low and colleagues had looked for HIV in children aged 0-9 years in the five surveys they used to study HIV in adolescents, would they have found similar percentages of unexplained infections?

Disputes about estimates are, of course, matters of judgment. But Low and colleagues’ and UNAIDS’ low estimates of non-vertical (unexplained) HIV infections in children arguably support government decisions not to investigate unexplained infections, which is a matter of fact not judgment: governments in sub-Saharan Africa have not investigated unexplained infections. Unexplained infections challenge governments to investigate to find and fix dangerous skin-piercing procedures to protect public health (see, e.g., recent investigations in Pakistan[7] and Cambodia[8]).

Avoidable infections from undiscovered risks are not the only consequences when public health experts overlook unexplained HIV infections. Low and colleagues decry stigma as an obstacle to finding and treating HIV-positive adolescents. Unfortunately, their estimates contribute to stigma: attributing almost all infections to mothers or sex stigmatizes parents of infected children and/or infected adolescents, whether or not sexually active.

References

1. Low A, Teasdale C, Brown K, et al. Human Immunodeficiency Virus Infection in Adolescents and Mode of Transmission in Southern Africa: A Multinational Analysis of Population-Based Survey Data. Clin Infect Dis 2021, 73: 594-604. doi: 10.1093/cid/ciab031. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8366830/ (accessed 14 September 2021).

2. Mahy M, Penazzato M, Ciaranello A, et al. Improving estimates of children living with HIV from the Spectrum AIDS Impact Model. AIDS 2017; 31:13–22. Available at: https://pubmed.ncbi.nlm.nih.gov/28301337/ (accessed 24 October 2021),

3. Ng’eno BN, Kellogg TA, Kim AA, et al. Modes of HIV transmission among adolescents and young adults aged 10-24  years in Kenya. Int J STD AIDS 2018; 29:800–5. doi:10.1177/0956462418758115. Available at:  https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5995643/pdf/nihms950188.pdf (accessed 12 September 2021).

4. Okinyi M, Brewer DD, Potterat JJ. Horizontally acquired HIV infection in Kenyan and Swazi children. Int J STD AIDS 2009; 20: 852-857. Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/19948900 (accessed 27 October 2018). Available at: http://www.interscientific.net/IJSA2009Okinyi.html (accessed 15 October 2018).

5. Mozambique: Survey of Indicators on Immunization, Malaria and HIV/AIDS in Mozambique (IMASIDA) 2015, Supplemental Report Incorporating Antiretroviral Biomarker Results. Maputo: Ministério da Saúde (MISAU) Instituto Nacional de Estatística (INE), 2019. Available at: https://www.dhsprogram.com/pubs/pdf/AIS12/AIS12_SE.pdf (accessed 15 October 2021).

6. Little KM, Kilmarx PH, Taylor AW, et al. A review of evidence for transmission of HIV from children to breastfeeding women and implications for prevention. Pediatr Infect Dis J 2012; 31: 938-942. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4565150/ (accessed 15 October 2021).

7. Ahmed T. Ratodero HIV stats continue to rise 19 months after outbreak. Samaa 1 December 2020. Available at: https://www.samaa.tv/news/2020/12/ratodero-hiv-stats-continue-to-rise-19-months-after-outbreak/ (acessed 12 December 2020).

8. Rouet F, Nouhin J, Zheng D-P, et al. Massive iatrogenic outbreak of human immunodeficiency virus type 1 in rural Cambodia, 2014-2015. Clin Infect Dis 2018; 66: 1733-1741. Available at: https://pubmed.ncbi.nlm.nih.gov/29211835/ (accessed 24 February 2021).

Africans at risk when health experts ignore unexplained HIV infections


Across sub-Saharan Africa, governments have not investigated unexplained HIV infections (not from sex or mother-to-child). If you know of one or more unexplained infections in your community, you might be at risk to get HIV when you go for health care, manicure, or other skin-piercing procedure. Because governments have not investigated, it’s up to people at risk to start their own informal investigations — asking people in the community if they know of more unexplained infections, and asking if they have any ideas about where doctors or others might be giving skin-piercing procedures with unsterile instruments. Governments will follow and help if people lead.

Failing their duty, government health experts and foreign experts and researchers have ignored evidence of HIV infections from unsafe healthcare. Here’s an example from one of the world’s worst HIV epidemics — in uMkhanyakude district, KwaZulu-Natal Province, South Africa.

In 2019 a random sample of adults in a large mostly rural study area in uMkhanyakude district found 67.5% of women aged 30-40 years to be HIV-positive (see page e972 in reference 5, below). How could so many be infected? For almost two decades, health experts have been surveying and studying people in the district — without ever bothering to investigate unexplained infections, without finding and stopping their source, and without warning people at risk.

Why have health experts been so negligent and careless about public health? Dense, heartless, some other excuse?

In August  2021, I submitted the following short account of evidence of bloodborne HIV transmission in the study area as a letter to the Proceeding of the National Academy of Science. The editor rejected it without explanation.

Submitted and rejected letter: HIV-1 incidence patterns in KwaZulu-Natal

            Dr Akullian and co-authors report large reductions in HIV incidence, especially for young men and women, during 2012-19 in the Africa Health Research Institute’s surveillance area in KwaZulu-Natal, South Africa.[1] Even so, incidence remained high: in 2019, the highest estimated age-specific incidence was circa 4.4% per year for women and circa 2.0% per year for men (see Figure 4C in [1]).

            Although changes in HIV incidence are clear, the reasons for those changes are less well established. Authors ignore the possibility – hypothesis – that non-sexual transmission through skin-piercing procedures in health care and cosmetic services might be making a substantial contribution to incidence in the study area. In ignoring this hypothesis, authors disregard evidence from the study area, including:

            * Unexplained infections: During 2004-15, adults and adolescents who claimed to be virgins accounted for 189 (8%) of 2,367 recognized incident infections (Table 1 in [2]).

            * A cluster of 63 HIV with closely related sequences: Sequence analyses dated the cluster’s most recent common ancestor to June 2013; within 18 months to November 2014, infections from this common ancestor had reached 63 persons (slide 10 in [3]). The speed of transmission required to explain this cluster has been seen in nosocomial outbreaks (e.g., in Cambodia[4]). Moreover, evidence from the study area suggests sexual partner change made little or no contribution to the cluster: only 43 (1.8%) of 2,367 adults with new infections in the study area during 2004-15 reported more than one partner in the previous year (Table 1 in [2]).

            * Incidence too high to be explained by sex: The estimated circa 4.4% per year age-specific peak incidence rate in women in 2019 is greater than could be expected based the estimated percentage of their partners with unsuppressed viral loads: in 2019 <20% of men aged 30-39 years and lower percentages in other cohorts had unsuppressed viral loads (Figure 3A in [5]). In two large studies in Africa that included discordant couples in which many if not most wives did not know their husbands were infected, wives got HIV at rates of 10.5-12 per 100 person-years[6,7]. If women in the study area with sexual exposure to HIV got infected at such rates, one would expect circa 2% incidence per year, far less than peak age-specific incidence. This estimate ignores mitigating factors, such as concordant positive partnerships and condom use (during 2012-17, averages of more than 60% of women and 70% of men reporting condom use[8]).

            It is not possible to explain the above evidence from the study area without the hypothesis that bloodborne transmission is important. Alternately, one could hypothesize that evidence is wrong, and explain how and why that could be so. Researchers’ failure to respect – accept or reject – evidence pointing to bloodborne transmission parallels public health agencies’ failure to investigate unexplained infections: identifying sites with skin-piercing procedures, testing others attending such sites to find more victims, and thereby finding and stopping sources of bloodborne transmission.

References

1. A. Akullian et al. Large age shifts in HIV-1 incidence patterns in KwaZulu-Natal, South Africa. PNAS 118: e2013164118 (2021). [Available at: https://www.pnas.org/content/118/28/e2013164118, accessed 8 September 2021.]

2. A. Akullian et al. Sexual partnership age pairings and risk of HIV acquisition in rural South Africa. AIDS 31: 1755-1764 (2017). [Available at: https://pubmed.ncbi.nlm.nih.gov/28590328/, accessed 8 September 2021.]

3. C. Coltart et al. Ongoing HIV micro-epidemics in rural South Africa: the need for flexible interventions. Conference on Retroviruses and Opportunistic Infections, Boston, 4-7 March 2018. Abstract 47LB and oral abstract (2018). [Available at: http://www.croiwebcasts.org/console/player/37090?mediaType=slideVideo&amp;, accessed 8 September 2021.]

4. F. Rouet et al. Massive iatrogenic outbreak of human immunodeficiency virus type 1 in rural Cambodia, 2014-2015. Clin. Infect. Dis. 66, 1733-1741 (2018). [Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5963970/pdf/cix1071.pdf, accessed 8 September 2021.]

5. E. B.  Wong et al. Convergence of infectious and non-communicable disease epidemics in rural South Africa: a cross-sectional, population-based multimorbidity study. Lancet Glob. Health 9, e967–76 (2021). [Available at: https://www.thelancet.com/action/showPdf?pii=S2214-109X%2821%2900176-5, accessed 8 September 2021.]

6. T. C. Quinn et al. Viral load and heterosexual transmission of human immunodeficiency virus type 1. N. Engl. J. Med. 342, 921-929 (2000). [Available at: https://pubmed.ncbi.nlm.nih.gov/10738050/, accessed 8 September 2021.]

7. L. M. Carpenter et al. Rates of HIV-1 transmission within marriage in rural Uganda in relation to the HIV sero-status of the partners. AIDS 13, 1083-1089 (1999).

8. A. Vandormael et al., Declines in HIV incidence among men and women in a South African population-based cohort. Nat. Commun. 10, 5482 (2019). [Available at: https://www.nature.com/articles/s41467-019-13473-y, accessed 8 September 2021.]

Geologists can’t find sand in Saudi Arabia!


OK, that’s not so. Geologists know there’s sand in Saudi Arabia. But what about health experts not finding HIV infections from health care in Africa?

All the best evidence says blood exposures in health care and possibly also cosmetic services – not sex — have been driving Africa’s HIV epidemics all along. (Yes, this is a controversial statement; so here are details and references[1].) But just like geologists who don’t know there’s sand in Saudi Arabia, health experts have only rarely identified HIV infections from health care in Africa. And when they have found evidence pointing to HIV from health care, they have mostly ignored and/or denied that happened. For example:

  • A self-declared virgin is HIV-positive? Experts say she lied (administering a double stigma – she’s a liar and a slut).
  • Baby is infected but mother not? Experts can’t deny that, so they ignore it.

I post this blog on the 40th anniversary of the first report of AIDS on 5 June 1981.[2] As soon as AIDS cases were discovered in the US, doctors recognized similar cases in Africa. In the 40 years from 1981 to 2021, medical researchers could have found and stopped HIV transmission through hospitals and clinics in Africa. But that hasn’t happened. No government in sub-Sahara Africa has investigated any unexplained HIV infection to find others infected from the same clinics and to find and stop the risks. Just let it happen, in other words.

When HIV transmission through health care has been so common for so long, how can health experts miss it? To miss it, experts have to be either naturally incompetent (simply not up to the job) or professionally incompetent (keeping quiet so as to keep their jobs).

Such consistent and widespread incompetence requires bad international leadership – discouraging people from finding and/or talking about HIV from health care. WHO, UNAIDS, CDC, and leading US and European universities and journals have helped to organize and enforce deliberate incompetence. Too many people have accepted bad leadership. As a consequence, Africans have suffered tens of millions of unnecessary HIV infections.

Finally, to avoid misunderstanding: sex is a risk. But it’s a secondary risk – people who got HIV from unsafe health care can infect unsuspecting sex partners. So: test sex partners for HIV, because you can’t tell from their sexual behavior if they might be infected. But don’t just worry about sex – blood exposures may be your biggest risk.

References

1. See chapter 6 in: Gisselquist D. Stopping Bloodborne HIV: investigating unexplained infections. London: Adonis & Abbey, 2021. Available at: https://sites.google.com/site/davidgisselquist/stoppingbloodbornehiv

2. Gottleib MS, Schanker HM, Fan PT, et al. Pneumocystis pneumonia – Los Angeles. Morb Mort Weekly Rep 1981; 30: 250-252. Available at: https://www.cdc.gov/mmwr/preview/mmwrhtml/june_5.htm (accessed 5 June 2021).

Mistakes explain Africa’s HIV epidemics: Evidence from a double-barreled smoking gun


A recent double-barreled smoking gun calls attention to mistakes that fuel Africa’s HIV/AIDS epidemics.[1] The first smoking barrel is the discovery of an HIV outbreak in South Africa which is best explained by bloodborne transmission during health care.[2] The second smoking barrel is the subsequent silence by public health and HIV/AIDS experts and officials about the likelihood that unsafe health care caused the outbreak. (A “smoking gun” is “an object or fact that serves as conclusive evidence of a crime or similar act…”[3])

First smoking barrel: HIV outbreak in Kwazulu-Natal, 2013-14

South Africa has one of the world’s most intense HIV epidemics with more than 20% of adults infected.[4] Things are even worse in some places: for example, in a large mostly rural study area in KwaZulu-Natal province more than 60% of women aged 30-49 years were HIV-positive in 2016.[5]

In 2010-14, researchers collected HIV from a random sample of adults in the KwaZulu-Natal study area mentioned in the previous paragraph. The team then sequenced 1,376 HIV samples (i.e., determined the order of HIV’s constituent parts). Because HIV changes over time, similar sequences from two or more people suggest recent and close transmission linkages. Among the 1,376 sequences, the study team found a cluster of 63 very similar HIV. The study team estimated that HIV from one person in June 2013 had somehow reached and infected 63 people within 17 months through November 2014.[2]

The cluster reported from the study area is similar to clusters that governments outside sub-Sahara Africa have investigated and traced to unsafe health care. For example, the diagram linking 63 infections in KwaZulu-Natal (see slide 10 in reference [2]) is similar to diagrams linking HIV sequences from outbreaks in Libya in 1995-99 and in Cambodia in 2013-14.[6,7]

Because the 1,376 HIV came from a random sample of an estimated 9% of HIV-positive adults in the study area, the observed cluster of 63 infections may well be 9% of a much larger cluster in the study area. Moreover, because many of the 63 HIV came from a town on the border of the study area, the cluster likely extends outside the area; and transmission appeared to be ongoing when the study stopped collecting HIV samples in 2014.

Because it is almost impossible for such an outbreak to come from anything other than bloodborne transmission, the government of South Africa could protect public health by investigating to find and fix whatever caused it: asking people in the cluster what skin-piercing procedures they received and where during 2013-14, and then inviting others who visited suspected facilities to come for HIV tests. From 1986, at least 11 governments outside sub-Saharan Africa have investigated unexplained HIV infections to find and fix health care procedures that had caused large HIV outbreaks, infecting more than a hundred to as many as 50,000 people in China.[8,9]

The study that reported this KwaZulu-Natal outbreak suggested it might be from sex, but provides no information about sexual risks for anyone in the cluster. In any case, the possibility that sex could transmit HIV from 1 to 63 infections (much less hundreds) in 17 months is vanishingly small, considering:

  • Even between spouses who are unaware one spouse is infected, it takes on average years for one to infect the other. In a 2016 national survey in South Africa fewer than half of men and women with HIV-positive spouses were themselves infected.[4]
  • According to self-reported sexual behavior, having multiple partners had little to do with HIV transmission in the study area. Repeat surveys in the study area during 2004-15 identified 1,265 new HIV infections in adults with information on sexual behavior; only 43 (3.4%) of adults with new infections reported more than one sex partner in the previous year, while 189 (14.9%) said they were virgins (Table 1 in reference [10]).
  • Widely quoted estimates of the risk to transmit HIV through penile-vaginal sex say transmission occurs in fewer than 1 in 1,000 coital acts.[11]

Even if someone, nevertheless, wants to argue or believe that sex could somehow account for all infections in the cluster, bloodborne transmission during health care remains a possible explanation. That possibility challenges the government of South Africa to investigate to protect public health.

Second smoking barrel: Expert and official silence about the likelihood unsafe health care cased the outbreak

Researchers from the African Health Research Institute and the University College London, who collected HIV from the study area in 2010-14, subsequently sequenced HIV samples and discovered the cluster in 2017. They reported their discovery on 5 March 2018 at the Conference on Retroviruses and Opportunistic Infections (CROI) in Boston.[2] Although the cluster suggests unsafe health care transmitted HIV:

  • We have found no evidence government of South Africa has investigated to protect public health.
  • During their 2018 presentation at CROI the research team did not acknowledge the possibility that unsafe health care caused the outbreak, and none of the discussants even mentioned such risks.[2]
  • To the best of our knowledge, as we are writing this more than two years after the cluster was reported in 2018, no expert in HIV sequencing and no official in any international or foreign health organization or agency has publically acknowledged the possibility the cluster comes from unsafe health care.

Considering the many experts knowledgeable about sequencing and about Africa’s HIV epidemics, the fact that no one has said the obvious – that the cluster likely (or at least possibly) comes from unsafe health care – is strong evidence that people are choosing to keep silent. That in turn suggests they are aware of pressures not to say what is obvious. (The only exceptions to this silence are blogs on this website [search “KwaZulu-Natal] and several papers posted on SSRN by the authors of this blog, for example [1]).

Silence is strong circumstantial evidence – smoking gun evidence – that influential officials who control research funds and jobs for people working on HIV do not want them to talk about health care transmitting HIV in Africa. If anyone wants to challenge evidence-based suspicions that organizations such as the United States’ National Institutes of Health enforce such silence, the way forward is not to debate whether that is so but simply to break the silence – to acknowledge the cluster likely came from bloodborne transmission, and to recommend government of South Africa to investigate. Setting aside debate, the priority should be protecting patients and stopping Africa’s epidemics.

Perspective and context: 35 years of evidence and silence about HIV transmission during healthcare in Africa

Genetic evidence from the HIV cluster in KwaZulu-Natal, and subsequent silence about that evidence, are only the latest in decades of evidence and silence about health care transmitting HIV in Africa.[12-14] The double-barrelled smoking gun discussed in this note is remarkable because it involves experts in gene sequencing, a group that has only recently gotten more involved in HIV-related research in Africa and therefore has had no investment or involvement in decades of dismissive silence about unexplained and likely bloodborne HIV infections in Africa (such as HIV-infected children with HIV-negative mothers, HIV-positive virgin men and women).

Those who are silent are not explaining why they are silent. But insofar as Africans are at risk, the reasons for experts’ and officials’ silence is not important. What is called for, to protect Africans at risk, is not to explain why experts and officials are not doing their jobs, but rather to get some investigations underway and to warn Africans about risks to get HIV from health care as long as those risks are not found and fixed.

References

  1. Gisselquist D, Collery S. Africa’s HIV epidemics: Evidence from a double-barreled smoking gun. Social Science Research Network, 1 May 2020. Available at: https://papers.ssrn.com/sol3/papers.cfm?abstract_id=3590251 (accessed 1 May 2020).
  2. Coltart CEM, Shahmanesh M, Hue S, et al. Ongoing HIV micro-epidemics in rural South Africa: the need for flexible interventions. Oral abstract. Conference on Retroviruses and Opportunistic Infections, 4-7 March 2018. Available at: http://www.croiwebcasts.org/console/player/37090?mediaType=slideVideo&&crd_fl=0&ssmsrq=1522772955419&ctms=5000&csmsrq=5001(accessed 7 March 2020).
  3. Smoking gun. Wikipedia, 5 March 2020, at: https://en.wikipedia.org/wiki/Smoking_gun
  4. ICF. South Africa Demographic and Health Survey 2016. Rockville (MD): ICF, 2019. Available at: https://dhsprogram.com/pubs/pdf/FR337/FR337.pdf (accessed 1 May 2020).
  5. Vandormael A, Akullian A, Siedner M, de Oliveira T, Bärnighausen T, Tanser F. Declines in HIV incidence among men and women in a South African population-based cohort. Nature Comm 2019; 10: 5482. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6889466/pdf/41467_2019_Article_13473.pdf (accessed 7 March 2020).
  6. de Oliveira D, Pybus OG, Rambaut A, et al. HIV-1 and HCV sequences from Libyan outbreak. Nature 2006; vol 444: pp 836-837.
  7. Black A, Bedford T. Roka/HIV/bayesian_timetree: evolutionary and epidemiological analysis of the Roka HIV outbreak. Bedford Lab. Available at: https://bedford.io/projects/roka/HIV/bayesian_timetree/(accessed 15 November 2018).
  8. Gisselquist D. Points to Consider: responses to HIV/AIDS in Africa, Asia, and the Caribbean. London: Adonis and Abbey, 2008. Available at: https://sites.google.com/site/davidgisselquist/pointstoconsider (acccessed 1 May 2020).
  9. Gisselquist D, Collery S. Bloodborne HIV: don’t get stuck. no date. Available at: https://bloodbornehiv.com/cases-unexpected-hiv-infections/ (accessed 7 March 2020).
  10. Akullian A Bershteyn A, Klein D, Vandormael A, Barnighausen T, Tanser F. Sexual partnership age pairings and risk of HIV acquisition in rural South Africa. AIDS 2017; 31: 1755-1764. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5508850/ (accessed 1 May 2020).
  11. Centers for Disease Control and Prevention (CDC) HIV risk reduction tool. Atlanta: CDC, no date. Available at: https://wwwn.cdc.gov/hivrisk/about_the_data.html (accessed 7 March 2020).
  12. Gisselquist D, Potterat JJ, Brody S, Vachon F. Let it be sexual: how health care transmission of AIDS in Africa was ignored. Int J STD AIDS 2003; 14: 148-161. Available at: http://www.cirp.org/library/disease/HIV/gisselquist1/gisselquist1.pdf (accessed 1 May 2020).
  13. Potterat JJ. Why Africa? the puzzle of intense HIV transmission in heterosexuals. In: Potterat J.J. Seeking the positives: a life spent on the cutting edge of public health. North Charleston (SC): Createspace, 2015. p. 175-229. Available at: https://www.researchgate.net/publication/311993589_Why_Africa_The_Puzzle_of_Intense_HIV_Transmission_in_Heterosexuals (accessed 1 May 2020).
  14. Fernando D. The AIDS pandemic: searching for a global response. J Assoc Nurses AIDS Care 2018; 29: 635-641. Abstract available at: https://www.sciencedirect.com/science/article/abs/pii/S105532901830133X?via%3Dihub (accessed 7 March 2020).

Will women who got HIV during the ECHO trial sue for damages?


The ECHO trial (Evidence for Contraceptive Options and HIV Outcomes) was both unethical and useless by design. The trial, reported June 2019, compared three birth control techniques: Depo-Provera (DMPA-IM) injections every three months, an IUD (intrauterine device), and levonorgestrel implants.[1]

  • Research to date has shown that Depo-Provera increases women’s risks to get HIV by 40%-50%.[2,3] By randomizing women to Depo-Provera, the trial violated articles 3, 4, and 9 of the World Medical Association’s Declaration of Helsinki on research ethics (eg, article 9: “It is the duty of physicians who are involved in medical research to protect the life [and] health…of research subjects).”[4]
  • Research to date has shown that birth control pills do not increase women’s risk for HIV.[2,3] By not including birth control pills among the contraceptive methods in the trial, the study violated article 33 of the Declaration of Helsinki (“The benefits, risks, burdens and effectiveness of a new intervention must be tested against those of the best proven intervention(s)…”).[4]

ECHO trial results have been widely misinterpreted. A report of the trial in The New York Times, for example, said the results show Depo-Provera “does not raise HIV risk.” Because the trial did not compare Depo-Provera to pills, it does not support that statement.[5]

The ECHO trial could have been both ethical and useful if it had compared birth control options for which there is limited evidence of their impact on women’s HIV risk (eg, IUDs, levonorgestrel implants, and monthly injections of norethisterone enanthate) to birth control pills, for which there is good evidence of little or no impact on women’s HIV risk.[2,3]

As it is, the trial suggests IUDs and levonorgestrel implants likely increase women’s risk for HIV less than does Depo-Provera, if at all. But how did women get HIV: from sex or skin-piercing health care procedures?[6] In countries where skin-piercing health care instruments are unreliably sterile, knowing how women got HIV is relevant for advising them about how to avoid HIV from health care, including skin-piercing birth control options.

Limited information on sexual risks for women in the trial suggests sex caused far less than half of new HIV infections during the trial. During quarterly follow-up visits, 49% of women reported more than 10 sex acts in the previous three months; to err on the high side, I assume all women averaged 15 sex acts per quarter or 60 per year. Fifty-five percent reported no condom use during their last sex act (see Table S11 in [1]). From this I estimate an average of 33 (= 55% x 60) unprotected sex acts per year for all women. I assume 25% of partners were HIV-positive. Using a transmission efficiency of 0.12 per 100 sex acts (from a study in Uganda[7]) I estimate women got HIV from sex at the rate of 1%/year (= 33 unprotected sex acts/year x 25% with an HIV-positive partner x 0.0012 transmissions per HIV-exposed sex act). This is far less than the observed 3.8%/year rate of new infections.[1]

Like many other studies in high-prevalence areas in Africa, the study withholds collected data relevant to assess sexual and non-sexual risks. Encouragingly, the study tested partners for HIV (pp 305-6 in [1]), following recent WHO advice.[8] But the study does not say how many partners tested HIV-positive or how much having an HIV-positive partner increased a woman’s HIV risk. The study does not report if women who got HIV during follow-up intervals reported any sex acts — with or without HIV-positive partners — during those intervals. This, too, violates the Declaration of Helsinki (article 36: “Researchers have a duty to make publicly available the results of their research on human subjects and are accountable for the completeness and accuracy of their reports…”).[4]

Aside from not reporting all relevant collected information, by all accounts the study did not collect other relevant information. Like most other foreign-funded HIV research in Africa, the study ignored non-sexual risks. not trace and test partners.

Unethical research funded from rich countries has harmed people in less developed countries for decades. The ECHO trial had no problem finding health care professionals willing to do the dirty work and no problem getting ethical approval: more than 750 people collaborated in ECHO research and 13 review boards approved it (supplementary appendix in [1]).

How to stop these outrages? Appealing to courts may get better results than waiting for health care professionals to change. Recently, a United States’ (US) court allowed Guatemalans harmed during medical research to sue private US institutions in US courts.[9] Does this mean that any woman in the ECHO trial randomized to Depo-Provera who got HIV during the trial could sue private US institutions involved in the trial in US courts?

References

1. Evidence for Contraceptive Options and HIV Outcomes (ECHO) Trial Consortium. HIV incidence among women using intramuscular depot medroxyprogesterone acetate, a copper intrauterine device, or a levonorgestrel implant for contraception: a randomised, multicentre, open-label trial. Lancet 2019; published online June 13. Available at: ht; tp://dx.doi.org/10.1016/S0140-6736(19)31288-7; supplementary appendix availabe at: http://echo-consortium.com/wp-content/uploads/2019/06/ECHO-primary-HIV-results-appendix-Lancet-online-first-June-2019.pdf (accessed 28 July 2019)

2. Morrison CS, Chen PL, Kwok C, et al. Hormonal contraception and the risk of HIV acquisition: an individual participant data meta-analysis. PLoS Med 2015; 12: e1001778. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4303292/ (accessed 26 July 2019).

3. Polis CB, Curtis KM, Hannaford PC, et al. An updated systematic review of epidemiological evidence on hormonal contraceptive methods and HIV acquisition in women. AIDS 2016; 30: 2665–83. Available at: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5106090/ (accessed 26 July 2019).

4. World Medical Association (WMA). Declaration of Helsinki – ethical principles for medical research involving human subjects. New York: WMA, 1964, revised 2013. Available at: https://www.wma.net/policies-post/wma-declaration-of-helsinki-ethical-principles-for-medical-research-involving-human-subjects/ (accessed 26 July 2019).

5. McNeil DG. Depo-Provera, an injectable contraceptive, does not raise HIV risk. New York Times 13 June 2019. Available at: https://www.nytimes.com/2019/06/13/health/depo-provera-hiv-africa.html (accessed 27 July 2019).

6. Gisselquist D. Advice to Young Women in Africa: Sex May Not Be Your Biggest Risk for HIV. SSRN, posted 1 May 2019. Available at SSRN: https://ssrn.com/abstract=3381252 (accessed 28 July 2019)

7. Wawer MJ, Gray RH, Sewankambo NK, et al. Rates of HIV-1 transmission per coital act, by stage of HIV-1 infection, in Rakai, Uganda. J Infect Dis 2005; 191: 1403-1409. Available at: https://academic.oup.com/jid/article/191/9/1403/860169 (accessed 26 July 2019).

8. WHO. Guidelines on self-testing and partner notification: supplement to consolidated guidelines on HIV testing services. Geneva: WHO, 2016. Available at: https://www.who.int/hiv/pub/vct/hiv-self-testing-guidelines/en/ (accessed 26 July 2019).

9. Stempel J. Johns Hopkins, Bristol-Myers to face $1 billion syphilis infections suit. Reuters 4 January 2019. Available at: https://www.reuters.com/article/us-maryland-lawsuit-infections/johns-hopkins-bristol-myers-must-face-1-billion-syphilis-infections-suit-idUSKCN1OY1N3 (accessed 26 July 2019).

 

 

Government of Pakistan protects patients. African governments don’t. Why not?


On 21 July 2019, at an international HIV/AIDS conference in Mexico, Farima Mir reported an ongoing investigation in Ratodero, Pakistan, that has found hundreds of children with HIV from healthcare[1]:

“At the end of April, 46 children in the city tested positive for HIV. And within 2 days, 14 more children were reported in nearby towns. The government mounted a response, screening around 32,000 people… Ultimately, over 770 of the 997 reported new infections were in young children, most from ages 2 to 5 years… Mir said that almost all children who tested positive for HIV had ‘repeated injections for any illness,’ meaning reused syringes were likely to blame.”

What happened in Pakistan echoes what has been found elsewhere, for example, Russia in 1988, Romania in 1989, Libya in 1998, etc (for more information about these and other HIV outbreaks from health care click on “outbreaks and unexpected infections” in the menu at the right of this page).

Almost surely there are many similar outbreaks of HIV from reused and unsterilized syringes, needles, razors, needles and tubes for infusions, and other health care instruments in African countries with the world’s worst HIV epidemics. But no government in sub-Saharan Africa has looked to find and stop HIV from unsafe health care! Whereas Government of Pakistan protects people by investigating unexpected HIV infections, governments of sub-Saharan Africa stick their heads in the sand. How many more people will get HIV from health care in Africa before governments investigate unexpected infections to find and stop the problem?

References

1. Walker M. ‘Man-Made Disasters’ Stymie Progress on Global HIV. Medpage Today 22 July 2019. Available at: https://www.medpagetoday.com/meetingcoverage/ias/81150 (accessed 23 July 2019).

Let’s stop HIV in Africa. What are you waiting for?


Question for African governments: Why haven’t you investigated unexplained HIV infections?

Question for CDC, UNAIDS, WHO: How can you say you want health care to be safe in Africa, but then NOT challenge governments to investigate unexplained infections?

Questions for people living in African: Do you know anyone who is HIV-positive who denies sexual risks? Do you believe them? Have you heard of a child with HIV but with an HIV-negative mother? If they got HIV from health care, you and your loved ones are also at risk. When are you going to ask your government to investigate unexplained infections to find and stop any hospital or clinic that has been infecting patients?

Question for researchers: Why haven’t you tried to find out how people got HIV: trace and test partners: ask where people got skin-piercing treatments?

Question for anyone: Why do you accept racist, sexual fantasies to explain Africa’s HIV epidemics? Yes, sex is a personal risk for HIV, but what is different in Africa that could explain Africa’s terrible HIV epidemics is not sexual behavior but unreliably sterile injections, infusions, and other health care procedures.

Hundreds of children in Pakistan infected by HIV from health care; government investigates to protect children


Beginning end-April 2019, government of Pakistan has been investigating an outbreak of HIV from unsafe health care in Ratodero county. As part of the investigation, government set up camps to test people for HIV. As of 23 May, tests on 20,800 people in Ratodero found >608 to be infected, including >500 children.[1] Almost all HIV-infected children had HIV-negative mothers. 

According to a recent report[2]: “Adviser to the Prime Minister for Health Dr. Zafar Mirza has said that outbreak of HIV in Ratodero has not only shaken the country but entire world adding when he was in Geneva he was also asked about surfacing of HIV… He said root cause of large number of children must be detected… He said federal government along with UNICEF, WHO, UNAID, Aga Khan, Aga Khan University Hospital and other organizations is cooperating with the Sindh government in this connection and they will continue to coordinate till root cause is detected, he added.”

In sub-Saharan Africa, children get HIV from unsafe healthcare, but no government has investigated to protect them

Lots of HIV-positive children with HIV-negative mothers are reported in Africa, but unlike Pakistan, no government has investigated. Nor have WHO or UNAIDS advocated any investigation. Here are some of the many reports of HIV-positive children in Africa with HIV-negative mothers:

* Mozambique, 2015: A random sample national survey found 30 HIV-positive children aged 6-23 months; 10 (33%) of the 30 children had mothers who were HIV-negative.[3]

* Uganda, 2011: A random sample national survey tested adults and children aged 0-5 years for HIV. Based on reports from this survey,[4] an estimated 17% (12 of 70) HIV positive children had mothers who tested HIV-negative (click on “outbreaks and unexpected infections” and then “Uganda” country page).

* Mozambique, 2009: A random sample national survey in 2009 tested children as well as adults for HIV. The study found 63 HIV-positive children aged 0-11 years old, of which 18 (29%) had mothers who tested HIV-negative.[5,6]

* Swaziland, 2006-7: A random sample national survey tested 1,665 mother-child pairs with children aged 2-12 years. Fifty children were infected; 11 (22%) of their mothers tested HIV-negative.[7,8]

WHO’s double standard

WHO’s double standard goes back decades. For example, during 1990-93, WHO’s Global Programme on AIDS coordinated studies in four African countries – Kigali, Rwanda; Kampala, Uganda; Dar es Salaam, Tanzania; and Lusaka, Zambia – to test inpatient children and their mothers for HIV infection. Combining data from the four cities, 61 (1.1 percent) of 5,593 children aged 6-59 months were HIV-positive with HIV-negative mothers.[9] Only three children had been transfused. Although these infections suggested a lot of HIV transmission through unsafe healthcare, WHO, incredibly concluded ‘the risk of…patient-to-patient transmission of HIV among children in health care settings is low.’[10]

At least WHO in 2019 is acting to protect children in Pakistan from getting HIV from unsafe healthcare. Will this ongoing investigation lead WHO to change its long-standing policy of neglect in Africa?

References

1. Masood T. Situationer: dealing with HIV outbreak among children. Dawn 23 May 2019. Available at: https://www.dawn.com/news/1483999 (accessed 24 May 2019).

2. Dawoodpoto J. “HIV in Ratodero has not only shaken the country but entire world.“ Daily Times 24 May 2019. Available at: https://dailytimes.com.pk/399789/hiv-in-ratodero-has-not-only-shaken-the-country-but-entire-world/ (accessed 24 May 2019).

3. page 231 in: Ministério da Saúde (MISAU), Instituto Nacional de Estatística (INE), e ICF, 2015. Inquérito de Indicadores de Imunização, Malária e HIV/SIDA em Moçambique 2015. Rockville, Maryland: ICF, 2018. Available at: https://dhsprogram.com/pubs/pdf/AIS12/AIS12.pdf

4. Table 8.13 in: Uganda Ministry of Health, and ICF International. Uganda AIDS Indicator Survey (UAIS) 2011. Calverton: ICF International, 2012. Available at: https://dhsprogram.com/publications/publication-AIS10-AIS-Final-Reports.cfm(accessed 6 December 2018).

5. pp. 177-181 in: INS, INE, and ICF Macro. Inquérito Nacional de Prevalência, Riscos Comportamentais e Informação sobre o HIV e SIDA em Moçambique 2009. Calverton, Maryland: ICF Macro, 2010. Available at: http://measuredhs.com/pubs/pdf/AIS8/AIS8.pdf (accessed 19 January 2012).

6. Brewer D. Scarification and male circumcision associated with HIV infection in Mozambican children and youth. Webmedcentral 2011, Article ID WMC002206. Available at: http://www.webmedcentral.com/article_view/2206(accessed 19 January 2012).

7. CSO, eSwatini, and Macro Int. Swaziland Demographic and Health Survey 2006-07. Mbabane, Swaziland: CSO and Macro International, 2008. Available at:  https://dhsprogram.com/pubs/pdf/FR202/FR202.pdf (accessed 8 November 2018).

8. Okinyi M, Brewer DD, Potterat JJ. Horizontally acquired HIV infection in Kenyan and Swazi children. Int J STD AIDS 2009; 20: 852-857. Abstract available at http://www.ncbi.nlm.nih.gov/pubmed/19948900(accessed 27 October 2018); article available at: http://www.interscientific.net/IJSA2009Okinyi.html (accessed 15 October 2018).

9. Hitimana D, Luo-Mutti C, Madraa B, et al. ‘A multicentre matched case control study of possible nosocomial HIV-1 transmission in infants and children in developing countries’, 9thInt Conf AIDS, Berlin 6-11 June 1993. Abstract no. WS-C13-2.

10. Global Programme on AIDS. 1992-1993 Progress Report, Global Programme on AIDS. Geneva: WHO, 1993. p. 85.