South Africa, where doctors achieved the first human heart transplant and one of the wealthiest countries in Africa, has a terrible HIV epidemic. In 2015, an estimated 30.8% of pregnant women were HIV-positive at their first antenatal visit, with more pregnant women infected in parts of the country: for example, 44.5% in KwaZulu-Natal province and 48.4% in Zululand district of that province. Even more adults were infected in some age cohorts and regions: for example, in a 2014 survey of a study population in uMungundlovu district, KwaZulu-Natal, more than 66% of women aged 30-39 years were HIV-positive as were 59.6% of men aged 40-44 years. Although South Africa has only 0.75% of the world’s population, a 2017 national survey estimated 7.9 million South Africans infected, more than a fifth of the world’s total HIV infections.
The South African government is doing a lot of what is required to respond to this epidemic with one glaring exception: the government has not investigated any unexpected and unexplained infections (i.e., not from sex, mother-to-child, or injection drug use) to find and stop blood-borne HIV transmission during health care and cosmetic services.
Doing things right: 90-90-90
In 2014, UNAIDS launched the 90-90-90 initiative, setting targets for testing and treatment to be achieved by 2020: 90% of people with HIV know they are infected, 90% who know are on antiretroviral therapy (ART), and 90% on ART have suppressed viral loads.
Government of South Africa has made encouraging progress towards 90-90-90 targets. In a 2017 national survey, 84.9% of HIV-positive adults aged 15-64 years knew they were infected, 70.6% of those who knew were on ART, and 89.5% of people taking ART were virally suppressed. Putting these numbers together, 54% of HIV-positive adults were virally suppressed (54% = 84.9% x 70.6% x 89.5%). The 90-90-90 targets are intended not only to reduce AIDS sickness and deaths but also to reduce HIV transmission. People with suppressed viral loads are not likely to transmit sexually because they have so little virus in semen or vaginal fluids.
Government of South Africa has also done well with prevention of mother-to-child transmission. As of 2017, more than 95% of pregnant women were tested for HIV and those found infected were given ART both to protect them and to prevent HIV transmission to their babies. In 2016-17, less than 1% of HIV-positive mothers transmitted HIV to their babies before and during birth.
Even before the 90-90-90 initiative, government of South Africa in 2010 began an HIV testing campaign, testing 13.3 million people over 18 months, finding 2 million with HIV, and putting 400,000 on treatment. Also in 2010, government told providers to offer an HIV test to anyone seeking health care at a public facility. To make testing easier, government in 2016 approved sale of self-testing kits through private pharmacies and other outlets. These policies and programs support efforts to reach the testing target for 2020 – that 90% of people who are infected know it. More testing contributes to prevention by making it easier for people to know if their (potential) sex partner is HIV-positive, so they know to use condoms or otherwise protect themselves.
Doing things wrong: not investigating unexpected infections
With more testing, treatment, and other factors, the annual number of new HIV infections in South Africa fell 40% from 386,000 in 2010 to 231,000 in 2017. Even so, South Africa’s HIV/AIDS disaster is reaching the next generation: in 2017 young women aged 15-24 years were getting HIV at the rate of 1.5% per year.
The terrible scale of South Africa’s HIV epidemic is due in part to government not doing what it could to protect people. Over the years, public media and medical journals have recognized and reported unexpected HIV infections in South Africa. Nevertheless, as of early 2019, government has not investigated any unexpected infection by identifying suspected source facilities and then tracing and testing others treated at those facilities. For example, beginning in 1999, a group of doctors in Cape Town from time to time asked about and identified possible health care risks for more than 20 HIV-positive children with HIV-negative mothers.[11,12] But government did not subsequently trace and test others treated at suspected source facilities. Without tracing and testing to find others infected at the same facilities it is not possible to determine the extent of any outbreak or to find and fix the specific lapses in standard precautions responsible; and the public remains at risk.
Government of South Africa’s response to unexpected infections contrasts sharply with responses by governments outside sub-Saharan Africa. For example, in 1988 doctors in Elista, Russia (part of the USSR at the time), found and reported unexpected HIV infections in a hospitalized baby with an HIV-negative mother and a blood donor with no sexual risk. Government investigated, testing thousands, tracing transmission from one child directly and indirectly to 265 children in 13 hospitals, and ending the outbreak by August 1989.[13,14] From 1989 through 2014, nine other governments (Cambodia, China, India, Kazakhstan, Kyrgyzstan, Libya, Mexico, Romania, and Uzbekistan) investigated unexpected infections to uncover nosocomial (through health care) HIV outbreaks with more than 100 to more than 55,000 infections [15-17]). Many other governments have investigated unexpected infections to find smaller outbreaks.
A lot of evidence suggests HIV transmission through skin-piercing procedures in health care, and possibly also during cosmetic services, have been and remain common in South Africa. Following paragraphs summarize selected evidence from later to earlier reports.
Incidence in children aged 2-14 years: The fifth South African National HIV Prevalence, Incidence, Behavior and Communication Survey, 2017, reported children aged 2-14 years acquired new HIV infections at the rate of 0.13% per year.
Higher HIV prevalence in Black Africans than in other groups: The same 2017 national survey reported much higher HIV prevalence in Black Africans of all ages (16.6%) than in Whites (1.1%), Coloured (5.3%), or Indian/Asians (0.8%). The survey gives no explanation for these differences in terms of sexual behavior. Male circumcision is not a factor: as of 2012, it was more common among Black African adults (52.4%) compared to Whites (23.3%), Coloured (26.4%), or Indian/Asians (33.5%). There is, however, a big difference in where people get health care: in the second national HIV survey in 2005, 80% of Whites reported they usually get health care from private providers, while 80% of Black Africans reported they got most health care from public services.
Unexplained infections in high school women: A 2011-2017 study in Mpumalanga province tested 2,533 high school women aged 13-20 years; 81 were HIV-positive, including 38 who reported never having vaginal or anal sex. The study then followed and retested the women for 1-6 years during which 190 got HIV, including 44 who reported no lifetime sex. At annual surveys during the first three years of follow-up an average of only 9% of women reported any sex without a condom in the previous three months; and from what women reported about partners’ ages (less than 9% were aged over 24 years) less than 10% were HIV-positive.[22,23] Even if all women reporting unprotected sex in the previous three months had unprotected sex 104 times per year (or twice per week; an intended overestimate, considering most were in school), one could expect to see only 0.1% of women get HIV from sex each year, far less than observed incidence of 1.8% per year (0.1% = 9% of women reporting unprotected sex in the previous three months x 104 sex acts per year x 10% of partners are HIV-positive x transmission efficiency of 1 per 1,000 coital acts; the next paragraph references this estimated transmission efficiency)
(This paper estimates transmission efficiencies of HIV through unprotected vaginal sex at 1 per 1,000 coital acts or 10% per year from an infected spouse based on the following references. The United States Centers for Disease Control and Prevention estimates transmission per unprotected coital act at 0.8 per 1,000 from men to women and 0.4 per 1,000 from women to men. A widely cited estimate from a study in Uganda is 1.2 per 1,000 coital acts (with some condom use, which had no impact on estimated transmission efficiency). Six studies in Africa followed discordant couples in which most partners were not aware of their infections or risks and/or did not use condoms; from these six studies both the mean and average rates of HIV incidence in initially HIV-negative partners were less than 10% per year.[26-31] Here and elsewhere I report rates of HIV incidence as percentages per year, a statistic more familiar for non-technical readers than the technical term, infections per 100 person-years.)
HIV-positive virgin men and women: In a 2014-15 survey among adults aged 15-49 years in uMgungundlovu district, KwaZulu-Natal, 11.2% of (self-reported) virgin women were HIV-positive as were 9.0% of virgin men.
Higher incidence in young women than can be explained by sex: Repeated surveys of a study population in mKhanyakude district, KwaZulu-Natal, reported young women aged 15-24 years acquired new HIV infections at the rate of 5.9% per year (486 infections in 8,211 person-years) during 2011-15. Such high incidence is difficult to reconcile with women’s limited sexual exposures to HIV, suggesting most infections come from risks other than sex. In the 2015 survey, 34% (847/2,467) of young women reported at least one coital act without condoms in the previous year, and HIV prevalence was 10% among men who reported sex with a young woman in the past year. Assuming women who reported unprotected sex in the past year averaged 104 unprotected coital acts per year (an intended over-estimate) and a transmission efficiency of 1 per 1,000 coital acts, sex explains incidence of only 0.4% per year, far less than the observed rate of 5.9% per year (0.4% = 34% of women with any unprotected sex in the past year x 104 coital acts per year x 10% of partners were HIV-positive x 0.001 transmissions per unprotected coital act[24,25]).
Cluster of 63 recent and linked infections: The African Health Research Institute found a cluster of 63 very similar HIV (similar sequences of amino acids) in blood collected during 2011-14 from 1,376 adults in a study population in uMkhanyakude district, KwaZulu-Natal. The Institute estimated HIV from one (unidentified) person in mid-2013 was somehow transmitted directly and indirectly over 18 months to 63 men and women. Such fast transmission does not seem possible through sex, with transmission through vaginal sex requiring on average circa 1,000 coital acts; even for receptive anal sex an estimated average of 70 events are required for each transmission. However, such rapid transmission is seen in nosocomial outbreaks; compare, for example, the phylogenetic tree of HIV genetic sequences from an outbreak in Cambodia with the cluster of 63 HIV sequences from KwaZulu-Natal (slide 10 in ).
Unexplained infections in pregnant women: Four studies reported numbers of new HIV infections and rates of HIV incidence ranging from 10.7%-11.2% per year (or data to calculate these statistics) in pregnant women during 2002-12. Women would not get HIV through sex at such rates unless all or almost all of their partners were infected. But during those years, less than 15% of adult men in South Africa were HIV-positive; and many HIV-positive married men were married to women who were already infected. The four studies are as follows: Wand and colleagues followed pregnant women in Durban during 2002-5, reporting data to calculate 81 incident infections in pregnant women and incidence of 10% per year; Moodley and colleagues followed pregnant women in Mpumulanga, Eastern Cape, and Free State during 2006-7, observing 72 incident infections and incidence of 10.7% per year; Kharsany and colleagues followed pregnant women in KwaZulu-Natal during 2007-8, observing four incident infections and calculating incidence of 11.2% per year; and Dinh and colleagues reported 212 incident infections in a national sample of pregnant women and data to calculate incidence at 11% per year.
HIV in high school virgin boys and girls: A 2012 survey of students in grades 8-12, averaging 15.8 years old, in KwaZulu-Natal reported 21 (55%) of 38 HIV-positive boys said they were virgins as did 56 (54%) of HIV-positive girls.
HIV incidence in adults with no reported sex risks: The South Africa HIV Prevalence, Incidence, Behaviour and Communication Survey, 2005 (the second such national survey) reported HIV incidence of 1.5% per year in self-reported virgin adults, 2.4% per year in non-virgin adults who reported no sex in the previous year, and a similar 2.4% per year in adults who said they had been sexually active in the previous year.
South Africa’s early epidemic doubles in 9-14 months: At the beginning of the HIV epidemic among Black South Africans in the late 1980s, the number of HIV-positive people doubled in about nine months. During 1990-94, the doubling time for HIV prevalence in pregnant women throughout South Africa averaged 14 months (from 0.7% in 1990 to 7.6% in 1994). The speed of transmission required for such rapid epidemic expansion is much faster can be explained by estimated rates of sexual transmission (1 per 1,000 coital acts or 10% per year between discordant couples[24-31]).
Fixing South Africa’s incomplete HIV prevention program: investigating unexplained infections
South Africa’s promotion of testing and treatment to reach 90-90-90 targets can be expected to slash sexual transmission. As targets are reached, more than 70% (~90% x 90% x 90%) of those infected will have suppressed viral loads and very little risk to transmit to a sexual partner. And with more testing, more people will know if partners are infected, so they will know to be careful.
But 90-90-90 may have less limited impact on blood-borne transmission. Based on outbreak investigations in other countries, blood-borne infections are often found in bunches. For example, HIV went from one in-patient baby to 265 children in 16 months in Russia, from one to 418 infections in 3-4 years in Libya, and from two to more than 200 infections in several years in Cambodia. Large outbreaks characteristically come from facilities giving repeat treatments, where some people infected earlier get another procedure within weeks to month when they have primary infections and high viral loads, making their blood more dangerous and contributing to later transmissions.
The frequent bunching of blood-borne infections from specific facilities means that any identified unexpected HIV infection should be considered – until proven otherwise – to be one of many in an outbreak. When onward transmission occurs within several months, routine testing is not likely to find people with new blood-borne infections before they infect others through the outbreak. Moreover, even if someone tests HIV-positive with a very early infection, if the only risk anyone thinks about is sex, knowing he or she is infected would have no impact on their getting more skin-piercing procedures at the facility that is the source of the outbreak.
Educating health care workers – a continuing effort – has not stopped unexpected infections. Without outbreak investigations, no one knows the specific skin-piercing procedures and facilities responsible for unexpected infections, so there is no way to know where and how to focus efforts to repair dangerous procedures. Investigations in other countries have implicated a long list of health care procedures, including intra-muscular and intravenous injections, flushing intravenous lines, taking medicine from multi-dose vials, dental care, blood tests, blood and plasma donation, and others. Skin-piercing cosmetic procedures, such as tattooing, shaving, and manicures may also be involved.
Getting from no to yes: Officials in the government of South Africa have for decades consistently decided not to investigate unexpected infections. Increasing public awareness of unexpected infections could create public pressure for investigations. Libya and Cambodia provide examples of public pressure successfully pushing governments to investigate.
- In Libya in August 1998, a magazine reported HIV infections in children traced to the El Fatah Hospital, Benghazi. The government’s initial response was to close the magazine. But parents did not take “no” for an answer. In November 1998 “a group of desperate fathers interrupted a medical conference Ghadafi was attending in Benghazi and appealed to him for help.” Gaddafi ordered treatment for infected children and an investigation that offered HIV tests to all children treated at El Fatah Hospital in the previous year. The investigation found 418 children with HIV from healthcare.
- In Roka, Cambodia, in November 2014, a 74-year-old man tested HIV-positive. Surprised, he sent his son-in-law and granddaughter for tests; both were infected. More villagers, alerted and worried, went for tests; many found they were infected. Acting on this information, government began an investigation in mid-December. The investigation reported 242 infections, attributing most if not all to skin-piercing procedures from a local private health care provider.[48,49]
With South Africa pursuing 90-90-90 targets, more people are getting tested. In the 2017 national HIV survey, 75.2% said they had ever been tested for HIV, and 66.8% had been tested within the past 12 months. For many South Africans, an HIV-positive test comes as a surprise. In the previous 2012 survey 80% of adults considered themselves at low risk for HIV, giving reasons such as: “I use condoms”; “I abstain from sex”; “I am faithful to my partner.” But many self-assessed low risk adults were infected, accounting for 56% of adult HIV infections (calculated from data in Table 3.56 in ). As testing expands, more people are finding themselves with unexpected infections.
What happens next may well depend on whether people who have unexpected infections are able to get a respectful hearing from counselors, the media, churches, lawyers, support groups, non-government organizations, etc. To date, too few of those who manage or participate in public dialogue about HIV have been willing to believe people who report unexpected infections and to push government to mount the proper response to protect public health, i.e., to investigate, to look for outbreaks.
Making investigations work for public health: From a public health point of view, the priority for investigations is to determine the extent of the problem (to find all who were infected in each investigated outbreak) and to identify specific procedural lapses and facilities responsible. What might be ideal under such circumstances is for government to legislate to allow no-fault investigations along the lines of the post-apartheid Truth and Reconciliation Commission.
Attempting to punish or to collect compensation can create situations of conflict in which people who know what happened are motivated not to tell, investigators are pressured not to look, and blame and punishment fall on scapegoats. Open and thorough investigations educate and alert everyone – health care staff, cosmetic service providers, and the public – to be more aware of blood-borne risks. Punishing past mistakes is not necessary to improve health care safety; many health care staff will no doubt be mortified to learn that what they thought was safe may have infected patients. As for compensation, considering decades of inaction and inattention, it is not easy to identify anyone other than the government which both shares responsibility and has resources commensurate with whatever the problem might be. In any case, those who have been harmed already have free treatment.
Public trust in healthcare safety: Although officials have not explained why they have not investigated unexpected HIV infections, one reason may have been to maintain public trust in health care safety. Outbreak investigations that ask former patients at specific facilities to come for HIV tests challenge that trust by making the public aware of possible mistakes. But that is only a short term view of the matter. Acknowledging, investigating, and fixing problems builds trust in the long term.
No one has identified differences in sexual behavior that could explain much higher HIV prevalence in South Africa than in all non-African countries as well as in all but a few regional countries in Africa. One possible explanation is that lapses in health care safety have been driving South Africa’s epidemic. If that is so, then investigations of unexpected infections could lead to a dramatic drop in HIV transmission.
But even if blood-borne risks make only a limited contribution to South Africa’s epidemic, investigations protect public health. According to the World Medical Association’s Declaration of Lisbon on the Rights of the Patient, health care managers and providers have a responsibility to give patients “medical care of good quality” and “health education that will assist him/her in making informed choices about personal health and about the available health services.” Without outbreak investigations, this is not possible.
Similarly, even if blood-borne risks make only a limited contribution to South Africa’s epidemic, investigations that recognize blood-borne transmission at any level undermine the stigmatizing belief that an HIV infection is a sign of sexual behavior.
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