Chapter 9


Failing to provide safe healthcare, 1989-2009

 

Healthcare involves two parties: those who provide it, and those who receive it. When healthcare is unsafe, both parties have failed. Providers have failed to ‘first do no harm.’ The public – together with government and civil society organizations – have failed to demand safe care. This chapter discusses the providers’ failure, and the next chapter discusses how the public can demand safe care.

 

Different responses to unexplained HIV infections 

 

Investigations in Russia and Romania, 1988-92        

 

In late 1988, doctors in Elista, Russia, found an HIV-positive child with an HIV-negative mother. Suspecting that the child might have acquired HIV infection as an inpatient at a local hospital in mid-1988, the Ministry of Health tested other children who had been inpatients at the same time. When these tests found more HIV-positive children, the Ministry traced where and when they might have been infected during earlier treatment (see references in Table 9.1). In this way, investigators found the source of the outbreak in a child who had been hospitalized in early 1988. The child’s father had received a blood transfusion in Brazzaville, Congo, in 1981, and had subsequently infected the mother, who infected the child.

Extending the investigation to other hospitals, the Ministry of Health found that from May 1988 through August 1989, 13 hospitals in Elista and elsewhere in the region had spread HIV from that one child to more than 260 children. HIV appears to have passed from child to child through intravenous catheters, intramuscular injections, and possibly other equipment and procedures. In addition, 22 mothers acquired HIV from their children, most likely through breastfeeding.

In June 1989, about the time that Russia’s Ministry of Health stopped the Elista outbreak, doctors in Bucharest, Romania, unexpectedly found HIV in a hospitalized girl. Testing more inpatient children in the same hospital, doctors found that 12 of 30 were infected. Concerned doctors extended testing to other hospitals, finding more infections. Through mid-1991, tests on more than 29,000 people found almost 1,500 to be infected, 93 percent of whom were children aged 0-3 years (Table 9.1). A small minority of their mothers were HIV-positive (likely infected through breastfeeding). Transmission continued into the early 1990s, infecting more than 10,000 children before hospitals and orphanages implemented adequate infection control. One plausible theory to explain the coincident outbreaks in children throughout Romania in the late 1980s is that a locally produced, HIV-contaminated blood product (gamma globulin) infected children in multiple districts, after which HIV spread from child to child through unsterile injections.

 

Not investigating unexplained HIV infections in Africa, 1984-93      

 

While Russian and Romanian doctors and governments responded to unexplained HIV infections with alarm and investigations, doctors and governments in Africa did not investigate HIV infections in children with HIV-negative mothers. For example, at a hospital in Kigali, Rwanda, during 1984-90, Commenges and colleagues found 54 children with AIDS and HIV-negative mothers. They reported that 22 of the children had been transfused, but they did not report other healthcare risks, and they did not investigate cases by testing other children who had received healthcare at the same clinics and hospitals. Moreover, they showed declining interest to find more unexplained cases: ‘The proportion of children [with AIDS] whose mother’s serological [HIV] status was investigated decreased over time during the study period.’[i]

Around 1990, WHO’s Global Programme on AIDS coordinated studies in the major cities of 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, WHO reported that 61 (1.1 percent) of 5,593 children aged 6-59 months were HIV-positive with HIV-negative mothers.[ii] Only three children had been transfused. WHO’s report presented no evidence that infections had come from risks other than blood exposures (such as child sexual abuse, breastfeeding by someone other than the mother, etc.). Incredibly, WHO concluded that ‘the risk of…patient-to-patient transmission of HIV among children in health care settings is low.’[iii] A similar conclusion would have been unacceptable for WHO as well as for national ministries of health if 1 percent of inpatient children had been found with unexplained HIV infections in almost any country outside Africa.

There is no indication that any of the four governments investigated any of these 61 infections, tracing where children had received medical treatment and testing other children attending those facilities. Neither WHO nor any of the research teams from the four countries has said how many of the 61 unexplained infections were found in each country – information which could have helped people to see and to reduce their risks for HIV infection.

 

Outbreak investigations continue in countries with concentrated epidemics  

 

The point-counterpoint of investigations in countries with concentrated epidemics but not in countries with generalized epidemics continued into 2009. Some investigations in countries with concentrated epidemics point to risks that may be common in generalized epidemics.

For example, in early 1993, a doctor in New South Wales, Australia, reported to the state government that one of his patients had an unexplained HIV infection, which the doctor suspected had come from invasive procedures at another clinic. The government responded with an investigation, tracing and testing other patients who had visited the suspected clinic on the same day as the patient who triggered the investigation. This investigation found four other patients who were HIV-positive. Four of the five HIV-positive patients had no risk factor other than visiting the clinic. The fifth, an MSM, appears to have been the source of the HIV that infected the others. One hypothesis is that HIV from the source patient got into a multidose vial of local anesthetic, from which it was able to reach and infect the other patients.[iv] Multidose vials of local anesthetic can be especially dangerous because doctors sometimes re-inject patients who continue to feel pain. If a doctor reuses the same syringe (even with a new needle) to withdraw anesthetic more than once for one patient, this could transfer trace amounts of blood – and pathogens – from the patient to the vial.

The largest documented iatrogenic outbreak occurred in China. Companies buying blood plasma from poor people in rural areas during 1990-95 transmitted HIV to as many as 100,000 or more paid donors (see references in Table 9.1).

 

Table 9.1: Documented outbreaks of HIV infection from medical procedures*

Country, year of outbreak

Who was infected

Number of cases identified

Search to find all cases?

Mexico, circa 1986[v]

Blood and plasma sellers

281

No

Russia, Elista, 1988-89[vi]

Inpatient children 

>260

Yes

Romania, circa 1988-1992[vii]

Children

~10,000

No

India, Pune, circa 1988[viii]

Blood and plasma sellers

97

No

India, Mumbai, circa 1988[ix]

Blood and plasma sellers

~172

No

Egypt, 1991 and before[x]

Dialysis patients 

82

Yes

Argentina, 1990[xi]

Dialysis patients

33

Yes

Columbia, 1992-93[xii]

Dialysis patients 

13

Yes

Argentina, 1993[xiii]

Dialysis patients

20

Yes

Egypt, 1993[xiv]

Dialysis patients

64

Yes

China, 1990-95[xv]

Blood and plasma sellers

~100,000

No

Libya, 1997-99[xvi]

Inpatient and outpatient children 

>400

Yes

Kazakhstan, 2006[xvii]

Children

>140

Yes

Kyrgyzstan, 2007[xviii]

Children

>70

Yes

* Outbreaks with 10 or more infections, except outbreaks in which most infections come from receipt of blood or blood products.

 

In 1998, doctors at a hospital in Benghazi, Libya, discovered HIV-positive children with HIV-negative mothers (see references in Table 9.1). To investigate this outbreak, the government offered HIV tests to children who had been treated at the hospital during 1997-98. The investigation identified more than 400 HIV-positive children. Sequencing of HIV from a large sub-sample of these children found that the infections were related, and that the outbreak likely began from one infection around 1995. Apparently, injections and other invasive procedures passed HIV from child-to-child. As many as 19 mothers appear to have contracted HIV from their children, possibly through breastfeeding.

Very likely many healthcare workers contributed to the outbreak, infecting children through ignorance and carelessness, but with no intention to harm. Unfortunately, the government’s investigation went off track to accuse seven foreign healthcare workers – six Bulgarians and a Palestinian – with deliberately infecting the children. Most of the accused did not begin to work at the hospital until years after the outbreak began. Nevertheless, a Libyan court convicted six of the seven for murder, and sentenced them to death. In July 2007, the Libyan government commuted their sentences to life in prison, and transferred them as prisoners to Bulgaria, where the government immediately freed them. They had spent more than eight years in prison.

In July 2006, doctors in southern Kazakhstan discovered children with unexplained HIV infections. This discovery led to an investigation that tested more than 10,000 children and discovered more than 140 infected children. More than 10 mothers appear to have been infected through breastfeeding. The investigation led to criminal convictions for 21 doctors and officials for actions that contributed to unsafe healthcare.

 

Lack of investigations continues in Africa and India 

 

Through early 2009, journals, newspapers, and other publications have reported hundreds of children in Africa[xix] and at least 30 in India[xx] with unexplained or nosocomial HIV infections (excluding infections from transfusion of blood or blood products). Such public reports document only a small portion of the unexplained infections that have been recognized. In any city with a generalized epidemic, one can usually find one or more cases by asking around among doctors at major hospitals and counselors at HIV testing centers. In countries with generalized epidemics, no government investigated any unexplained infections in children by testing other children attending suspected facilities.

An incomplete investigation in Mumbai, India, in 1997 illustrates dangers to the public when governments do not investigate unexplained infections. In 1996, a Mumbai nursery arranged HIV tests for infants intended for adoption by Danish families. All children tested HIV-negative. In 1997, one child was tested again because of illness – and was found to be HIV-positive. Subsequent testing of all children in the nursery (the report does not say how many) found seven more who were HIV-positive. Sequencing of HIV from six of the eight HIV-positive children found that the viruses were similar, so that the infections were linked. All eight children had received treatment at a Mumbai nursing home in October 1996. Several had received blood or blood products. For five children, the only reported risks were ‘intravenous antibiotic treatment and routine immunization.’[xxi]

A visiting Danish team managed the investigation. A copy of their unpublished report is on file in the office of the Safe Injection Global Network (SIGN) at WHO in Geneva. There is no indication that any government agency extended the investigation to other children who had been treated in the implicated nursing home during 1996, and there is no indication that anyone warned anyone or changed any procedures to protect other children. In 2005, during a visit to Mumbai, I met with government officials and doctors involved in AIDS prevention and in hospital infection control. No one I talked with had heard of the incident or of the Danish investigation.

In 2000, a team at Stellenbosch University in South Africa established a registry of unusual HIV infections among children.[xxii] Through early 2004, they recorded 16 HIV-positive children with HIV-negative mothers. Two had possible sexual exposures, and one appears to have been infected by close contact with a sibling. All the other 13 had been inpatients prior to their HIV diagnosis.[xxiii] Although the team identified the hospitals where the children might have been infected, the government did not investigate by testing other children who had attended those hospitals. After the Stellenbosch team reported these infections in the South African Medical Journal, a subsequent editorial in the Journal urged that ‘scarce resources should not be devoted to research into the extent of nosocomial transmission of HIV-1.’[xxiv]

A 2004-05 national survey in Uganda tested more than 8,000 children aged 0 to 5 years, and was able to test most of their mothers as well. Approximately 15 percent of the mothers of HIV-positive children tested HIV-negative.[xxv]

Aside from children, studies and surveys have reported hundreds of adults with unexplained infections (see Chapter 7). These reports are routinely discounted with the suspicion that the men and women had lied about their sexual activities. As has happened with children, no African government has investigated any unexplained HIV infection in adults.

 

AIDS prevention programs pay little attention to healthcare risks        

 

In the late 1980s, WHO’s Global Programme on AIDS shifted attention and money away from patient safety in countries with generalized epidemics (Chapter 5). Officials in WHO accomplished and sustained this shift even though they were aware of widespread and persistent infection control lapses in Africa. In 1991, for example, senior officials in WHO’s Global Programm on AIDS noted that in Africa:[xxvi]

 

…it has been difficult to ensure proper sterilization procedures because of low equipment-to-patient ratios which make sterilization of equipment between use difficult; lack of sterilization equipment and protective clothing, and irregular power supplies.…[A]lthough as few as 60% of needles and 21% of syringes are sterilized in some immunization programmes, these percentages can be increased to over 95% when health staff are retrained and supervision is ensured.

 

In 1993, the Programme’s proposed budgets for HIV prevention in developing countries included only 4-7 percent for blood safety and nothing for infection control.[xxvii] Similarly, the Global Programme did not mention infection control in its own proposed budget for 1994-95.[xxviii]

From end-1995, WHO’s Global Programme on AIDS dissolved, passing its work to UNAIDS (the Joint United Nations Programme on HIV/AIDS). UNAIDS is not part of WHO, but is rather a new organization that as of 2006 reported to 10 UN agencies, including WHO, World Bank, UNICEF, and others. UNAIDS was positioned to deal with the AIDS epidemic as an economic and social issue, going beyond the mandates of ministries of health.[xxix] In this way, the formation of UNAIDS further weakened attention to infection control.

During the 1990s through 2009, international and foreign-supported AIDS programs paid almost no attention to standard precautions to prevent patient-to-patient transmission of HIV (the one major exception, from 2004, was US aid for injection safety, discussed later in this chapter). However, AIDS programs during this period paid modest – but insufficient – attention to occupational risks for healthcare workers and to blood transfusions.

 

Not protecting healthcare workers       

 

In the US and in other developed countries, governments in the early 1980s tightened rules and recommendations for healthcare workers to wear gloves and other protective gear and to avoid blood exposures (see Chapter 4). From the late 1980s, hospitals in developed countries began to offer short-term treatment with zidovudine, an antiretroviral drug, to healthcare workers after needlestick accidents. Such treatment – known as post-exposure prophylaxis (PEP) – provides partial protection against HIV infection. Post-exposure prophylaxis became standard in the mid-1990s in rich countries with concentrated epidemics.

AIDS programs in countries with generalized epidemics have allocated funds to protect healthcare workers. However, it has not been enough. Gloves and other protective gear have often been in short supply. Post-exposure prophylaxis was rarely available before 2000, and as of 2009 is still not generally available. In Tanzania, for example, a 2007 survey found that only 4 percent of healthcare facilities offered post-exposure prophylaxis for their workers.[xxx] In India, post-exposure prophylaxis is available for government health staff, but not for most private healthcare workers.

In countries with generalized epidemics, HIV infections from occupational blood exposures have only rarely been documented. A worldwide compilation of reported HIV infections among healthcare workers from occupational exposures through 1997 found 94 cases, of which only 4 came from Africa.[xxxi] This is an absurdly low figure, considering that 70 percent of HIV infections have been in Africa, where healthcare workers have much less protective gear than in developed countries.[xxxii] In 2003, a WHO team used information on numbers of needlestick accidents and HIV infections among patients to estimate that occupational exposures infect 1,000 healthcare workers with HIV per year, including more than 800 in Africa and Asia.[xxxiii] Continuing high risk for healthcare workers undermines health systems and programs.

 

Holding back on blood safety   

 

In 1988, WHO’s Global Programme on AIDS and the League of Red Cross and Red Crescent Societies established the Global Blood Safety Initiative. In early 1989, after consultations with countries and organizations, the Initiative proposed minimum targets and essential consumables and equipment for blood transfusion services.[xxxiv] These proposals fell on deaf ears. A 1989 editorial in the Lancet criticized that governments ‘have often found it easier to funnel resources into cleaning up the blood supply than into interventions directed at high-risk groups.’[xxxv] In 1991, senior officials in WHO’s Global Programme on AIDS recommended that countries should not put too much money into blood safety, so that ‘funds are not diverted from higher priority strategies for prevention of HIV sexual transmission.’[xxxvi]

Lack of money and support for blood safety has meant that doctors in much of Africa continued to transfuse untested blood. In 1989, for example, a doctor in Burkina Faso wrote to a major medical journal[xxxvii]:

 

The rainy season is just starting and shortly the wards will be inundated with patients, especially pregnant women and young children, suffering from severe anaemia induced by malaria on top of chronic nutritional anaemias. We have no means of screening blood before transfusion

We wait for the national anti-AIDS programme to reach our hospital. Meanwhile we work in the dark against a largely unknown enemy, our patients at risk and the AIDS epidemic unchecked.

 

A 1990 study in Kinshasa found that at least 28 percent of recently transfused blood had not been tested for HIV, the supply of test kits was irregular, many healthcare facilities did not have sterilized instruments on hand, and supposedly sterile instruments were contaminated.[xxxviii] A comment on this paper in WHO’s AIDS Technical Bulletin called the findings ‘a horrifying indictment…of the international response to the African AIDS epidemic.’[xxxix]

Even in countries with some of the best blood banking systems in Africa, quality control was a problem. In Uganda, the international community has maintained its own blood supply for expatriates. During a visit to Zimbabwe in the late 1990s, I met a resident foreign health expert who thought about having his arm tattooed, ‘Do not transfuse,’ so that if he were in a traffic accident and unconscious the medics would see his message.

International AIDS prevention programs that put a low priority on blood safety influenced national programs to do so as well. For example, in the early 1990s, the government of India ‘initially requested World Bank support primarily for blood safety,’ but ‘Following an intensive dialogue with the [World] Bank and WHO’ the project was redesigned to emphasize other issues.[xl] With the revised design, India proposed to test only ‘the majority of blood units.’ The government of India did not implement policies to stop HIV transmission through blood transfusions until India’s Supreme Court ordered it to do so in 1996.

A 1997 review of blood transfusions in Africa rues that the Global Blood Safety Initiative ‘did not receive the financial and other backing commensurate with the proportion of the pandemic fueled by blood transfusion…’[xli] Towards the end of the 1990s, WHO formed a Blood Safety Unit to assist member states. This too operated with limited resources. When I visited the unit in 2001, staff presented strategies to ensure safe blood transfusions, but without any budgets or timelines to show that these strategies could be or would be implemented any time soon – or indeed ever.

From 2003, the US Senate directed USAID and CDC to use a portion of money allocated for AIDS prevention in Africa, Asia, and the Caribbean to improve blood safety. During 2004-06, these agencies committed a total of more than $100 million to blood safety in 15 target countries (12 in Africa, and Guyana, Haiti, and Vietnam), although actual spending lagged.[xlii]

Although most countries in Africa report that all or most blood is tested for HIV, WHO assessed in 2006 that less than 12 percent was ‘tested for HIV in a quality-assured manner.’[xliii] As of 2005, WHO estimated that transfusions infect 160,000 people worldwide each year,[xliv] accounting for 5 percent of new HIV infections. This is a weak estimate, calculated from estimates of the numbers of transfusions and the percentage of transfused blood that is contaminated. Because transfusions are not so common, and because countries with some of the worst HIV epidemics (especially South Africa) do a pretty good job screening transfused blood, 5 percent may over-estimate the proportion of HIV infections from transfusions.

Because of insufficient attention to sterile procedures, blood donors have also been at risk. Studies in India, China, Mexico, and other countries show that tens of thousands of people have been infected with HIV during blood and plasma donation. In Africa, with rare exceptions, researchers have not asked about blood donation as a risk for HIV, even though repeat paid and replacement donors often had higher HIV prevalence than other adults. During hearings on blood safety in Africa in the US Congress in 2006, one witness noted that blood donors in the US ‘take for granted that…the needle is sterile, and that being at the health facility will not threaten our own health,’ whereas ‘These are all assumptions that do not necessarily apply in Africa.’ [xlv]

 

Preventing HIV through injections: Too late, too little       

 

Among all public health programs advised and supported by international agencies, the Expanded Programme on Immunization (EPI) was most alert to lapses in infection control. From the end of the 1970s, EPI managers recognized that a large proportion of immunization injections were unsafe. Responses included supplying autoclaves, training healthcare workers and managers, and a search for safer technologies.

In 1987, US Surgeon General Koop asked the US patent office to expedite patent applications for non-reusable injection equipment.[xlvi] In the same year, EPI staff met with inventors and representatives of companies producing syringes to review proposed designs for auto-destruct syringes (that break after one use) and pre-filled disposable syringes that could not be refilled and reused. From these meetings, EPI’s experts recognized a number of promising designs, and anticipated ‘Volume production…by the end of 1988 for more than one manufacturer.’[xlvii]

For various reasons, including disagreements about the best strategy to ensure safe injections[xlviii] and alleged opposition by at least one syringe producer,[xlix] the shift to auto-destruct (currently known as autodisable) syringes for immunizations dragged out over several decades. UNICEF’s first contract for 80 million syringes asked for delivery to begin in 1992.[l] This was delayed. As of 1996, WHO estimated that only 60 million (6 percent) of 1 billion immunization injections in developing countries used autodisable syringes.[li]

 

Building support for injection safety   

 

Through the late 1980s, although public health experts were generally aware that injections in Africa and Asia were often unsafe, they had only a vague sense of the size of the problem. From 1989, surveys provided progressively better information about the numbers of injections and the frequency of unsafe practices.

In six African countries during 1989-90, adults reported an average of 1.7 to 2.7 injections per year.[lii] A WHO-sponsored study in Uganda in the early 1990s found that 37 percent of households reported a history of an injection-related abscess, and that healthcare facilities often reused equipment without sterilization. One clinic, for example, sterilized its three syringes once each day, but reused them to inject an average of 15 patients per day.[liii] A 1997 study of immunization injections in 26 health facilities in Swaziland found that health staff in eight facilities changed needles while reusing syringes, and in two facilities reused disposable syringes and needles.[liv]

During 1995-98, WHO surveyed injection practices in 13 African countries. A summary of findings from these surveys concluded:[lv]

 

…the study countries have not made any progress with regard to safety over the last 10 years. The high rates of injection-associated abscesses indicate that injection practices are still poor. However, abscesses only represent the tip of the iceberg of AEFIs [adverse events following immunization]. In Africa, where hepatitis B virus (HBV) and the human immunodeficiency virus (HIV) are very prevalent, transmission of bloodborne pathogens from one patient to another…could lead to a much higher burden of initially asymptomatic chronic diseases.

 

Unsafe injections reflect, in part, lack of knowledge among health care workers about what is required to give a safe injection. For example, 81 percent of doctors surveyed in India[lvi] in 1992, and 91 percent of healthcare workers surveyed in Ethiopia[lvii] in 2003-04 thought that an injection was safe if the provider changed the needle but reused the syringe.

During the 1990s, WHO’s EPI staff recognized that ‘Rapid and substantial progress towards safer injections needs a much broader approach to encompass all types of injections,’ not only injections for immunization.[lviii] EPI found allies for injection safety in WHO’s Action Programme on Essential Drugs, USAID, CDC, and elsewhere. In 1994, African ministers of health meeting in Yamoussoukro, Cote d’Ivoire, endorsed a declaration that 95 percent of injections for immunization should use sterile syringes and needles by 1997.[lix] However, not everyone associated with immunizations was equally concerned about injection safety. Notably, the strategic plan for 1998-2001 of the Global Programme for Vaccines and Immunization did not mention injection safety among its 12 priorities.[lx]

 

Late progress towards injection safety

 

In 1999, advocates for injection safety achieved major breakthroughs. In October 1999, the Bulletin of the World Health Organization published a landmark paper that reported previously unpublished information from WHO-sponsored surveys of injection practices during 1987-1999. In 10 of 12 African and Asia countries from which data were available (listed by region, but naming only five countries) healthcare workers had reused syringes or needles without sterilization for 50 percent to more than 90 percent of injections.[lxi] Health officials in WHO and in member governments had kept this information away from populations at risk. By not reporting most of these data according to countries, they continued to do so. A companion paper in the same issue of the Bulletin estimated that unsafe injections in developing and transition countries infected 80,000-160,000 people with HIV in a year,[lxii] which was roughly 2-4 percent of estimated HIV incidence (see Chapter 8).

This accumulated evidence was too much to ignore. In 1999, WHO identified ‘immunization safety’ as a priority program within the Department of Vaccines and Biologicals, and established a Steering Committee on Immunization Safety to advise the Department. The report of the first meeting of the Steering Committee acknowledges – 25 years after EPI began – that ‘up to one-third of immunization injections are not carried out in a way that guarantees sterility.’[lxiii]

In the same year, WHO together with UNICEF and the UN Population Fund set a goal to shift immunization injections to autodisable syringes by the end of 2003.[lxiv] Along with this new policy, WHO along with other organizations established the Safe Injection Global Network (SIGN) as a loose affiliation of public and private organizations. With a small secretariat housed in WHO’s offices in Geneva, SIGN worked with public and private organizations to reduce unsafe practices not only for immunizations, but also for curative injections.

SIGN also promoted national assessments of injection practices that progressively improved information about injection numbers and practices. In 2002, a WHO team used information from new studies to estimate that Africans received an average of 2.0-2.2 injections per person per year, of which 17-19 percent reused syringes and/or needles without sterilization.[lxv] A massive study of injection practices in India during 2002-03 reported an average of 5.8 injections per person per year, of which 23 percent reused unsterile or unreliably sterile syringes and/or needles.[lxvi] Unsafe injections in India were more common in four southern states with relatively high HIV prevalence than in most other states.

During 2002-03, an unpublished review commissioned by UNAIDS along with several articles in medical journals proposed that injections might be responsible for much more than 5 percent of HIV infections (see Chapter 8). WHO and UNAIDS rejected these new estimates. However, the US Senate responded with several hearings,[lxvii] and subsequently pressed the US government to use a portion of the funds allocated for AIDS prevention to promote infection control. During 2004-06, the US provided roughly $2 million per country per year for injection safety in 12 African countries and Guyana, Haiti, and Vietnam (funding varied by country). But the US cut this funding back to about $1 million per country in 2007.

As of 2009, immunization injections are safer, but not safe. UNICEF and other international and foreign aid agencies have shifted immunization support to autodisable syringes. From 2006 India shifted all centrally-funded immunizations to autodisable syringes, and many other – but not all – developing countries have done so as well. However, donors and countries continue to rely on multidose vials containing vaccine for as many as 20 patients, which are a risk to spread bloodborne pathogens. Although there was much left to do, in 2005 WHO disbanded the Steering Committee on Immunization Safety.[lxviii]

Less progress has been achieved with curative injections, which account for more than 90 percent of injections. Autodisable syringes have made few inroads into this market. As of early 2009, a handful of governments, including governments of DRC, Uganda,[lxix] Nigeria, and India (for central government hospitals only)[lxx] require autodisable syringes for curative injections. However, autodisable syringes are, at best, only part of the solution. People get too many (unnecessary) injections, much of what is injected comes from multidose vials, and reuse cannot be avoided for some specialized injection equipment.

 

Other invasive procedures: Unsafe!         

 

Taken together, other blood exposures in formal and informal healthcare and cosmetic services could well be more important than injections in transmitting HIV and other bloodborne pathogens. Beginning in 1999, USAID has sponsored national surveys to assess the ability of public and private health facilities to provide various kinds of health services. Along with other issues, these ‘Service Provision Assessments’ examine each facility’s capacity to sterilize instruments – equipment, knowledge, and written guidelines – but do not look at actual practices. Through early 2009, survey results are available from seven countries with generalized HIV epidemics, Ghana, Guyana, Kenya, Rwanda, Tanzania, Uganda, and Zambia. Depending on the country, surveys focused on facilities delivering maternal and child healthcare and/or HIV/AIDS testing and care. Setting aside the first survey in Kenya in 1999, nine surveys during 2001-2007 found that only 55-89 percent (median 68 percent) of facilities had equipment to sterilize instruments (through autoclaving, high-level chemical disinfection, dry heat, boiling, or steaming).[lxxi]

A study of infection control in maternity wards in Free State, South Africa, in 2004 found traces of blood on 11 of 49 instruments that regularly come into contact with mothers’ or infants’ wounds or mucous membranes, such as forceps, scissors, and staple guns.[lxxii] In dental clinics, the same study found traces of blood on 17 of 69 items such as gloves, drill heads, and forceps. In dental clinics, ‘Visible blood was noted on 15 items, 12 of which were immediately used for the next patient without cleaning.’[lxxiii]

Doctors in India have been observed to reuse suture needles for eye surgery after soaking in disinfectant or wiping with alcohol (precautions which are not adequate to kill HIV).[lxxiv] In Africa and India, saline infusions are popular and common. During recent research on blood exposures in India, people in several states reported doctors giving infusions with needles and tubes reused without sterilization.[lxxv]

Several studies in India report men and women reported standing in line for tattoos administered with the same needles and inkpots. With such practices, HIV and other bloodborne pathogens can pass from client to client both on the needles and through the ink.[lxxvi]

 

Women at risk    

 

Some evidence shows that women receive more invasive healthcare than men. A study of admissions to a mission hospital in northern Uganda during 1992-2004 found 1.8 women admitted for every man in the age range 15-44 years. In that age range, ‘delivery and gynaeco-obstetrical conditions’ and ‘inflammatory diseases of the female pelvis’ accounted for more than 40 percent of women’s admissions. The study summarized that ‘women suffer disproportionately from their reproductive role.’[lxxvii]

Antenatal care in African and Asia commonly includes taking venous blood (to test for syphilis) and tetanus vaccinations. Immunization schedules in most African countries prescribe five tetanus vaccinations for women,[lxxviii] and two are often given in the several months before delivery.

Some birth control methods involve invasive procedures. As of 2005, an estimated, 4.8 percent of married women of reproductive age in Africa (including more than 10 percent in Botswana, Kenya, Lesotho, Madagascar, Malawi, Namibia, South Africa, and Swaziland) used injectable hormones for birth control, most often Depo-Provera injected every three months.[lxxix] An analysis of information from national surveys in Kenya, Lesotho, Malawi, and Zimbabwe found that women aged 15-24 years who had ever used Depo-Provera were 1.34 times more likely to be HIV-positive than other young women (after taking into consideration other relevant factors such as sexual behavior).[lxxx] Another study, among low-risk women in Malawi, found that women taking Depo-Provera acquired HIV infection at the rate of 6 percent per year, compared to less than 2 percent per year among women not taking Depo-Provera.[lxxxi]

Injectable hormones have been rare in India. On the other hand, 34 percent of married women in India and 14 percent in Southern Africa rely on female sterilization for birth control.[lxxxii] India’s family planning program offers female sterilization (tubal ligations) to poor women in health camps (temporary clinics with visiting doctors). Observers at one health camp reported that the surgical team sterilized 48 women in just over two hours. The time allowed for each surgery appeared too brief to sterilize the instruments.[lxxxiii]

Vaginal exams can expose women to sexually transmitted pathogens. Surveys of health facilities in Kenya, Rwanda, and Tanzania during 2004-07 reported that only 1 percent to 32 percent of specula used in vaginal exams were sterilize.[lxxxiv] Similarly, healthcare staff in India commonly reuse specula without sterilization. In surveys during 2001-04, sterile gloves were available in only 48-67 percent of facilities offering maternal and child healthcare in Ghana, Kenya, and Rwanda.[lxxxv] Healthcare staff who use gloves to protect themselves may not sterilize or discard them between patients. ‘Promiscuous’ specula and gloves could spread genital herpes and other sexually transmitted disease.

WHO, UNICEF, and the UN Population Fund estimate that at least 5 percent of births require caesarean sections to protect mother or child.[lxxxvi] In some African communities, caesarean sections are already common. For example, a study in rural Zimbabwe in 1992-93 reported that 6.3 percent of 831 deliveries were caesarean.[lxxxvii] Although induced abortions are illegal across most of Africa, they are common. WHO estimated 4.2 million abortions annually (14 per 100 live births) in Africa around the year 2000, and 7.2 million annually (18 per 100 live births) in south-central Asia.[lxxxviii]

Organizations and initiatives promoting healthcare for women include the UN Population Fund, which started in 1970,[lxxxix] and the Safe Motherhood Initiative, which began in 1987.[xc] No organization promoting healthcare for women has systematically surveyed and reported infection control practices in women’s healthcare in countries with generalized HIV epidemics.

 

Healthcare for sex workers 

 

Relative to other women, sex workers have more risks to acquire HIV infections not only from sex, but also from blood exposures. Sex workers seek frequent injections to treat and even to prevent sexually transmitted disease. In a 1987 study in Nigeria, most sex workers reported ‘injections of antibiotics as prophylaxis against infection.’[xci] In Tamil Nadu, India, some sex workers thought they were at low risk for HIV infection because, ‘I take injections regularly to prevent diseases.’[xcii] In Thailand during the early 1990s, brothel owners injected sex workers with Depo-Provera to prevent pregnancies. In Chennai, India, many brothel owners arranged for private doctors to give weekly injections of antibiotics to control sexually transmitted diseases.[xciii]

UNAIDS, USAID, Gates Foundation, and other donors have funded and/or promoted treating sex workers for sexually transmitted disease as a component in AIDS prevention programs. Because of insufficient attention to infection control, these initiatives could also spread HIV. Healthcare for sex workers, a stigmatized group, is likely no safer than for other adults. The only two studies I have found that looked at infection control practices during healthcare for sex workers surveyed facilities treating sexually transmitted disease in Maharashtra, India.[xciv] Both studies asked about gloves to protect healthcare staff, but ignored risks to sex workers.

 

World Alliance for Patient Safety promotes learning from errors         

 

During the UN General Assembly Special Session on HIV/AIDS in 2001, governments committed ‘By 2003, [to] implement universal precautions in health-care settings to prevent transmission of HIV infection...’[xcv] The goal was not achieved by 2003, but the commitment remains.

In formulating strategies to ensure universal precautions in Africa and Asia, it is relevant to consider EPI’s experience. During the 1980s and 1990s, EPI provided autoclaves, spare parts, training, and supervision to promote use of sterile syringes and needles. In 1999, EPI determined that all of its aid and efforts for 25 years had not been enough to ensure that syringes and needles were sterilized before being reused. The solution that EPI arrived at – to shift immunization injections to autodisable syringes – should ring alarms among healthcare providers and patients. Sterilization may not be reliable!

Although autodisable syringes reduce equipment reuse for immunizations, and may do so as well for curative injections, sterilizing and reusing equipment cannot reasonably be avoided during deliveries, dental care, surgeries, and other healthcare procedures. At the same time, EPI’s experience demonstrates that it is not enough for healthcare managers to train, encourage, and promote sterilization of reused instruments. These activities are all necessary, but they are not enough to ensure that instruments are sterilized.

If healthcare is to be safe, errors must be rare. An efficient way to ensure that errors are rare is to look for them, learn from them, and correct them. WHO began to emphasize this approach in 2004 with the formation of the World Alliance for Patient Safety, which is tasked to advise and assist WHO member countries to improve patient safety. One of the first initiatives of the Alliance was to develop guidelines for ‘adverse event reporting and learning systems.’ ‘Adverse events’ are instances in which patients have been harmed, and ‘potential adverse events’ are mistakes that could harm patients. According to these guidelines, healthcare organizations should ensure that ‘reporting is safe for the individuals who report,’ that ‘reporting leads to a constructive response,’ and that reports are analyzed and changes proposed.[xcvi]

The Alliance, with its emphasis on reporting and learning from adverse events, could make an important contribution to infection control for HIV prevention. On the other hand, if it ignores problems, it becomes an obstacle, by implicitly assuring people that all is well, or at least not so bad that change is required. When a guard dog does not bark, people think there is no danger. In its first several years, the Alliance has been a dog that does not bark. Silence on key issues undermines its potential contribution to improve patients’ safety.

 

Not investigating adverse events 

 

Through early 2009, at least five countries with concentrated HIV epidemics (see Table 9.1) responded to unexplained HIV infections in children with thorough investigations, testing thousands of possibly exposed children. No country with a generalized HIV epidemic – all of which receive substantial amounts of health aid – has done so.

Some evidence suggests that international agencies and foreign aid programs have discouraged investigations. In 1994, the head of WHO’s Global Programme on AIDS and the future head of UNAIDS criticized publicity given to Russia’s 1988-89 nosocomial HIV outbreak.[xcvii]

 

The media, which has publicized nosocomial outbreaks, has helped to increase public awareness about the dangers of nosocomial transmission. But the short-term benefits of increased public awareness may not always be positive [sic]. The current outbreak of diphtheria in Russia…has been blamed in part on publicity surrounding nosocomial HIV transmission in southern Russia and other problems in the health-care system, which are thought to have discouraged mothers of young children from seeking immunizations from a health-care system that they perceived to be unsafe.

 

During the Safe Injection Global Network’s annual meeting in Nairobi in 2003, a health officer from Burkina Faso asked for help to investigate unexplained HIV infections in children. WHO staff who were attending the meeting sat silent.

Through early 2009, the World Alliance for Patient Safety has said nothing to encourage investigations of unexplained HIV infections – adverse events – in countries with generalized epidemics. There have been many opportunities to do so. For example, the Alliance could have praised the government of Kazakhstan for investigating unexplained infections in children in 2006, and could have recommended Kazakhstan’s investigation as an example for African governments. The Alliance has also been silent about mounting numbers of unexplained HIV infections in African adults with no reported sexual risks.

 

Not investigating potential adverse events        

 

In countries where governments and courts enforce standard precautions, reported lapses lead to investigations. For example, when a clinic in California found that a healthcare worker had been reusing equipment to draw blood, the company that operated the clinic fired the worker and tested more than 15,000 people for bloodborne viruses.[xcviii] In contrast, in much of Africa and Asia, government health officials who hear about reuse of unsterile instruments may take steps to change the practice, but they rarely call anyone for tests. For example, when a 2004 study in South Africa reported common reuse of unsterile and even visibly bloody instruments in dental clinics,[xcix] no one made any effort to find and test patients at risk.

When potential adverse events are common, not all events can be investigated. When they occur in a wide range of formal and informal settings, multiple strategies are required to monitor and to respond. During 2004-09, the Alliance repeated previous WHO estimates about the frequency of unsafe injections,[c] but was silent about the inadequacy of current strategies to identify and to respond to common and even routine reuse of invasive instruments without sterilization in varied settings.

 

Not warning the public

 

During the last several decades, in countries with high prevalence of hepatitis B and C and HIV infection, ministries of health have not investigated unexplained infections, and have often withheld findings showing frequent reuse of syringes and needles in health facilities. At the same time, WHO and ministries of health have urged the public to come for immunizations, blood tests, treatment of sexually transmitted disease, and other invasive procedures. In 2003, AIDS experts criticized that public discussion of evidence linking healthcare to HIV could ‘undermine confidence in health care and vaccinations globally.’[ci]

In effect, healthcare professionals have asserted that they should decide the level of risk that is acceptable for patients in Africa and Asia. This transgresses medical ethics, which enjoin doctors to give patients accurate information about risks, leaving patients to decide how much risk they want to accept. Risk is something that even illiterate people can understand. Farmers deal with uncertainty about the weather. Prostitution may be the oldest profession, but gambling and bookmaking are not far behind. Moreover, not warning the public about dangers with unsterilized instruments disregards the role of an informed public in helping to devise, support, and enforce solutions.



[i] Commenges D, Alioum A, Lepage P, et al. ‘Estimating the incubation period of paediatric AIDS in Rwanda’, AIDS, 1992, 6: 1515-20. p. 1517.

[ii] 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’, 9th Int Conf AIDS, Berlin 6-11 June 1993. Abstract no. WS-C13-2. Available at:

http://www.aegis.com/aidsline/1993/nov/M93B3075.html (accessed 9 September 2007).

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

[iv] Chant K, Lowe D, Rubin G, et al. ‘Patient-to-patient transmission of HIV in private surgical consulting rooms [letter]’, Lancet, 1993, 342: 1548-1549; Collignon P. ‘Patient-to-patient transmission of HIV [letter]’, Lancet, 1994, 343: 415; Shields JW. ‘Patient-to-patient transmission of HIV [letter]’, Lancet, 1994, 343: 415.

[v] Avila C, Stetler HC, Sepúlveda J, et al. ‘The epidemiology of HIV transmission among paid plasma donors, Mexico City, Mexico’, AIDS, 1989, 3: 631-3.

[vi] Pokrovskii VV, Eramova II, Deulina MO, et al. ‘An intrahospital outbreak of HIV infection in Elista [in Russian]’, Zh Microbiol Epidemiol Immunobiol, 1990, 4: 17-23; Pokrovsky VV. ‘Localization of nosocomial outbreak of HIV infection in southern Russia in 1988-89’, 8th Int Conf AIDS, Amsterdam 19-24 July 1992. Abstract no. PoC 4138; Sauhat SR, Kotova EA, Prokopenkova SA, et al. ‘Risk factors for HIV transmission in hospital outbreak’, 8th Int Conf AIDS, Amsterdam 19-24 July 1992. Abstract no. PoC 4288.

[vii] Patrascu IV, Dumitrescu O. ‘The epidemic of human immunodeficiency virus infection in Romanian children’, AIDS Res Hum Retroviruses, 1993, 9: 99-104; Drucker E, Apetrei C, Heimer R, et al. ‘The role of unsterile injections in the HIV pandemic’, in Sande MA, Volberding PY, Lange J, et al. Global HIV/AIDS Medicine. Philadelphia: Saunders, 2007. pp. 755-67; Apetrei C, Loussert-Ajaka I, Collin G, et al. ‘HIV type 1 subtype F sequences in Romanian children and adults’, AIDS Res Hum Retroviruses 1997; 13: 363-5.

[viii] Banerjee K, Rodrigues J, Israel Z, et al. ‘Outbreak of HIV seropositivity among commercial plasma donors in Pune, India [letter]’, Lancet, 1989; ii: 166.

[ix] Bhimani GV, Gilada IS. ‘HIV prevalence in people with no fixed abode – A study of blood donorship patterns and risk determinants’, 8th Int Conf AIDS, Amsterdam 19-24 July 1992. Abstract MoC00937.

[x] Hassan NF, El Ghorab NM, Abdel Rehim MS, et al. ‘HIV infection in renal dialysis patients in Egypt [letter], AIDS, 1994, 8: 853.

[xi] Dyer E. ‘Argentinian doctors accused of spreading AIDS’, BMJ, 1993; 307: 584.

[xii] Velandia M, Fridkin SK, Cardenas V, et al. ‘Transmission of HIV in dialysis centre’, Lancet, 1995, 345: 1417-21.

[xiii] Dyer E. ‘Argentinian doctors accused’.

[xiv] El Sayed NM, Gomatos PJ, Beck-Sague CM, et al. ‘Epidemic of human immunodeficiency virus in renal dialysis centers in Egypt’, J Infect Dis, 2000, 181: 91-7.

[xv] Wu Z, Liu Z, Detels R. ‘HIV-1 infection in commercial plasma donors in China [letter]’, Lancet, 1995, 346: 61-2; Wu Z, Rou K, Detels R. ‘Prevalence of HIV infection among former commercial plasma donors in rural eastern China’, Health Policy Plan, 2001, 16: 41-6; Ministry of Health, China, UNAIDS, WHO. 2005 Update on the HIV/AIDS epidemic and response in China. Geneva: WHO, 2006.

[xvi] Visco-Comandini U, Cappiello G, Liuzzi G, et al. ‘Monophyletic HIV type 1 CRF02-AG in a nosocomial outbreak in Benghazi, Libya’, AIDS Res Hum Retroviruses, 2002, 18: 727-32; de Oliviera T, Pybus OG, Rambaut A, et al. ‘HIV-1 and HCV sequences from Libyan outbreak’, Nature, 2006, 444: 836-7.

[xvii] ‘Kazakhstan: more HIV-infected children found in southern Kazakhstan’, RadioFreeEurope/RadioLiberty, 3 October 2007. Available at:

http://uqconnect.net/signfiles/Archives/SIGN-POST00405.txt (accessed 10 October 2007);In the courts: Health workers sentenced to prison in Kazakhstan for criminal negligence after HIV outbreak among women, children’. Kaisernetwork.org, 2 January 2008. Available at: http://www.kaisernetwork.org/daily_reports/rep_index.cfm?hint=1&DR_ID=49564 (accessed 27 March 2009).

[xviii] Shersen D. ‘Kyrgyzstan: Officials grapple with HIV outbreak’, EurasiaNet, 30 October 2007. Available at: http://uqconnect.net/signfiles/Archives/SIGN-POST00419.txt (accessed 1 November 2007). ‘AP/Houston Chronicle examines HIV outbreak among 72 children, 16 mothers through tainted blood and used needles’. Kaisernetwork.org, 11 April 2008. Available at:

http://www.kaisernetwork.org/daily_reports/rep_index.cfm?hint=1&DR_ID=51472 (accessed 27 March 2009).

[xix] Gisselquist D, Potterat JJ, Brody S. ‘HIV transmission during pediatric health care in sub-Saharan Africa: Risks and evidence’, S Afr Med J, 2004, 94: 109-16.

[xx] Singhal T. ‘Burden of HIV in India due to unsafe injections and blood transfusions’, MSc thesis submitted to University of London, 2002; Correa M, Gisselquist D. HIV from Blood Exposures in India – An exploratory study. Colombo: Norwegian Church Aid, 2005.

[xxi] Christiansen CB, Nielsen C, Machucca R. ‘Cluster of HIV-1 infection among children in Indian Hospital in Bombay. Informal report to WHO, September 1998.’ Department of Virology, Statens Serum Institut, Copenhagen, Denmark.

[xxii] van Zyl GU, Cotton MF, van Rensburg EJ. ‘Registry: Unusual HIV transmission in children under the age of 10 years’, So Afr Med J, 2000, 90: 1064-5.

[xxiii] Hiemstra R, Rabie H, Schaaf H, et al. ‘Unexplained HIV-1 infection in children – documenting cases and assessing for possible risk factors’, So Afr Med J, 2004, 94: 188-93.

[xxiv] Farham B. ‘Risk of HIV transmission during paediatric health care in sub-Saharan Africa’, So Afr Med J, 2004, 94: 342-3. p. 343.

[xxv] ORC Macro. Uganda HIV/AIDS Sero-Behavioural Survey 2004-05. Calverton, Maryand: ORC Macro, 2006.

[xxvi] Heymann DL, Edstrom K. ‘Strategies for AIDS prevention and control in sub-Saharan Africa’, AIDS, 1991, 5 (suppl 1): S197-208. p. S201.

[xxvii] Global Programme on AIDS, WHO. ‘The cost of HIV/AIDS prevention strategies in developing countries.’ Doc. no. GPA/DIR/93.2. Geneva: WHO, 1993.

[xxviii] Global Programme on AIDS, WHO. ‘Proposed Programme Budget 1994-95.’ Doc. no. GPA/DIR/93.1. Geneva: WHO, 1993.

[xxix] Public Broadcasting Service. ‘Frontline: The age of AIDS – Interview with Peter Piot.’ Posted May 2006. Available at:

http://www.pbs.org/wgbh/pages/frontline/aids/interviews/piot.html (accessed 22 September 2007).

[xxx] ORC Macro. Tanzania Service Provision Assessment Survey 2006. Calverton, Maryland: ORC Macro, 2007.

[xxxi] Ippolito G, Puro V, Heptonstall J, et al. ‘Occupational human immunodeficiency virus infection in health care workers: worldwide cases through September 1997’, Clin Infect Dis, 1999, 28: 365-83.

[xxxii] Sagoe-Moses C, Pearson RD, Perry J, et al. ‘Risks to health care workers in developing countries’, N Eng J Med, 2001, 345: 538-41.

[xxxiii] Pruss-Ustun A, Rapiti E, Hutin Y. ‘Estimation of the global burden of disease attributable to contaminated sharps injuries among health-care workers’, Am J Ind Med, 2005, 48: 482-90.

[xxxiv] Global Blood Safety Initiative. ‘Consensus Statement on Accelerated Strategies to Reduce the Risk of Transmission of HIV by Blood Transfusion.’ Doc. no. WHO/GPA/INF/89.13, Geneva: WHO, 1989.; Global Blood Safety Initiative. ‘Minimum Targets for Blood Transfusion Services.’ Doc. no. WHO/GPA/INF/89.14, Geneva: WHO, 1989; Global Blood Safety Initiative. ‘Essential Consumables and Equipment for a Blood Transfusion Service.’ Doc. no. WHO/GPA/INF/89.15, Geneva: WHO, 1989.

[xxxv] ‘AIDS: Prevention, policies, and prostitutes’, Lancet 1989; i: 1111-13. pp. 1112-13.

[xxxvi] Heymann DL, Edstrom K. ‘Strategies for HIV prevention’. p. S202.

[xxxvii] Flander A. ‘HIV infection in Africa [letter]’, BMJ, 1989, 299: 260.

[xxxviii] N’tita I, Mulanga K, Dulat C, et al. ‘Risk of transfusion-associated HIV transmission in Kinshasa, Zaire’, AIDS, 1991, 5: 437-9.

[xxxix] Peter Jones. ‘Annotation to abstract of N’tita I, Mulanga K, Dulat C, et al. “Risk of transfusion-associated HIV transmission in Kinshasa, Zaire”’, AIDS, 1991; 5: 437-9, in: AIDS Technical Bulletin, 1991, 4: 174.

[xl] World Bank. Project Performance Assessment Report: India National AIDS Control Project (Credit No. 2350), Report No. 26224. Washington DC: World Bank, 2003. pp. 2-3.

[xli] Fleming AF. ‘HIV and blood transfusion in sub-Saharan Africa 1997’, Transfu Sci, 18, 167-79. p. 172.

[xlii] ‘Making safe blood available in Africa: Hearing before the Subcomm on Africa, Global Human Rights and International Operations of the House Comm on International Relations.’ 109th Cong, 2nd Sess (27 June 2006). Testimony by Ryan C, p. 39. Available at:

http://commdocs.house.gov/committees/intlrel/hfa28424.000/hfa28424_0f.htm (accessed 9 September 2007).

[xliii] Ibid. Testimony by Dinghra, p. 130.

[xliv] WHO. Global Patient Safety Challenge 2005-2006. Geneva: WHO, no date. Available at:

http://www.who.int/gpsc/background/en/index.html (accessed 9 September 2007).

[xlv] ‘Making safe blood available in Africa: Hearing before the Subcomm on Africa’. Testimony by Green E, p. 101.

[xlvi] Marmor M, Hartsock P. ‘Self-destructing (non-reusable) syringes’, Lancet, 1991, 338: 438-9.

[xlvii] WHO. ‘Evaluation of injection technologies’, Geneva: WHO, 1987. Doc. no. WHO/EPI/CCIS/87.2. p. 9.

[xlviii] Battersby A, Feilden R, Stoeckel P, et al. ‘Strategies for safe injections’, Bull WHO, 1999, 77: 996-1000.

[xlix] Holding R, Carlsen W. ‘Deadly needles: Lost chance to avert crisis’, San Francisco Chronicle, 28 October 1998; Holding R, Carlsen W. ‘Deadly needles: Epidemic’s devastating toll’, San Francisco Chronicle, 29 October 1998.

[l] Marmor M, Hartsock P. ‘Self-destructing (non-reusable) syringes’.

[li] WHO. ‘State of the world’s vaccines and immunization.’ Geneva: WHO, 1996. Doc. no. WHO/GPV/96.04.

[lii] Ferry B. ‘Risk factors related to HIV transmission: Sexually transmitted diseases, alcohol consumption and medically-related injections’, in Cleland J, Ferry B (eds). Sexual Behaviour and AIDS in the Developing World. Geneva: WHO, 1995. pp. 193-207.

[liii] van Staa A, Hardon A. ‘Injection practices in the developing world: a comparative review of field studies in Uganda and Indonesia’, Doc. no. WHO/DAP/96.4.

[liv] Daly AD, Nxumalo MP, Biellik RJ. ‘An assessment of safe injection practices in health facilities in Swaziland’, S Afr Med J, 2004, 94: 194-7.

[lv] Dicko M, Oni A-QO, Ganivet S, et al. ‘Safety of immunization injections in Africa: Not simply a problem of logistics’, Bull WHO, 2000, 78: 163-9. p. 166.

[lvi] Bollinger RC, Tripathy SP, Quinn TC. ‘The human immunodeficiency virus epidemic in India: Current magnitude and future projections’, Medicine, 1995, 74: 97-106.

[lvii] W/Gebriel Y. ‘Assessment of the safety of injections and related medical practices in health institutions at Sidama Zone, SNNPRS’, Thesis for the degree of Master of Public Health, 2004, Addis Ababa University.

[lviii] WHO. ‘Report of the Meeting of Interested Parties of the Global Programme for Vaccines and Immunization.’ Doc. no. WHO/GPV/98.08. p. 15. Geneva: WHO, 1998.

[lix] WHO. ‘State of the world’s vaccines’.

[lx] Global Programme for Vaccines and Immunization, WHO. ‘Strategic Plan 1988-2001.’ Doc. no.: WHO/GPV/98.04. Geneva: WHO, 1998.

[lxi] Simonsen L, Kane A, Lloyd J, et al. ‘Unsafe injections in the developing world and transmission of bloodborne pathogens: A review’, Bull WHO, 1999, 77: 789-800.

[lxii] Kane A, Lloyd M, Zaffran M, et al. ‘Transmission of hepatitis B, hepatitis C and human immunodeficiency viruses through unsafe injections in the developing world: Model-based regional estimates’, Bull WHO, 1999, 77: 801-7.

[lxiii] WHO. ‘Report of the first meeting of the Steering Committee on Immunization Safety, Geneva, 25-26 October 1999.’ Doc. no.: WHO/V&B/00.17. Geneva: WHO, 2000.

[lxiv] WHO. ‘Safety of injections: WHO-UNICEF-UNFPA joint statement on the use of auto-disable syringes in immunization services.’ Doc. no.: WHO/V&B/99.25. Geneva: WHO, 1999.

[lxv] Hauri AM, Armstrong GL, Hutin YJF. ‘The global burden of disease attributable to contaminated injections given in health care settings’, Int J STD AIDS, 2004, 15: 7-16.

[lxvi] India Clinical Epidemiology Network (IndiaCLEN) Program Evaluation Network (IPEN). Assessment of Injection Practices in India (2002-03). New Delhi: IPEN, 2005.

[lxvii] AIDS Crisis in Africa: Health Care Transmission. Hearing before the Senate Committee on Health Education, Labor and Pensions. 108th Cong, 1st Sess (27 March 2003). Available at:

http://help.senate.gov/Hearings/2003_03_27/2003_03_27.html (accessed 3 March 2007); Solutions to the Problem of Health Care Transmission of HIV/AIDS in Africa: Hearing before the Senate Comm on Health Education, Labor and Pensions. 108th Cong, 1st Sess (31 July 2003). Available at:

http://help.senate.gov/Hearings/2003_07_31/2003_07_31.html (accessed 3 March 2007).

[lxviii] ‘Sixth meeting of the Steering Committee on Immunization Safety’, Wkly Epidemiol Rec, 2005, 80: 389-96.

[lxix] Star Syringe. ‘ADs only please: Uganda ban on standard syringes comes into force.’ Available at: http://www.starsyringe.com/news.html (accessed 7 April 2009).

[lxx] Star Syringe. ‘ADs only please (part 2): India & Nigeria assured safe injections.’ Available at: http://www.starsyringe.com/news.html (accessed 7 April 2009).

[lxxi] ORC Macro. Ghana Service Provision Assessment Survey 2002. Calverton, Maryland: ORC Macro, 2003; ORC Macro. Guyana HIV/AIDS Service Provision Assessment Survey 2004. Calverton, Maryland: ORC Macro, 2005; ORC Macro. Kenya Service Provision Assessment Survey 2004: Maternal and Child Health, Family Planning and STIs. Calverton, Maryland: ORC Macro, 2005; ORC Macro. Kenya HIV/AIDS Service Provision Assessment Survey 2004. Calverton, Maryland: ORC Macro, 2005; ORC Macro. Rwanda Service Provision Assessment Survey 2001. Calverton, Maryland: ORC Macro, 2003; ORC Macro. Rwanda Service Provision Assessment Survey 2007. Calverton, Maryland: ORC Marco, 2008; ORC Macro. Tanzania Service Provision Assessment Survey 2006. Calverton, Maryland: ORC Marco, 2007; ORC Macro. Uganda Service Provision Assessment Survey 2007. Calverton, Maryland: ORC Marco, 2008; ORC Macro. Zambia HIV/AIDS Service Provision Assessment Survey 2005. Calverton, Maryland: ORC Macro, 2006.

[lxxii] Shisana O, Mehtar S, Mosala T, et al. HIV risk exposure among young children: A study of 2-9 year olds served by public health facilities in the Free State, South Africa. Cape Town: HSRC Press, 2005.

[lxxiii] Mehtar S, Shisana O, Mosala T, et al. ‘Infection control practices in public dental care services: findings from one South African Province’, J Hosp Infect, 2007, 66: 65-70. p. 69.

[lxxiv] Kermode M, Holmes W, Langkham B, et al. ‘Safer injections, fewer injections: Injection safety in rural north India, Trop Med Int Health, 2005, 10: 423-32.

[lxxv] Correa M, Gisselquist D. HIV from Blood Exposures in India.

[lxxvi] Ibid.; Panda S, Kumar MS, Lokabiraman S, et al. ‘Risk factors for HIV infection in injection drug users and evidence for onward transmission of HIV to their sexual partners in Chennai, India’, J Acquir Immune Defic Syndr, 2005, 39: 9-15.

[lxxvii] Accorsi S, Fabiani M, Nattabi B, et al. ‘Differences in hospital admissions for males and females in northern Uganda in the period 1992-2004: A consideration of gender and sex differences in health care use’, Trans R Soc Trop Med Hygiene, 2007, 101: 929-38. pp. 933, 935.

[lxxviii] ‘Expanded Programme on Immunization (EPI): Immunization schedules in the WHO Africa Region, 1995’, Wkly Epidemiol Rec, 1996, 71: 90-95.

[lxxix] Population Division, UN. ‘World Contraceptive Use 2005.’ New York: UN, no date. Available at:

http://www.un.org/esa/population/publications/contraceptive2005/WCU2005.htm (accessed 9 September 2007).

[lxxx] Leclerc PM, Dubois-Colas N, Garenne M. ‘Hormonal contraception and HIV prevalence in four African countries’. Contraception, 2008, 77: 371-6.

[lxxxi] Kumwenda NI, Kumwenda J, Kafuafula G, et al. ‘HIV-1 incidence among women of reorductive age in Malawi’. Int J STD AIDS, 2008, 19: 339-41.

[lxxxii] Population Division, UN. ‘World Contraceptive Use 2005.’

[lxxxiii] Ramanathan M, Dilip TR, Padmadas SS. ‘Quality of care in laparoscopic sterilization camps: observations from Kerala, India’, Reprod Health Matters, 1995, 3: 84-93.

[lxxxiv] ORC Macro. Kenya Service Provision Assessment Survey 2004. ORC Macro. Rwanda Service Provision Assessment Survey 2007. ORC Marco. Tanzania Service Provision Assessment Survey 2006.

[lxxxv] ORC Macro. Ghana Service Provision Assessment Survey 2002; ORC Macro. Kenya Service Provision Assessment Survey 2004; ORC Macro. Rwanda Service Provision Assessment Survey 2001.

[lxxxvi] AbouZahr C, Wardlaw T. ‘Maternal mortality at the end of a decade: Signs of progress? Bull WHO, 2001; 79: 561-8.

[lxxxvii] Nilses C, Nystrom L, Munjanja S, et al. ‘Self-reported reproductive outcome and implications in relation to use of care in women in rural Zimbabwe’, Acta Obstet Gynecol Scand, 2002, 81: 508-15.

[lxxxviii] Ahman E, Shah I. ‘Unsafe abortion: Worldwide estimates for 2000’, Reprod Health Matters, 2002, 10: 13-17.

[lxxxix] Department of Economic and Social Affairs, United Nations (UN) Secretariat. ‘Fertility, Contraception and Population Policies.’ Doc. no. ESA/P/WP.182. New York: UN, 2003.

[xc] Inter-Agency Group for Safe Motherhood. The Safe Motherhood Action Agenda: Priorities for the next decade. New York: Family Care International, 1998.

[xci] Chikwem JO, Ola TO, Gashau W, et al. ‘Impact of health education on prostitutes’ awareness and attitudes to acquired immune deficiency syndrome (AIDS)’, Public Health, 1988, 102: 439-45. p. 442.

[xcii] AIDS Prevention and Control Project (APAC). ‘HIV risk behavior surveillance survey in Tamil Nadu, wave VII’, Chennai: APAC, no date. p. 28. Available at: http://apacvhs.org/Pub_Res_BSS.html (accessed 30 September 2007).

[xciii] Asthana S, Oostvogels R. ‘Community participation in HIV prevention: problems and prospects for community-based strategies among female sex workers in Madras’, Soc Sci Med, 1996, 43: 133-48.

[xciv] Avert. Health Care Provider Survey in Maharashtra. Maharashtra: Avert, 2001; Avert. Health Care Provider Survey in Maharastra 2004, Round 2. Maharashtra: Avert, no date.

[xcv] UN General Assembly. ‘Declaration of Commitment on HIV/AIDS’, 2 August 2001. Doc. no. A/Res/S-26/2. New York: UN, 2001.

[xcvi] WHO. WHO draft guidelines for adverse event reporting and learning systems: From information to action. Doc. no. WHO/EIP/SPO/QPS/05.3. Geneva: WHO, 2005. p. 49.

[xcvii] Heymann DL, Piot P. ‘The laboratory, epidemiology, nosocomial infection and HIV’, AIDS, 1994; 8: 705-6. p. 705.

[xcviii] Porco TC, Aragon TJ, Fernyak SE, et al. ‘Risk of infection from needle reuse at a phlebotomy center’, Am J Pub Health, 2001, 91: 636-8.

[xcix] Mehtar S et al. ‘Infection control practices’.

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