Three years before, Rwanda had decided to make preventing cervical cancer a health priority. The government agreed a partnership with pharmaceutical company Merck to offer Rwandan girls the opportunity to be vaccinated against human papillomavirus (HPV), which causes cervical cancer.
Cervical cancer is the most common cancer in Rwandan women, and there were considerable cultural barriers to the vaccination program -- HPV is a sexually transmitted infection and talking about sex is taboo in Rwanda. Added to this, rumors that the vaccine could cause infertility made some parents reluctant to allow their daughters to be vaccinated.
Rwanda's economy and history also made it seem an improbable candidate for achieving high HPV vaccination coverage.
After the 1994 genocide, it was ranked as one of the poorest countries in the world. High-income countries had only achieved moderate coverage of the HPV vaccine; if the United States and France couldn't achieve high coverage, how could Rwanda?
The fourth most common cancer in women
Worldwide, cervical cancer is the fourth most common cancer in women. There were an estimated 570,000 new cases in 2018 -- and over 310,000 deaths, the vast majority in low- and middle-income countries. Sub-Saharan Africa has lagged behind the rest of the world in introducing the HPV vaccine and routine screening, which means the cancer often isn't identified and treated until it has reached an advanced stage.
Almost all cases of cervical cancer are caused by HPV. It is one of the commonest sexually transmitted infections globally, and most of us are infected with at least one type of genital HPV at some point in our lives -- usually as teenagers or young adults. In most cases the virus is harmless and resolves spontaneously without causing any symptoms such as genital warts.
The first vaccine against HPV became available in 2006. The news that there was a new vaccine which could drastically reduce the number of women getting cervical cancer went around the world. But with the excitement about the new vaccine came the realization that not all girls would have the same opportunity to receive it.
More than 800,000 people died in the Rwandan genocide, and its widespread destruction left the country devastated. Coverage of most World Health Organization-recommended childhood vaccinations plummeted to below 25%. But within 20 years, the number of babies in Rwanda receiving all recommended vaccinations, such as polio, measles and rubella, had increased to around 95%.
The Rwandan government had demonstrated the determination and thoroughness of its approach to vaccinations. Could it now have the same success with HPV?
Skepticism among parents
Bugesera is a district in the Eastern Province, not far from the border with Burundi. Billboards line roads through the district, advertising soft drinks alongside public health messages. One says: "Talk to your children about sex, it may save their lives."
Not far off the main road is Karambi, a village surrounded by banana plantations. Toddlers roll tyres down the red-earth roads, teenagers carry handfuls of firewood on their heads, and adults herd cows and goats.
In 2013, the then 12-year-old Ernestine Muhoza was vaccinated against HPV at her school. "The teachers called just girls for assembly and told us that there was a rise of a specific cancer among girls aged 12 and that it was time for us to get vaccinated," she says.
When she went home to tell her parents about the vaccination, they'd already heard about it on the radio and via community health workers.
Muhoza's parents readily agreed. But not every parent did. Some were skeptical. Why, they wondered, would their girls be getting vaccinated now, at this age? Why couldn't all girls and women receive the vaccine? And rumour had it that the vaccine would make girls infertile.
Community health worker Odette Mukarumongi worked tirelessly in Karambi to counteract the rumours. "I told parents that a girl will go into constant menstruation -- like endless bleeding -- if she gets cervical cancer," she says.
Mukarumongi says parents eventually "surrendered" and allowed their daughters to be vaccinated. Today, she says, parents rarely refuse, now that they can see the widespread acceptance of it in the community.
Fears over promiscuity
Leela Visaria, social researcher and honorary professor at the Gujarat Institute of Development Research in India, says: "The underlying reason why people don't want it [the vaccine] is the fact it's given to adolescent girls. They fear that girls will become promiscuous."
There is no evidence that boys or girls who receive the vaccine have sex earlier than those who do not have the vaccine. But this concern is one of the reasons that India -- a country where more than 67,000 women die from cervical cancer every year -- has refused to introduce HPV vaccine into its routine immunization program.
Peter Hotez, a vaccine scientist and dean of the National School of Tropical Medicine at Baylor College of Medicine in Texas, agrees that there is a problem in the fears that the vaccine sexualises young girls. "The other problem is that the anti-vax movement has been making false assertions about it -- claims that it leads to autoimmune diseases and paralysis.
"I think the movement is attempting to draw a line in the sand and say, 'no more vaccines' and when something like HPV comes along they are throwing everything they can at it. It's having a devastating impact. I worry that we will start to export this garbage and it will impact vaccine uptake in Africa."
Debate over free vaccines
"Initially, when the HPV vaccine was introduced in different countries, there were differences of opinion on whether to focus on HPV and how it's transmitted, or to focus on the fact that HPV leads to cancer and this vaccine will prevent cancer," says Mark Feinberg. He is the former chief public health and science officer at Merck who was involved with the Rwanda programme.
"Rwanda emphasized cancer prevention. It sought to communicate that the vaccine is here to protect young women from cervical cancer."
When Rwanda and Merck signed their agreement, it meant that from 2011 the pharmaceutical company would supply the country with HPV vaccinations for three years at no cost.
Merck wanted to demonstrate that it was feasible to introduce the vaccine in low-income countries in the hope that Gavi -- a global health alliance to increase access to vaccination in these countries -- would take note and get on board.
"You quickly recognize that you have a vaccine that can have such a major impact in preventing cervical cancer, and the greatest disease burden is concentrated in the world's poorest communities. You cannot with any conscience not come forward and make the vaccine affordable and create a sustainable vaccination program," Feinberg said.
"The program in Rwanda had two purposes: to get the vaccine to a population who could benefit, but also to demonstrate what was possible. Rwanda is an incredible country in its commitment to national health. If it wasn't possible in Rwanda, we knew it wouldn't be possible anywhere else."
Rwanda's decision to partner with Merck wasn't without its critics. In a scathing letter to the Lancet, German public health researchers voiced "serious doubts" that the HPV programme was "in the best interest of the people." A major issue, they contended, was that while the burden of cervical cancer in the region was substantial, there were far more pressing diseases to vaccinate against, such as tetanus and measles.
Rwanda's then Minister of Health, Agnes Binagwaho, replied publicly in a letter co-signed by two US researchers. They said that Rwanda already had very high vaccination rates for tetanus and measles, and asked: "Are the 330,000 Rwandan girls who will be vaccinated against a highly prevalent, oncogenic virus for free during the first phase of this program not regarded as 'the people'?"
Drawing an analogy with earlier opposition to antiretroviral therapy in Africa, they said that such objections were "the latest backlash against progressive health policies by African countries. When the possibility of prevention exists, writing off women to die of cancer solely because of where they are born is a violation of human rights."
Binagwaho, now vice-chancellor at the University of Global Health Equity in Rwanda, is still scathing about the critics of the decision to rollout the HPV vaccine. "The people who have created a backlash haven't done their homework -- they don't know our country, they don't know that our kids are well vaccinated with other vaccines available. [The HPV vaccine is] a great tool to prevent one of the most ravaging women's cancers. It is less costly to prevent cervical cancer and all its suffering."
Rwanda has proved to the world that it can achieve excellent HPV vaccination coverage. The Ministry of Health reports that 93% of girls now receive the vaccine.
Road to elimination
Since 2006, over 80 countries have introduced the HPV vaccine into their routine immunization programs. The majority are high-income, from Australia to the United Kingdom to Finland. These countries also have screening programmes for HPV and are moving from the pap smear test to a more advanced test, taken every five years, that detects high-risk HPV infections before cancer develops.
In Rwanda, before the HPV vaccine was introduced in 2011, there was no cervical cancer screening available in public health facilities. Along with the vaccination program, Rwanda also launched a national strategic plan for the prevention, control and management of cervical lesions and cancer. Done by nurses and doctors, the screening is available to women with HIV aged 30 to 50, and other women aged 35 to 45. It's unclear how effective and widespread this screening is.
Given that most cervical cancer cases occur in women in their 40s and 50s, if Rwanda is going to eliminate cervical cancer it will need a robust screening program that reaches women who