How a Zambian morgue is exposing the real covid toll in Africa

The morgue at Lusaka's University Teaching Hospital (UTH), a sprawling brick facility near the center of Zambia's capital, is not the most pleasant place to carry out a clinical study. Inside the cavernous interior, newly arrived bodies linger unattended-on rolling metal tables or on the concrete floor wrapped in blankets. Others lie stacked on open-air racks, where some stay unclaimed for months. The stench is overwhelming.

But it is here, among the cadavers at Zambia's largest hospital, that researchers are finally close to solving one of the pandemic's enduring mysteries: why Africa appeared to have been spared the brunt of the covid death toll experienced elsewhere. The truth, it increasingly appears, is that it wasn't.

That's the claim made by a new study, which has not yet been peer reviewed, based on tests of corpses carried out by staff equipped with nasal swabs and a heavy tolerance for the macabre. It constitutes perhaps the strongest clinical evidence yet that covid-19 deaths in Lusaka, and likely much of Africa, have been vastly undercounted.

Between January and June of 2021, the researchers found that 32% of the dead in the morgue tested positive for SARS-CoV-2. The numbers testing positive rose to 82% during one week of Zambia's deadliest wave in June. Most had died at home without seeking treatment, and fewer than 10% had tested positive while living-a criterion health authorities required to count them as part of the official covid-19 toll.

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Although some of the deceased who were infected with the virus likely died from unrelated causes, interviews with relatives and records of those who'd sought treatment for covid-like symptoms before succumbing suggest that roughly 70% of adult dead testing positive were probably" or possibly" victims of covid-19.

And while Lusaka, a city of 3.5 million people at the crossroads of eastern and southern Africa, might not be a perfect proxy for a continent of nearly 1.4 billion, the authors stress that their study's findings are consistent with a growing body of estimates from other countries in the region: the world, they believe, may have grossly underestimated Africa's true covid toll.

Our study punctures the myth that covid-19 skipped Africa," says Christopher Gill, an infectious disease specialist at the Boston University School of Public Health who was one of the study's lead authors.

The Africa paradox

In the pandemic's early months, there were fears that underfunded health-care systems in Africa would be overwhelmed: one UN report from April 2020 predicted between 300,000 and 3.3 million Africans would die that year alone.

Yet as SARS-CoV-2 and its variants spread across the globe, Africa-where HIV/AIDS, malaria, and tuberculosis kill more than a million people each year-appeared surprisingly resilient. Early on, according to Oliver Watson, an epidemiologist at Imperial College London, the region's comparatively small number of international flights and a series of strict lockdowns likely helped to keep the virus's spread in check.

Yet even after most containment measures were relaxed, and antibody studies began to show that SARS-CoV-2 was circulating widely, mortality remained far lower than expected. As of April 7, Africa's 54 countries had recorded just 251,516 official covid deaths-4.1% of the global total, on a continent with 18% of the world's population.

New Leopards Hill cemetery in Lusaka, ZambiaJASON MULIKITA

From the beginning, the apparent Africa paradox" set off a wave of speculation. Those seeking to explain it pointed out that Africa is the world's least urbanized continent, with a climate that enables year-round outdoor gatherings. They also noted that a younger population-Africa's median age is less than 20-was likely more resilient to a disease that hits the elderly the hardest.

Some, like Bruce Kirenga, a respiratory physician who's helped lead the covid-19 response in Uganda, suspect that certain African populations could be less vulnerable thanks to genetics. Others postulate that a lifetime of exposure to different pathogens, including other viruses or parasites endemic to Africa's tropical regions, might confer some level of immunity that protects against severe infection.

Many of these explanations remain plausible, and most epidemiologists believe that Africa's comparative youth is indeed a critical factor. Still, the broader idea that Africa had been skipped" was based on an unlikely assumption: that official country-level death figures were largely correct. In resource-poor settings, experts say, even diseases that have been around for centuries are often subject to significant undercounts. According to the WHO, fewer than a quarter of estimated deaths from malaria are captured by official national statistics-in some cases because diagnoses are missing and in others because the deaths themselves aren't reported.

Something similar probably happened with covid-19. Testing was costly and scarce: more than two years into the pandemic, according to the Africa Centres for Disease Control and Prevention, only one out of 13 Africans, on average, has been tested. In Nigeria, Africa's most populous country, that figure is less than one in 40.

In many middle- and high- income countries, estimates of excess mortality-recorded deaths above a given historical benchmark-were being used to approximate the pandemic's impact if gaps in disease surveillance were apparent. In most of Africa, though, up-to-date death statistics aren't available either. According to Stephane Helleringer, a demographer at New York University who studies mortality, few countries on the continent have an administrative structure near complete enough" to measure deaths in a reliable and timely way.

Swabbing the departed

In Zambia, where death registries are often patchy and testing for covid-19 was hindered by shortages of materials and the stigma that attended a positive result, Gill and fellow lead author Lawrence Mwananyanda suspected that the main cause of the paradox" was a simple lack of data. They happened to be uniquely positioned to pursue this hypothesis. Since 2017, their team had been testing for respiratory disease in infants at the UTH morgue, where 80% of Lusaka's bodies, including those of people who died in health facilities and at home, are brought to receive permission for burial. They had PCR machines, whose price tags had stymied testing efforts elsewhere, as well as seasoned staff who were experts in counseling grieving relatives and getting their buy-in for participation in an academic study.

They also had a funder, the Bill and Melinda Gates Foundation, that was supportive of expanding the project to test bodies of all ages for covid-19. In June of 2020, after tracking down the chemical compounds needed to process samples, the team got to work from a small office near the mortuary's back entrance. At their launch, Zambia had only one officially designated covid-19 death. The first round of their study-which tested 364 corpses between June and September 2020, all within 48 hours of death-detected SARS-CoV-2 in nearly one out of six. Only a handful of the deceased had been tested while alive.

Bodies outside University Teaching Hospital mortuary in Lusaka, ZambiaJASON MULIKITA

Their initial paper, published in the BMJ in February 2021, made a compelling case for their undercounting thesis. Yet it was still based on a relatively small number of dead, so the team returned in 2021 for a longer follow-up. This time, their work coincided with the second and third waves of the pandemic, which hit harder than anything in 2020.

By June of 2021, as the delta variant tore across Lusaka, the morgue's previous volume of a couple of dozen bodies per day had ballooned to nearly 100. The tree-lined cul-de-sac leading to its entrance was deadlocked with traffic. Vendors selling caskets from adjacent shops were running out of stock. It was so depressing," says Benard Ngoma, a 55-year-old clinical research officer who led the team's cadaver swabbing-adding that it brought back memories from the height of Zambia's HIV/AIDS crisis in the early 2000s. That period of 2021 was something else," he says.

The new study made possible by Ngoma's efforts shows that covid-19 was indeed the culprit. In round two, Ngoma and his colleagues swabbed more than 1,100 cadavers, enrolling five to six randomly selected bodies per day, and found positivity more than double what was observed before. This time, half of those who died with covid-19 in hospitals had been tested while alive. But roughly 80% of the bodies testing positive were people who had died at home, and almost none of those had received an official covid-19 diagnosis.

Compared with covid-19 victims elsewhere on the globe, they found, Zambians with the disease were also dying young: the median age of cadavers testing positive was 48, 58% were younger than 60, and 15% were children or adolescents. Both rounds of the study also found a disproportionate number of covid-19 positive deaths coming from the city's compounds-its poorest, most densely populated neighborhoods. According to Ngoma, this contrasted with early perceptions of many living there, who'd insisted the pandemic was something that only afflicted rich people."

These new results, like those published last year, do come with some caveats. Although the study provides a snapshot of how covid-19 hit one African city, it offers little insight into its impact in rural areas, where gaps in both disease surveillance and death registration are the greatest. As the authors admit, its method of inferring whether death of someone who tested positive for SARS-CoV-2 was caused by the disease itself isn't foolproof: family members bringing bodies to the morgue typically aren't medical experts, and the study's verbal autopsies" based on their recollection of symptoms could be subject to some misclassification.

By measuring deaths but not background rates of infection, the study does not attempt to calculate the chances that a Lusaka resident with SARS-CoV-2 will develop a severe infection or die. (A WHO meta-analysis of antibody studies from 14 African countries, which has not yet been peer reviewed, estimates that two-thirds of cases on the continent have been asymptomatic.)

Still, as a rare attempt to probe Africa's death toll with clinical data, the BU team's work has had a significant impact, outside experts say. Before its first paper, says Watson, who's worked on several studies related to covid-19 in low-income settings, there was a fairly equal balance" within academia between those who believed there was something fundamentally different going on in Africa that meant there wasn't that much death occurring" and those who emphasized a lack of data.

The Zambia study, he says, played an important role in shifting the narrative" toward the latter idea. Uganda's Kirenga says the study resonates with his observations of likely undercounting there. But Roma Chilengi, special covid-19 advisor to Zambian president Hakainde Hichilema, who also heads the organization that compiles Zambia's official surveillance data, says he still believes the pandemic hasn't been as deadly in his country as expected: initial fears it would sweep like wildfire," he told me, haven't come to pass. Still, Chilengi broadly agrees with the BU team's conclusions. As an exploratory observation, there's no doubt we had a lot of people who died of covid but were not diagnosed," he says.

Survivors-and algorithms-concur

Beyond the UTH cadavers, a growing body of nonclinical studies has also added heft to the assertion that a majority of Africa's deaths have been missed. A paper published in The Lancet last May, which tracked nearly 6,800 confirmed or suspected covid-19 patients referred to critical-care facilities in 10 African countries, found that fewer than half were admitted and 48% of those who were died within a month. According to the paper's authors, this represents excess in-hospital mortality of 11 to 23 deaths per 100 patients compared with the global average-a figure they link to insufficient staffing and the frequent absence of life-saving interventions like oxygenation and dialysis.

Baron Nkonde in the hospital's lab JASON MULIKITA

Although Zambia was not included in the study, locals told me treatment gaps there were also acute. Sky Banda, a 58-year-old resident of Kaunda Square, a compound named after Zambia's first president, says many community members who fell ill during the height of the pandemic viewed hospital admission as a ticket straight to the mortuary." Most opted for home-based herbal treatments instead.

Onechi Lwenje, a 36-year-old filmmaker who spent a week in the covid-19 ward at UTH during Zambia's second wave in early 2021, says staff were so overwhelmed that some patients would die and not be discovered for hours. Most people who went into that ward never came out," he says.

Although death records from Africa remain patchy, attempts to approximate excess mortality through statistical workarounds also support the theory of substantial undercounting. A machine-learning model developed by The Economist, based on more than 100 indicators that correlate with excess deaths in countries where that data is available, suggests Africa has seen 1.1 million to 3 million excess deaths since the start of the pandemic. A model from the University of Washington's Institute of Health Metrics and Evaluation, included in a paper published by The Lancet in March, puts the number, as of December 2021, at 2.1 million for sub-Saharan Africa alone, with a central estimate for Zambia of 81,000-20 times the official toll of 3,967.

Experts warn that these models, which are built with algorithms largely trained on data from wealthy countries, need to be approached with caution. Still, excess-mortality estimates from South Africa, which are based on actual death records, paint a broadly similar picture. That country's official covid-19 death rate, owing in part to better surveillance, is nearly eight times as high as Zambia's-yet the state-affiliated Medical Research Council estimates that it still undercounts these deaths by a factor of three.

Mwananyanda, a former clinician and researcher who's now a top advisor to Hichilema, believes the two countries have enough in common to suggest that their real rates of covid-19 death are likely similar.

I think what happened in South Africa is exactly what happened here," he says. The only difference is they have a way to collect and make sense of the data and we don't."

Lingering questions

Although the BU team has already made substantial progress in compensating for that data gap, its study has also unearthed some lingering questions. One big unknown relates to the topic of Gill and Mwananyanda's earlier research: pediatric deaths. While most adults who died with covid-19 in their study presented with the disease's usual respiratory symptoms, both rounds found that the majority of young children with covid-19 didn't.

According to Gill, this could be because their deaths were unrelated to the virus. Alternatively, he suspects, SARS-CoV-2 might have a greater pediatric impact in settings where children are often undernourished and afflicted with other ailments than it does in the West, where childhood deaths have been minimal. A third phase of the project, which began in February, will seek to unravel this mystery by conducting biopsies of child cadavers testing positive. It's a totally plausible theory," Gill says, but we have to prove it."

Benard Ngoma swabs corpses at the morgue for signs of covid infectionJASON MULIKITA

Given the pandemic's current trajectory, though, Gill isn't sure whether the team will get the chance. As in much of the world, the arrival of the omicron variant in Zambia last December heralded a big spike in infections. But when I visited the UTH morgue in March, everyone from project staff to shopkeepers selling coffins near the entrance said the latest wave had brought far less death than those that came before. Although only 12% of Zambians are fully vaccinated-health authorities have the supplies but have struggled to combat hesitancy and logistical bottlenecks-many in the country believe the worst of covid-19 has now passed.

Whatever happens, Gill and Mwananyanda expect that a deeper understanding of its impact will continue to emerge: project staff recently spent months scouring burial registries across Lusaka to gather data in support of an excess-mortality analysis meant to provide a clearer sense of how severe the city's undercounting has been.

The forthcoming findings, though, are unlikely to change the broad thrust of the conclusions emerging from the months Ngoma and his colleagues spent among the bodies at UTH: that covid-19 hit Africa hard-and those tracking it simply couldn't keep up.

Jonathan W. Rosen is a writer and journalist reporting from Africa.