Manaus, in Brazil, suffered one of the world's most devastating outbreaks. Now, epidemiologists want to know why.
Ulisses Xavier will never forget the noise. At the peak of the pandemic, when workers in Manaus were forced to abandon individual graves in favour of long trenches excavated with a faded yellow digger, the cemetery's tranquillity was shattered.
"At that time you could barely hear yourself think," the 52-year-old gravedigger recalls.
"There was just the sound of machines working, men digging, families crying. It was relentless."
On the outskirts of Manaus, a sprawling port-city in the heart of the Amazon rainforest, this new clearing at Parque Taruma cemetery is a grim reminder of what can happen if Covid-19 spreads uncontrolled.
On April 10 Francisco da Silva Nascimento was the first to be buried here. Within three days the 63-year-old was joined by 102 others; by April 16 that figure had more than doubled to 250.
From there a sea of wooden blue crosses multiplied as the virus spread like wildfire across an isolated city caught off-guard.
Dates, names and numbers painted on to the wood in thick black lettering are a sober record of just how quickly fatalities mounted.
By April 20, 524 people were buried in the tawny earth; on May 5 that figure stood at 1018. In total, close to 2000 coronavirus victims are in this graveyard alone.
"I've been digging graves for 16 years and I've never witnessed anything like it," says Xavier, who helped bury upwards of 100 people in a single day at the peak of the crisis.
"I still can't stop dreaming about it – well, more like nightmares."
Manaus, home to some 2.2 million people, suffered one of the most devastating outbreaks in the world. On the banks of the Negro River, the city was once an epicentre of the slave-driven rubber trade – then nicknamed "Paris of the Tropics".
Today its shabby colonial buildings are a reminder of the disparities the city was built on, divisions that only worsened Covid's sting.
By some estimates, two-thirds of the population here contracted the disease. And while the city is a fraction of the size of London, its infection rate is four times higher – 2445 cases per 100,000 people, compared to 615 in the capital.
According to data from Amazonas' state government, there have been 54,292 cases and 2662 fatalities in Manaus. But because testing remains limited and cases are often listed as "respiratory disease" rather than Covid-19, experts estimate that there have actually been five times more infections and twice as many deaths.
"Crowded Manaus hospital lives chaos with lack of respirators and people on the floor," said one local newspaper headline in late March, cataloguing the crisis. "Manaus has burials in collective ditches," another lamented in mid-April, shortly followed by "Manaus has stock of coffins for just another five days."
A week later Correio Braziliense reported that a video circulating on social media appeared to show patients in one hospital ward lying next to the dead bodies of at least 10 suspected Covid victims.
"Manaus was taken by surprise," says the city's Archbishop, Leonardo Steiner, sitting in his residence in the centre of town. "There was this denial of the disease, [the government] just said 'no it doesn't exist' ... Certainly we would have seen fewer deaths had the approach been different."
Like so many of the world's most intense outbreaks, the viral storm here followed a party. In late February, as the first 1000 infections were confirmed outside China, the city was engulfed in carnival – the Brazilian festival to mark the beginning of Lent.
Just as those skiing in Europe's soaring Alps felt invulnerable, there was a sense that Manaus would be excluded from the scenes unfolding in faraway places like Wuhan, Iran and Italy.
"People here thought that the climate and the isolated geography would prevent an outbreak," says Lucas Ferrante, a researcher at the National Institute for Research in Amazonia (INPA).
"Even though we saw what was happening around the world, we took too long to take decisions and respond to the threat."
And so the virus – still thought to be thousands of miles away – was the last thing on anyone's mind as they danced in the streets and crammed into bars, sipping caipirinhas and cold beers as the samba bands played.
Three weeks later, on March 13, the Amazonas government detected the state's first Covid-19 case in Manaus – a 39-year-old woman with a recent travel history to London. The authorities insisted that they were well prepared, with a contingency plan already in place to "contain flu-like syndromes".
On March 16 schools were closed, followed by bars and restaurants five days later. But it was already too late; over the following weeks, growing numbers of people arrived at health clinics and hospitals complaining of a cough and fever.
By early April the disease had a firm hold in deprived districts and crowded markets where social distancing was implausible, as well as in the indigenous communities long sidelined by the state.
The hospital system was on the verge of collapse, with ICU occupancy surpassing 100 per cent, while ambulances were forced to leave stretchers and oxygen canisters at the emergency room alongside their patients as resources grew increasingly scarce.
"Our state is no longer an emergency, it is a calamity," Manaus's Mayor, Arthur Virgílio, said frankly at the end of the month, by which point excess deaths stood at 815 – a 325 per cent increase compared to the same week last year.
"All day long we were listening to the sound of ambulance sirens and funeral cars," says Samela Sateré Mawé, who lives with her extended family in a series of narrow buildings in one of the city's poorest districts.
"Two of our neighbours, on either side of us, died from Covid and we could barely isolate. It was terrifying."
Case study of a catastrophe
The scale of the outbreak in Manaus has attracted the interest of epidemiologists around the world.
What made the city so vulnerable? Why did the virus spread so fast? Because the first wave was so explosive, might the city have conferred some protection?
Standing in the glaringly white corridors of the Delphina Aziz hospital – the referral centre for Covid-19 cases in Manaus – the state's assistant secretary for health, Dr Thales Schincariol, insists that the government "did nothing wrong".
Most authorities across the globe struggled to contain the virus, he says. But in the Amazonas high rates of comorbidities, including diabetes and hypertension, made infections more severe – it's no coincidence that all four patients in this wing of the hospital's ICU are obese, Schincariol notes.
He adds that much of the population ignored social distancing rules and regulations mandating face masks. This is in part because many here are Jair Bolsonaro supporters – the country's President has repeatedly downplayed Covid-19 as "little flu".
But the pandemic was also exacerbated by existing disparities; isolating at home was a luxury for the wealthy. For large inter-generational families living together in cramped houses in the poorest districts, social distancing was an almost impossible feat.
Infection control was also a challenge. Just 12 per cent of people in Manaus have access to sewage collection, according to the Brazil Institute, while 10 per cent (some 228,000 people) do not have running water.
Add to that list an already stretched healthcare system and you have a "perfect storm", says Ferrante. While Brazil has an average of 2.1 doctors per 1000 people, this drops to 1.2 in Amazonas, where there are just 919 ICU beds for 4 million people.
"Even before Covid the biggest hospital was around 80 per cent full," says Dr Alessandra Said, a doctor with the federal ambulance service, SAMU.
"On a busy Saturday night, when there was lots of drinking or accidents, the emergency room would hit 90 to 95 per cent occupancy.
"So if we are already that full without a pandemic – imagine how it is with Covid," she adds. "Even within three to five days of it arriving, hospitals were full."
According to the Archbishop, decades of opportunism are to blame for inadequate resources. "Brazil probably has one of the most complete health systems in the world," he says, referring to the country's public healthcare system, Sistema Único de Saúde, which was inspired by the UK's NHS.
"But it doesn't work because of corruption. If people weren't robbing the system, we would certainly have seen fewer deaths and cases in Manaus," he adds.
At least 11 states in Brazil have open investigations into corruption scandals – including Amazonas. The Governor, Wilson Lima, has been accused of misusing emergency purchase powers to buy overpriced ventilators from a wine importer.
Meanwhile, disjointed policies between the city and state governments have triggered confusion, not helped by a conveyor belt of health secretaries (three between April and July), the Archbishop adds.
The authorities have also been accused of neglecting indigenous communities. In Parque das Tribos, an informal settlement on the outskirts of Manaus home to some 450 families from 35 ethnic groups, Joilson Karapana estimates that 60 to 70 per cent of residents had Covid symptoms.
Joilson himself lost his father and his closest friend – Messias Kokama, the cacique, or chief of the community. "It hurts," he says, sitting in the school room attached to his small home. "I can't express how much it hurts. Sometimes it feels impossible to overcome."
Yet, in spite of little aid from the government, the overall death toll in Parque das Tribos was lower than it might have been. This was partly because the population is relatively young, but the community also took decisive action to stem infections.
"I knew we had to look after ourselves," says Vanda Ortega, a community nurse who led the charge against Covid.
In March, she created videos about the importance of handwashing and shared them throughout the neighbourhood. She bought reusable face masks so people with symptoms wouldn't infect others and treated those she could at their homes.
When the conditions of patients deteriorated, it was Vanda who convinced them to go to hospital before it was too late.
"I feel emotional as, looking back, it was a huge responsibility. Especially because many people here were nervous about going to hospital – I had to persuade them they weren't going there to die," the 33-year-old says.
People here believe that without her, the situation would have been far worse.
Along the Amazon, many other indigenous communities were less fortunate, as the virus spread from Manaus to isolated towns and villages via crowded boats.
According to a preprint published on MedRvix, the six Brazilian cities with the highest exposure to Covid-19 are all on the winding river, while indigenous people have been roughly six times more likely to be infected with Covid-19 than white people.
Some critically ill patients in these villages made it to an ICU in Manaus via boat or plane, including Marie Amorim. The frail 79 -year-old has spent 13 days in the Delphina Aziz hospital, having travelled five hours along the Amazon in a speed boat.
But for most, accessing care was an "immense" logistical challenge due to the vast distances involved, says Gabriela Romero, a spokeswoman for Médecins Sans Frontières who spent several months working in Tefé – a riverside town some 480 kilometres west of Manaus.
"Indigenous peoples weren't more susceptible to Covid, but existing inequalities put them at greater risk once they did contract the disease," she adds.
Yet, precisely because of the scale of the devastation unleashed across Amazonas, the state's assistant health secretary is confident that a "second wave" is not imminent.
This theory is based on a study led by the University of Sao Paulo's Institute of Tropical Medicine, which tested recent blood bank donations for Sars-Cov-2 antibodies.
Researchers found that the city had an "unusually high" infection rate – from May to August between 44 and 66 per cent of people contracted Covid-19.
According to the paper, which was published as a preprint and is yet to be peer reviewed, "herd immunity played a significant role" in declining cases in August – the virus ran out of people to infect.
"Obviously I'm not comfortable knowing that the virus is still around, but studies suggest two-thirds of the Manaus was already infected," Schincariol says.
"We don't know the exact figure for herd immunity, but because we've crossed the 50 per cent mark we don't expect a second wave.
"Of course we're preparing, but we don't have any cases of reinfections in Amazonas."
Yet many experts here are incredulous at what they see as yet another example of government complacency. They stress that Sao Paulo University's study makes no mention that the high infection rate could prevent a resurgence and notes that immunity may only be temporary.
"Now we're seeing complacency take place again," says Fernate. "But instead of geography and weather, we're using herd immunity as an argument for why we don't need to act.
"It's absurd – especially when other models, like ours at INPA, estimate the infection rate was more like 20 per cent," he adds, warning that cases are ticking slowly upwards.
On September 1 the seven-day rolling average for new infections in Amazonas state stood at 565, according to an analysis of data from Brasil.io. By October 1, this average had risen to 850.
While the weekly average is still well below the peak – Amazonas saw around 1600 new cases a day in early May – there are growing signs that the health system is already straining under the renewed pressure, while the city and state government are at odds over whether to impose a new lockdown.
'Preparing to do it all again'
The red sirens wail as the ambulance darts across Manaus's south zone, dodging vehicles and skipping traffic lights. Inside Dr Said and her colleagues, clad head to toe in bright blue PPE, fight to keep a patient's condition constant.
The 58-year-old man is struggling to breathe – his symptoms have been worsening for a week. After he walked into a basic health clinic doctors quickly concluded that he needed intensive care.
But when the ambulance reaches one of Manaus's largest hospitals, 28 DeAgosto, doctors there have already run out of the oxygen the man desperately needs.
"It feels like we've been through this agony before," says Said. "Now I'm preparing my spirits to do it all again – and again and again and again ... "
At the graveyard, too, the work hasn't stopped. Harsh scrapes of shovels against the ochre earth reverberate as two men in bright green protective suits unceremoniously bury yet another coronavirus victim.
Iris Goncalves Alves, aged just 54, is the 1950th Covid casualty in this sloping site at Parque Taruma cemetery. Fallen trees on its perimeter are a reminder that until the pandemic hit, this plot was covered in thick foliage, rather than hundreds and hundreds of graves.
While most victims are memorialised with a simple blue cross – which bunch together where the mechanical diggers excavated long trenches for mass burials – some graves are marked only by a mound of dirt. The crosses cost 80 Brazilian reals, roughly NZ$22, and many families couldn't afford them.
Alves' relatives, however, have spared no expense. Her burial, for this is barely a funeral, is sparse; there are no comforting words from a priest, no eulogy from her children. But her engraved wooden coffin is polished, with a small perspex window so her family can see her face one final time before she disappears into the ground.
The site becomes eerily quiet as the gravediggers finish and lay down their shovels, chucking their surgical gloves to one side. The still is punctured only by birdsong and the occasional sob as the family say their final, low-key goodbyes.
Ulisses prays for the relative calm to remain. "In April the noise was non-stop, the work was non-stop," he says, sweat dripping down his brow in the heat. "We can only ask God to spare us now."