The northern Italian province became one of the deadliest killing fields for the virus in the Western world. But a Times investigation found that faulty guidance and bureaucratic delays rendered the toll far worse than it had to be.
BERGAMO, Italy — When Franco Orlandi, a usually hale former truck driver, arrived in mid-February with a cough and fever at an emergency room in the northern Italian province of Bergamo, doctors determined that he had a flu and sent him home. Two days later, an ambulance brought the 83-year-old back. He couldn’t breathe.
Italy had not recorded a single domestic coronavirus case, but Mr. Orlandi’s symptoms puzzled Monica Avogadri, the 55-year-old anesthesiologist who treated him at Pesenti Fenaroli Hospital. She didn’t test him for the virus because Italian protocols, adopted from the World Health Organization, recommended testing only people with a link to China, where the outbreak had originated.
When she asked whether Mr. Orlandi had a connection to China, his wife seemed befuddled. They hardly ever ventured beyond their local cafe, Patty’s Bar.
‘‘China?” Dr. Avogadri recalled Mr. Orlandi’s wife responding. “She didn’t even know where it was.”
What Dr. Avogadri did not know was that Covid-19 had already arrived in her region of Lombardy, a discovery made five days later by another doctor in nearby Lodi who broke the national testing protocol. By then, Dr. Avogadri, hamstrung by those same protocols, had herself fallen ill after days caring for Mr. Orlandi and other patients. Her hospital, rather than identifying and treating the disease, was accelerating its spread across Italy’s economic heartland.
Bergamo became one of the deadliest killing fields for the virus in the Western world, a place marked by inconceivable suffering and a dreadful soundtrack of ambulance sirens as emergency medical workers peeled parents away from children, husbands from wives, grandparents from their families.
Hospitals became makeshift morgues and produced parades of coffins and scenes of devastation that became a warning to officials in other Western countries of how the virus could rapidly overwhelm health systems and turn infirmaries into incubators.
Officials confirmed that more than 3,300 people died with the virus in Bergamo, though they said the actual toll was probably double that. Mr. Orlandi’s town, Nembro, became perhaps Italy’s hardest struck, with an 850 percent increase in deaths in March. So many, the local priest ordered a stop to the incessant tolling of the bells for the dead.
The question of how such a tragedy could unfold in Bergamo, a wealthy, well-educated province of just more than a million, with top-level hospitals, has remained an uneasy mystery, a blood stain that the government prefers to avoid as it points with pride to Italy’s success in flattening the first wave of infections.
Image A Mass remembering Covid victims at a Bergamo cemetery on Nov. 2. Red Cross workers helped a woman who felt ill that day. Unchecked, the virus spread everywhere. At one Bergamo nursing home, 34 of 87 guests died.
The World Health Organization’s guidance on testing engendered a misplaced sense of security and helped blind doctors to the spread of the virus. But missteps and inaction after Covid-19 exploded into view aggravated the situation and cost Bergamo — and Italy — precious time when minutes mattered most.
The director of Pesenti Fenaroli Hospital closed its doors almost as soon as he realized he had an outbreak. But regional officials ordered them opened hours later. Hospital workers, visitors and discharged patients were exposed to the virus, and then moved through the province.
For days, there was an expectation that the national government would lock down towns in Bergamo, as it had earlier done immediately and decisively in Lodi. Some mayors in Bergamo waited anxiously for the police to seal the borders, even as many business and local leaders expressed reluctance.
Italy’s prime minister, Giuseppe Conte, publicly turned to a committee of scientific advisers, which formally proposed that he follow the example of Lodi and shut down the newly infected towns in Bergamo. Privately, though, national business lobbies urged him not to close the area’s factories.
Ultimately, after critical days filled with bureaucratic dithering, as well as spats between Rome and the regional authorities, the government decided the time to save Bergamo had passed.
With the virus out of control in the province and clusters emerging all around it, the government waited longer but then went bigger. Two weeks after Mr. Orlandi had tested positive, Italy locked down the whole region. Then the country. But Bergamo was lost.
Now that the coronavirus, deep into its second wave, has washed across the globe and left virtually no nation untouched, it is easy to forget how alone among Western democracies Italy was in February, confronted with a threat for which it had no playbook.
Throughout flu season, some local family doctors in the Lombardy region had noticed strange pneumonia cases and were prescribing more scans than usual. The region has business ties to China, and local infectious disease doctors had kept an eye on the coronavirus outbreak in the city of Wuhan. They also trusted Italy’s new and narrower protocols, adopted from the W.H.O. at the end of January, which essentially limited testing to people linked to China.
But hardly any of the pneumonia patients had such a link, which meant that the few people being tested were mostly air travelers. All had come back negative.
Transferring a coronavirus patient from the Bolognini Hospital in Seriate to a better equipped hospital in the Bergamo province. Praying in the Alzano Lombardo church. By March the virus had ravaged the province.
Then, on Feb. 20, Annalisa Malara, a doctor in the town of Codogno, in Lodi province, decided to break the protocol and test a 38-year-old man with serious pneumonia who was not responding to standard treatments. The man’s test came back positive that same evening and he became Italy’s first known locally transmitted case of Covid-19.
Two days later, on the outskirts of Rome, an emergency meeting was held at Italy’s Civil Protection Agency, the national disaster relief body. Crammed into a small conference room, Mr. Conte sat at the head of an oval table, surrounded by his ministers, as Italy’s health minister, Roberto Speranza, proposed a dramatic lockdown of towns in the Lodi area.
The ministers, exchanging nervous looks, unanimously agreed and the government dispatched Italy’s police and army to seal the borders on Feb. 23 — a decision that it cites to this day as the metric of its boldness and willingness to put Italy’s public health over its economy.
Mr. Speranza weighed the momentous decision carefully, deciding it was better to err on the side of caution.
‘‘I was playing with the lives of people,” he said, adding that in the story of the pandemic, “It was the first time in the history of Western countries that we were locking down and taking away the freedom of the people.”
The discovery of the virus in Lodi, just 60 miles from Bergamo, struck Dr. Avogadri, sick in bed at home, with the force of a revelation.
She picked up the phone on Feb. 21 and called her colleagues at Pesenti Fenaroli, in the town of Alzano Lombardo in Bergamo’s industrial and densely populated Serio river valley. She urged them to test her patient, Mr. Orlandi.
At first, they ridiculed her, noting that he’d never been anywhere near China. But other patients on the same floor were deteriorating, and another man with suspicious symptoms soon arrived in the emergency room. Hospital officials decided to swab test him and one of Mr. Orlandi’s roommates.
By midday on Feb. 23, the results were brought to Dr. Giuseppe Marzulli, the hospital director. Both tests were positive.
Dr. Marzulli grilled the reporting doctor about whether the staff had adequately investigated connections to China. They had. There weren’t any. The virus was already circulating in their midst.
“It was at that moment I understood we were screwed,” Dr. Marzulli said. “We had looked for who had been in China, and this was the tragic error.”
They swabbed Mr. Orlandi that day, as members of his family moved through crowded corridors of the third floor.
Some visitors noticed staff members coughing.
Red Cross workers helping a patient in Pradalunga, another area in the Serio river valley, in March. Dr. Giuseppe Marzulli, the former director of the Pesenti Fenaroli hospital, tried to shut its emergency room after finding cases in late February. He was swiftly ordered to reopen.
Given the government’s swift action in Lodi, Dr. Marzulli began to prepare for a lockdown. He canceled shift changes so that no new personnel would come in, and he closed the emergency room, mindful that the hospital had only about a dozen swabs to perform coronavirus tests.
“We didn’t have swabs. It was the biggest problem we had,” he said.
Hours later, the region and the Bergamo hospital network overseeing Pesenti Fenaroli decided together to reopen the emergency room over Dr. Marzulli’s objections.
Aida Andreassi, a senior Lombardy health official, said the emergency room had been sanitized and the hospital represented an “indispensable garrison” for a region that needed all its medical facilities.
But without enough swabs, Dr. Marzulli said, the hospital was defenseless.
On Feb. 24, Mr. Orlandi’s test results came back. He was positive, too. By then, about 50 more patients had arrived at the emergency room with symptoms, quickly burning through the hospital’s stock of swabs, Dr. Marzulli said.
A doctor, who tested Dr. Avogadri with one of the available swabs, pressed hospital officials for more tests, reminding them in a frantic email that they had “symptomatic colleagues who have not been swabbed.”
His superiors pleaded with another hospital in the region for 100 swabs, according to email correspondence seen by The New York Times. But Dr. Marzulli said only half of them made it to Pesenti Fenaroli, on Feb. 26.
He scrambled, separating patients with symptoms from those without, and sending home visibly sick staff members. But many patients who came in contact with the virus stayed put, while their nurses and doctors kept circulating.
On Feb. 27, documents provided by Lombardy show, the region sent hundreds more swabs to the Bergamo hospitals. But they didn’t arrive at Pesenti Fenaroli right away, Dr. Marzulli said.
He was forced to ration out a couple dozen swabs a day until March 1, when he himself fainted from exhaustion with the virus.
“If we have to identify a spark,” Giorgio Gori, the mayor of Bergamo city said as infections devastated his town, “it was the hospital.”
The small towns around the hospital increasingly became central to a drama playing out between Bergamo and Rome.
On Feb. 25, Bergamo province reported just 18 cases compared to 125 in Lodi. Lombardy’s top health official expressed concern about contagion at Pesenti Fenaroli Hospital but said, “It’s early to say if it’s another cluster.”
In Rome, Mr. Conte discouraged expanding testing, reasoning that health officials had to follow international protocols, “otherwise we would end up dramatizing” the emergency.
On Feb. 26, with 20 reported cases in Bergamo, Rome’s scientific committee said it didn’t see any flare-ups that required a lockdown. Claudio Cancelli, the mayor of Nembro, said Bergamo’s health officials threatened to cut off funding to the area’s 18 mayors if they closed centers for the elderly or disabled.
The next day, he said, they assured the mayors, “Don’t worry. There is no red zone foreseen.”
But on Feb. 28, Bergamo’s caseload had jumped to 103, against 182 in Lodi. At a Lombardy regional news conference, leading doctors identified the Pesenti Fenaroli Hospital as the outbreak’s source.
Confindustria Bergamo, the province’s industrial association, responded that same day by posting a video titled, “Bergamo Is Running.”
“Current health warnings from Italian government officials are that the risk of infection is low,” the narrator stated. The images showed factories humming.
That message resonated with Simona Ghilardi, who ran a national transport and logistics company in Nembro, about a mile from Pesenti Fenaroli Hospital. Colleagues in locked-down Lodi had told her about losing clients. Stopping industry in Bergamo was unthinkable to her.
“When you are born here the first thing they tell you is — you have to work,” she said.
Industrial leaders in Bergamo province lobbied the government not to close factories. Despite the concerns of industry, government leaders said they were guided by science alone in their decision making.
As talk of a lockdown persisted, she looked out onto her vast warehouse filled with stacks of grocery store circulars, bags of chemical products and crates of detergent to ship to China. “The factory has to survive too,” she said.
Business leaders, and even the Alzano Lombardo mayor, resisted a lockdown, telling the local newspaper that it would be a tragedy for the economy and contacting their commercial associations with influence in Rome.
In the capital, Mr. Conte stressed that he would be guided by science alone. He declined interview requests for this article but has denied ever receiving requests from Confindustria as his government weighed what to do in Bergamo.
The powerful industrial group’s own representatives said they made their requests clear.
“There was a direct line between Confindustria and the government at that time,” said Licia Mattioli, who was then the group’s vice president.
The leadership argued directly to Mr. Conte that the rapid lockdown of the factories in Lodi unnecessarily cost jobs and that in Bergamo’s factories steps like social distancing would be sufficient.
“What they were saying was that to stop all the industry, also locally, is really very, very dangerous,” she recalled.
“I don’t know if they understood,” she said of Mr. Conte and his ministers. “But they listened at least.”
The factories stayed open until late March, and many never closed.
“I can assure you that never, never, never we made considerations on this,” said Mr. Speranza, the health minister. “We decided since the beginning that the first point is health — everything else comes after.”
On March 3, the government’s scientific committee proposed a red zone around Nembro and Alzano Lombardo. The Lombardy authorities considered it a done deal. So did Mr. Cancelli, the Nembro mayor, who was now infected and working in isolation.
“This place should have been closed in February, when it became clear that there were officially declared cases in the hospital, that surely were in contact with health workers, relatives, other patients,” Mr. Cancelli said. “On March 3 we thought, ‘Now they will close tonight.’”
But Mr. Conte, who needed to approve the decision, has said that he didn’t hear of the plan for two more days.
A nurse during her night shift at Papa Giovanni XXIII hospital in Bergamo in November. Health care workers have braced for a second wave with dread. A stretcher in the courtyard of the Pesenti Fenaroli hospital, which found itself at the center of the province’s outbreak.
In the meantime, Mr. Speranza said, he pressed the scientific committee for a report on their rationale for closing the towns. “They said only ‘Close,’” Mr. Speranza said. “You can’t say, ‘I take away the freedom of people,’ for two words.”
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Words to Know About Testing
Confused by the terms about coronavirus testing? Let us help:
- Antibody: A protein produced by the immune system that can recognize and attach precisely to specific kinds of viruses, bacteria, or other invaders.
- Antibody test/serology test: A test that detects antibodies specific to the coronavirus. Antibodies begin to appear in the blood about a week after the coronavirus has infected the body. Because antibodies take so long to develop, an antibody test can’t reliably diagnose an ongoing infection. But it can identify people who have been exposed to the coronavirus in the past.
- Antigen test: This test detects bits of coronavirus proteins called antigens. Antigen tests are fast, taking as little as five minutes, but are less accurate than tests that detect genetic material from the virus.
- Coronavirus: Any virus that belongs to the Orthocoronavirinae family of viruses. The coronavirus that causes Covid-19 is known as SARS-CoV-2.
- Covid-19: The disease caused by the new coronavirus. The name is short for coronavirus disease 2019.
- Isolation and quarantine: Isolation is the separation of people who know they are sick with a contagious disease from those who are not sick. Quarantine refers to restricting the movement of people who have been exposed to a virus.
- Nasopharyngeal swab: A long, flexible stick, tipped with a soft swab, that is inserted deep into the nose to get samples from the space where the nasal cavity meets the throat. Samples for coronavirus tests can also be collected with swabs that do not go as deep into the nose — sometimes called nasal swabs — or oral or throat swabs.
- Polymerase Chain Reaction (PCR): Scientists use PCR to make millions of copies of genetic material in a sample. Tests that use PCR enable researchers to detect the coronavirus even when it is scarce.
- Viral load: The amount of virus in a person’s body. In people infected by the coronavirus, the viral load may peak before they start to show symptoms, if symptoms appear at all.
The interior ministry notified Bergamo’s military police to begin preparations for a lockdown, according to Col. Paolo Storoni, then the head of the Carabinieri in the area. Carmen Arzuffi, the owner of Hotel Continental, said the local police prefect called on March 4 to book 50 rooms for 100 incoming officers.
On March 5, the scientific committee again urged the government to lock down the towns. Mr. Speranza said he sent Mr. Conte the report that night. A member of Parliament from Bergamo privately pressed Mr. Conte’s office about what was taking so long, arguing that a human catastrophe was unfolding.
Mr. Conte’s office replied, according to correspondence seen by The Times, that there would be a ministerial-level meeting on Saturday, two days later, and that no decision would come before then.
By March 6, law enforcement had begun setting up at the hotel.
The police filled the hours by inspecting the routes they were supposed to close off and holding briefings in the basement, with commanders drawing maps of the towns and their streets on an easel.
“They knew it all by heart,” Ms. Arzuffi, the hotel owner, said.
As they ran drills, Mr. Conte met on March 6 with the scientific committee in Rome yet again. According to Mr. Speranza, the committee told Mr. Conte that closing Bergamo was no longer the issue. All of Lombardy, including Milan, needed to be locked down.
Two days later, on March 8, Mr. Conte did just that.
Mr. Conte has portrayed himself as urging the scientists to think bigger and bolder, saying he told them, “Shouldn’t we think of more radical measures?”
Later that day, the police officers at the Hotel Continental packed up and left.
“Nothing happened,” Mr. Cancelli said.
As the authorities decided what to do, the virus seemed to spread everywhere and touch everyone. Infections ravaged homes and apartments. People started dying.
Mr. Orlandi, the burly truck driver who had once delighted the children in his family by thumb wrestling them with his gaping hands, died the day after his family learned he had contracted the virus. Some of his family became infected and died, too.
Giuseppa Nembrini, 82, and Giovanni Morotti, 85, a married couple in two separate rooms down the hall from Mr. Orlandi, both died.
Angiolina Cavalli, 84, a patient across the hall, died as well. Her husband, Gianfranco Zambonelli, 85, who had visited the hospital, died of the virus, too.
“They never told us anything,” Francesco Zambonelli, their son, who also contracted the virus, said of the hospital. “I think without knowing it, we became a vehicle for contagion to others.”
Francesco Zambonelli’s mother died at Pesenti Fenaroli Hospital. Both he and his father, who died of coronavirus, visited her and contracted the virus. The empty stadium of the Atalanta soccer club in Bergamo. Just before the outbreak was detected, some 40,000 Atalanta fans traveled to Milan for a big European game.
Some of the sick included Bergamo soccer fans, 40,000 of whom had commuted to Milan on Feb. 19 to cheer for their local team, Atalanta, in a Champions League match against the Spanish team Valencia.
“We were stuck one next to the other,” recalled Matteo Doneda, 49, a rabid fan of Atalanta, who sang at the game, “You’ll know when we do damage! We are Bergamaschi, and we know no limits!”
On Feb. 26, Mr. Doneda said cookies began “tasting like sand” and his wife drove him to a hospital. He could barely walk and soon found himself breathing from within an oxygen helmet, surrounded by elderly people gasping for air. He said some of them had broken jaws under their masks, from fainting and falling in the ward.
Dr. Avogadri declined and lost consciousness, eventually drifting into a semi-comatose state in an intensive care ward, as she lost half of her hair. “I wanted to die,” she said.
When she was finally discharged, she discovered that the doctor who managed to find her a swab at Pesenti Fenaroli Hospital had died and that her older sister, who lived nearby, lay in an intensive care unit, a breathing tube down her throat.
All the authorities involved now recognize Bergamo’s losses as a tragedy. But invariably they lay blame for it elsewhere.
The World Health Organization says that it limited its case definitions for practical reasons, primarily not to waste resources at the outset of an uncertain contagion. The rationale, said Dr. Margaret Harris, a spokeswoman for the organization, was “to limit the testing to a specific population at risk.” It is a position that past W.H.O. officials considered reasonable.
But Dr. Harris also argued that when the agency updated the guidelines at the end of January, it made clear “that the patient’s doctor is the one, ultimately, to decide who to test.”
Doctors in Bergamo considered that a convenient caveat.
The guidance was “the thing that generated the huge problem of the spread of the pandemic,” Dr. Avogadri said. “It was a big limitation.”
Dr. Monica Avogadri, who pushed her colleagues to break protocol and test one of her patients for coronavirus, was sickened badly by the virus herself. In Bergamo last month. The Italian government has introduced a series of restrictive measures throughout the nation to contain the second wave of the virus.
The W.H.O. “made a mistake,” said Giuseppe Ruocco, Italy’s chief medical officer and a senior official in its health ministry, adding that if Italy hadn’t automatically followed the organization’s lead it “could have certainly avoided cases and the infection of medical staff.”
In June, Italy bestowed a knighthood in the Order of Merit of the Italian Republic on Dr. Malara, the physician who exposed the outbreak by disregarding the protocol.
Local officials and bereaved families in Nembro and Alzano Lombardo argue that closing the towns in February would have slowed the spread. A local prosecutor is investigating what happened and what didn’t happen and why.
But the government would prefer to focus on its closing of Lodi and then the region.
“It’s two small towns that everyone now knows,” Mr. Speranza, the health minister, said when asked how it was possible the prime minister didn’t know for three days about the shutdown proposal in Bergamo. “But it’s two small towns.”
And Mr. Conte has dismissed questions about the boldness of his decision making.
“There was no delay,” he has insisted.
Today Bergamo is a province gutted by loss.
Earlier this month, the Rev. Matteo Cella, who performed many abbreviated funeral rites for families he knew, greeted widows and widowers, sons and daughters, nieces and nephews on the Day of the Dead.
Wearing blue surgical masks, they leaned against the gravestones of their loved ones, or alongside the wood crosses of the unfinished graves of coronavirus victims.
Father Cella and other prelates read the names of the 231 people who had died in Nembro since the previous November. At least 188 had succumbed to Covid-19. They read the name of Mr. Orlandi, and of the other patients and doctors and visitors with whom he shared the third floor of the hospital during his final days.
As the mourners followed the priests in prayers, some wandered to the mausoleum wall at the back of the cemetery. Familiar names filled the wall.
“Franco Orlandi,” read one. “1-3-1936 – 25-2-2020.”
In Nembro, where the mortality increased 850 percent, clergy read out the names of the dead during a Mass on Nov. 1, All Saints’ Day. A Covid-19 patient undergoing rehabilitation being helped to walk by a nurse at the Bolognini hospital.
“It’s still astonishing,” said Luigia Provese, 81, who drank coffee at the same bar as Mr. Orlandi and said that three of the four people she played cards with had died from the virus. “These are all people I know.”
As the virus has exploded again throughout Italy, Bergamo’s massive infection rate during the first wave, doctors say, has given it a measure of immunity. Its hospitals, once an exporter of infection and the sick, are taking patients in from the surrounding areas.
On Nov. 2, Bergamo’s fairgrounds debuted as a newly converted intensive therapy ward. Dozens of beds radiated wires. Ventilators stood on standby. A team of nurses in hazmat gear huddled for a briefing about reserve oxygen tanks.
Their coordinator, Lauretta Rota, 56, looked on in disbelief.
“It took some time to believe this was happening all over again,” she said. “There is an emotional and physical exhaustion that comes with that knowledge of what we have to face.”
Her cellphone rang.
“OK,” she said, excusing herself. “The first patient is on the way.”
Emma Bubola contributed reporting from Bergamo and Rome.