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THE WASHINGTON POST

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Coronavirus death toll: Americans are almost certainly dying of covid-19 but being left out of the official count

By Emma Brown, Beth Reinhard and Aaron C. Davis
April 5, 2020 at 11:05 AM EDT



The fast-spreading novel coronavirus is almost certainly killing Americans who are not included in the nation's growing death toll, according to public health experts and government officials involved in the tally.

The U.S. Centers for Disease Control and Prevention counts only deaths in which the presence of the coronavirus is confirmed in a laboratory test. "We know that it is an underestimation," agency spokeswoman Kristen Nordlund said.

A widespread lack of access to testing in the early weeks of the U.S. outbreak means people with respiratory illnesses died without being counted, epidemiologists say. Even now, some people who die at home or in overburdened nursing homes are not being tested, according to funeral directors, medical examiners and nursing home representatives.

Postmortem testing by medical examiners varies widely across the country, and some officials say testing the dead is a misuse of scarce resources that could be used on the living. In addition, some people who have the virus test negative, experts say.

As a result, public health officials and government leaders lack a complete view of the pandemic's death toll as they assess its course and scramble to respond.

Scientists who analyze mortality statistics from influenza and other respiratory illnesses say it is too early to estimate how many fatalities have gone unrecorded. For a disease with common symptoms such as covid-19, they said, deaths with positive results almost certainly represent only a fraction of the total caused by the disease.

"You can't rely on just the laboratory-confirmed cases," said Marc-Alain Widdowson, an epidemiologist who left the CDC last year and now serves as director of the Institute of Tropical Medicine Antwerp in Belgium. "You're never going to apply the test on everybody who is ill and everybody who dies. So without doubt - it's a truism - the number of deaths are underestimated globally because you don't apply the test."

Clay Marsh, West Virginia's "coronavirus czar," acknowledged that the state's count is presumably incomplete. West Virginia was the last state to report a case of the virus and had recorded only two deaths as of Saturday.

"Based on the best recent information about limited testing and sizable false negative rates of testing, we are likely underestimating the number of deaths," said Marsh, vice president and executive dean for health sciences at West Virginia University. The count is also low in West Virginia, Marsh said, because the state has a small, rural population and had closed schools and nonessential businesses early.

The CDC has launched an effort to use national data on illnesses, hospitalizations and death certificates to estimate covid-19 infections and deaths. The agency already publishes such estimates weekly for flu, where laboratory-confirmed cases and deaths similarly represent only a fraction of the total attributable to the disease.

"We're probably getting more information on covid-19 because there's a greater awareness in the community of what it is," Nordlund said.

The CDC's official death count, which is based on reports submitted by states, stood at 6,593 as of Saturday. Because of a lag in reporting, the number was significantly lower than the more frequently updated counts by media organizations and university researchers. The Washington Post's count of fatalities surpassed 8,000 on Saturday.

The federal government's death count is broadcast around the world daily as an indicator of how quickly the virus is spreading and how profoundly the nation is struggling. It has clear political implications for President Trump, whose approval ratings rose in late March despite his having downplayed the virus's dangers for weeks.

On Wednesday, the White House estimated that 100,000 to 240,000 Americans may be killed by covid-19, far exceeding the nearly 60,000 combat troops killed in the Vietnam War. Scientists said they did not know how the White House had arrived at its projection, and the White House has declined to provide details.

The death toll has become a heavily politicized benchmark. Trump's defenders say the official number is inflated because it includes all deceased people who tested positive for covid-19, even if there was another cause of death, such as a heart attack or an accident.

Marc Lipsitch, a professor of epidemiology at Harvard, said there are probably some people dying with covid-19 who are not dying of covid-19. Such misattribution is a problem for any cause of death, he said, but it is a minor issue that is "swamped by the opposite problem: deaths that are caused by covid but never attributed, so the death count is underestimated."

Around the globe, public officials are questioning whether the numbers of deaths officially attributed to the virus are deceptively low.

In northern Italy, the town of Nembro recorded 31 deaths from the virus from January to March. But Mayor Claudio Cancelli recently said the total number of deceased in that time period - 158 - was four times higher than the average for that time of year.

"The difference is enormous and cannot be a simple statistical deviation," he wrote in a newspaper article co-authored with a medical executive.

The number of deaths in France attributed to the virus soared last week after officials began including previously unreported deaths in nursing homes, boosting the count by more than 2,000.

Observers inside and outside China, where the virus first appeared late last year, have accused the ruling Communist Party of reporting artificially low infection and death rates. Media outlets, including The Post, have reported that a count of cremation urns ordered to Wuhan, in central China's Hubei province, indicates that far more people died of covid-19 than the official death toll of about 2,500.

Trump said Wednesday that China's "numbers seem to be a little bit on the light side, and I'm being nice when I say that." Chinese officials denied the accusation, saying U.S. officials were trying to deflect responsibility for the American body count.

Studies of influenza have found that, in the middle of a pandemic, real-time fatality counts are often misleading.

Widdowson, the former CDC scientist, was part of a team that estimated global deaths from the 2009 H1N1 swine flu pandemic. The World Health Organization recorded 18,631 people with laboratory-confirmed diagnoses dying of that disease. But the pandemic probably caused 15 times as many deaths, the CDC team concluded in 2012.

A 2013 study by government and academic researchers suggested that lab-confirmed H1N1 deaths in the United States represented only 1 in 7 fatalities attributable to the disease.

In the United States, federal and state public health officials for weeks refused to test people unless they met strict eligibility criteria. Testing is more broadly available today, but some experts say the tests may not detect everyone with the virus. Precisely how common false negatives are is unclear.

Postmortem tests for covid-19 are happening unevenly across the country, experts said. Medical examiners, coroners and health-care providers should "use their judgment" to decide whether such testing is appropriate, according to CDC guidelines.

In addition to the 6,593 lab-confirmed deaths, the CDC on Friday reported that death certificate data shows 1,150 people have died of covid-19.

The numbers differ in part because of a lag in reporting, and because the code for recording covid-19 as a cause of death was not announced until March 24, weeks after the first known case of an American dying of the disease caused by the coronavirus. Death certificate data will be part of the CDC's new effort to estimate total covid-19 fatalities.

To estimate the total fatalities from a disease, scientists often look at "excess deaths" - the number of deaths over and above the average number during a particular period.

The most robust estimates require national statistics that in the United States can take two or three years to compile, according to Cécile Viboud, a National Institutes of Health scientist who co-authored the study estimating the U.S. undercount during the H1N1 flu.

The number of initially uncounted flu deaths typically includes people with pneumonia and other respiratory symptoms who were never tested for influenza, as well as a larger number of people who contract the flu and are left more susceptible to dying from such conditions as cardiac arrest, stroke and diabetes. Those people may not be reported as dying of the flu, but the flu still contributed to their deaths.

Scientists do not yet know whether or how often covid-19 is killing people with these kinds of secondary problems. But it is clear that covid-19 can cause non-respiratory symptoms, scientists say.

Last week, a group of Italian scientists published a study of a 53-year-old otherwise healthy woman who had arrived at a hospital complaining of extreme fatigue. She was suffering from acute heart problems, including inflammation of the heart muscle. She tested positive for the coronavirus.

In Albany, Ga., home to one of the nation's most explosive outbreaks, funeral director Jeffery F. Wakefield Sr. said he treats every body as if it is infected with the virus. Wakefield recently handled the body of a young man, around 40 years old, who died at home alone and was not found for several days. The man's death was attributed to cardiac arrest. He was not tested for the coronavirus.

"We'll never really have true, true numbers," Wakefield said. "We'll get almost close, but we'll never have the true numbers of who died from this."

Epidemiologists say that patients who need medical treatment for conditions other than covid-19 may also suffer and die in places where the health-care system becomes overwhelmed by the virus.

Even as testing has become much more widely available, it remains limited in such places as prisons and nursing homes where the disease is spreading quickly. The CDC says hospitalized patients and health-care workers should be at the front of the line for testing. People in long-term-care facilities should come next, the agency says.

In New York, the nation's largest hot spot, Suffolk County Medical Examiner Michael Caplan said in a memo to funeral directors on Wednesday that nursing homes and hospitals are responsible for collecting samples for postmortem testing.

That is unrealistic, said Michael A. L. Balboni, executive director of the Greater New York Health Care Facilities Association, which represents long-term-care residences.

"The last thing that a nursing home is going to do is try to determine if someone who has passed away is covid or no covid," he said in an interview. "They have their hands full trying to dispose of their remains appropriately. ... Why waste the swabs on decedents?"

A Suffolk County nursing home operator, who spoke on the condition of anonymity to protect the company's reputation, said some residents are sick with respiratory symptoms, and some have died, but virtually no one is being tested, dead or alive. The exception is when residents are taken to hospitals, the operator said.

"We're assuming that everyone is positive," the operator said. "To utilize a test on the deceased, it's not going to be very helpful. Because at the end of the day, there's a shortage of tests to begin with. We don't have tests. We don't have swabs."

The Federal Bureau of Prisons is no longer testing at a Louisiana prison where a dozen inmates have already tested positive and at least one has died. Sue Allison, a bureau spokeswoman, said that because the virus is spreading inside the facility, any inmate exhibiting symptoms is presumed infected.

Allison said the decision on whether to posthumously test inmates who died of suspected covid-19 would be made with health officials on a case-by-case basis, depending on the availability of tests and other factors.

In most states, people who die at home or have not been under medical care are reported to a patchwork system of medical examiners, lay and sheriff coroners, justices of the peace and other local authorities.

Sally Aiken, the president of the National Association of Medical Examiners, wrote in a news release that "the public, in general, does not understand that there is not a uniform death investigation system in the United States. ... So, a uniform response to COVID-19 by Medical Examiners will not occur."

Medical examiners typically investigate accidental deaths, homicides and suicides and are not going to get involved in a "natural death" such as that caused by covid-19, said Amy Schaefer, an investigator supervisor for the medical examiner's office in Summit County, Ohio, near Akron.

"You certainly are going to have numbers that aren't being counted because deceased people aren't being tested," she said. "We need to test people who are still alive."

But in Wyoming - the only state that had not reported a covid-19 death as of Saturday - Laramie County Coroner Rebecca Reid said she is ready to test anyone with symptoms who dies at home.

"We need an accurate cause of death to give the family some closure and make sure they have been safe," she said. "It's also very important that the public knows the truth."

She has supplies to test five people, she said.



Jacqueline Dupree, Abigail Hauslohner, Dalton Bennett and Lena H. Sun contributed to this report.



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NEW YORK TIMES

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Official Counts Understate the U.S. Coronavirus Death Toll

Inconsistent protocols, limited resources and a patchwork of decision-making has led to an undercounting of people with the coronavirus who have died, health experts say.

By Sarah Kliff and Julie Bosman
April 5, 2020



WASHINGTON - A coroner in Indiana wanted to know if the coronavirus had killed a man in early March, but said that her health department denied a test. Paramedics in New York City say that many patients who died at home were never tested for the coronavirus, even if they showed telltale signs of infection.

In Virginia, a funeral director prepared the remains of three people after health workers cautioned her that they each had tested positive for the coronavirus. But only one of the three had the virus noted on the death certificate.

Across the United States, even as coronavirus deaths are being recorded in terrifying numbers - many hundreds each day - the true death toll is likely much higher.

More than 9,400 people with the coronavirus have been reported to have died in this country as of this weekend, but hospital officials, doctors, public health experts and medical examiners say that official counts have failed to capture the true number of Americans dying in this pandemic. The undercount is a result of inconsistent protocols, limited resources and a patchwork of decision-making from one state or county to the next.

In many rural areas, coroners say they don't have the tests they need to detect the disease. Doctors now believe that some deaths in February and early March, before the coronavirus reached epidemic levels in the United States, were likely misidentified as influenza or only described as pneumonia.

With no uniform system for reporting coronavirus-related deaths in the United States, and a continued shortage of tests, some states and counties have improvised, obfuscated and, at times, backtracked in counting the dead.

"We definitely think there are deaths that we have not accounted for," said Jennifer Nuzzo, a senior scholar at the Johns Hopkins University Center for Health Security, which studies global health threats and is closely tracking the coronavirus pandemic.

Late last week, the Centers for Disease Control and Prevention issued new guidance for how to certify coronavirus deaths, underscoring the need for uniformity and reinforcing the sense by health care workers and others that deaths have not been consistently tracked. In its guidance, the C.D.C. instructed officials to report deaths where the patient has tested positive or, in an absence of testing, "if the circumstances are compelling within a reasonable degree of certainty."

In infectious outbreaks, public health experts say that under typical circumstances it takes months or years to compile data that is as accurate as possible on deaths. The reporting system during an epidemic of this scale is particularly strained. And while experts say they believe that virus-related deaths have been missed, the extent of the problem is not clear.

But as mayors and governors hold daily news conferences reporting the latest figures of infections and deaths related to Covid-19, Americans have paid close attention to the locations and numbers of the sick and dead - one of the few metrics available for understanding the new and mysterious disease threatening their communities.

Public health experts say that an accurate count of deaths is an essential tool to understand a disease outbreak as it unfolds: The more deadly a disease, the more aggressively the authorities are willing to disrupt normal life. Precise death counts can also inform the federal government on how to target resources, like ventilators from the national stockpile, to the areas of the country with the most desperate need.

For families who have lost a loved one in the midst of this epidemic, there is an urge simply to know: Was it the coronavirus?

Lingering questions

As the coronavirus outbreak began sweeping across the country last month, Julio Ramirez, a 43-year-old salesman in San Gabriel, Calif., came home from a business trip and began feeling unwell, suffering from a fever, cough and body aches. By the next day, he had lost his sense of taste and smell.

His wife, Julie Murillo, took him to an urgent care clinic several days later, where he was so weak he had to be pushed in a wheelchair. Doctors prescribed antibiotics, a cough syrup and gave him a chest X-ray, but they did not test for the coronavirus, she said. Just over a week after he returned from his trip, Ms. Murillo found him dead in his bed.

"I kept trying to get him tested from the beginning," Ms. Murillo said. "They told me no."

Frustrated, Ms. Murillo enlisted friends to call the C.D.C. on her behalf, urging a post-mortem test. Then she hired a private company to conduct an autopsy; the owner pleaded for a coronavirus test from local and federal authorities.

On Saturday afternoon, 19 days after the death, Ms. Murillo received a call from the Los Angeles County Department of Public Health, she said. The health department had gone to the funeral home where her husband's body was resting and taken a sample for a coronavirus test. He tested positive.

In a statement, the health department said that post-mortem testing has been conducted on "a number of cases," but did not provide specifics or comment on Mr. Ramirez's case.

The work of counting deaths related to the virus falls to an assortment of health care providers, medical examiners, coroners, funeral homes and local health departments that fill out America's death certificates. The documents typically include information on the immediate cause of death, such as a heart attack or pneumonia, as well as on any underlying disease. In coronavirus cases, that would be Covid-19.

The federal government does not expect to produce a final tally of coronavirus deaths until 2021, when it publishes an annual compilation of the country's leading causes of death.

A New York Times tally of known Covid-related deaths, based on reports from state and local officials, showed 9,470 deaths as of Sunday. On Friday, the National Center for Health Statistics, part of the C.D.C., began publishing preliminary estimates of coronavirus deaths, although a spokesman said that information would have a "lag of 1-2 weeks." Its first estimate noted 1,150 deaths, based on the number of death certificates that included Covid-19 as an underlying disease.

"It is not a 'real time' count of Covid deaths, like what the states are currently reporting," Jeff Lancashire, a spokesman for the National Center for Health Statistics, said.

But those who work with death certificates say they worry that relying only on those documents may leave out a significant number of cases in which coronavirus was confirmed by testing, but not written down in the section where doctors and coroners are asked to note relevant underlying diseases. Generally, certificates require an immediate cause, and encourage - but do not require - officials to take note of an underlying disease.

Then there are the many suspected cases.

Susan Perry, the funeral director from Virginia, said that she was informed by health workers and families that three recently deceased people had tested positive for the virus so that she and her staff could take necessary precautions with the bodies. Only one death certificate mentioned the virus.

"This probably happens all the time with different diseases, but this is the first time I'm paying attention to it," Ms. Perry said. "If we don't know the numbers, how are we going to be able to prepare ourselves and protect ourselves?"

'Now we're having the "aha!" moment'

Early in the U.S. outbreak, virus-linked deaths may have been overlooked, hospital officials said. A late start to coronavirus testing hampered hospitals' ability to detect the infection among patients with flulike symptoms in February and early March. Doctors at several hospitals reported treating pneumonia patients who eventually died before testing was available.

"When I was working before we had testing, we had a ton of patients with pneumonia," said Geraldine Ménard, chief of general internal medicine at Tulane Medical Center in New Orleans. "I remember thinking it was weird. I'm sure some of those patients did have it. But no one knew back then."

An emergency department physician in San Francisco recalled two deaths that were probably coronavirus but not identified as such. One patient died at home; a relative in the same home later tested positive for the disease. Another patient was an older man who came to the hospital with typical coronavirus symptoms, and who had been in contact with someone recently traveling to China, but arrived at the hospital before testing was available.

In New York City, emergency medical workers say that infection and death rates are probably far higher than reported. Given a record number of calls, many ambulance crews have encouraged anyone not critically ill to stay home. The result, medics say, is that many presumed coronavirus patients may never know for sure if they had the virus, so any who later die at home may never be categorized as having had it.

Across the country, coroners are going through a process of re-evaluation, reconsidering deaths that occurred before testing was widely available. Coroners and medical examiners generally investigate deaths that are considered unusual, or result from accidents or suicides, or occur at home.

Joani Shields, the coroner in Monroe County, Ind., said she wondered about a man diagnosed with pneumonia who died in early March.

A coronavirus test was requested at the time, but the local health department denied it, Ms. Shields said, on the ground that the supply of tests was too limited.

"I wish we could have tested him," she said.

In Shelby County, Ala., Lina Evans, the coroner, said she was now suspicious of a surge in deaths in her county earlier this year, many of which involved severe pneumonia: "We had a lot of hospice deaths this year, and now it makes me go back and think, wow, did they have Covid? Did that accelerate their death?"

Ms. Evans, who is also a nurse, is frustrated that she will never know.

"When we go back to those deaths that occurred earlier this year, people who were negative for flu, now we're having the 'aha!' moment," she said. "They should have been tested for the coronavirus. As far as underreporting, I would say, definitely."

Disparate reporting, more waiting

Even now, as testing is more widely available, there is a patchwork of standards about information being reported by state and local health officials on deaths in the United States.

Around the world, keeping an accurate death toll has been a challenge for governments. Availability of testing and other resources have affected the official counts in some places, and significant questions have emerged about official government tallies in places such as China and Iran.

In the U.S., uncertainties and inconsistencies have emerged, and health departments have had to backtrack on cases of previously reported deaths. Florida officials rescinded an announcement of a Covid death in Pasco County. In Hawaii, the state's first announced coronavirus death was later re-categorized as unrelated after officials admitted misreading test results. Los Angeles county officials announced that a child had died from the virus, then said they were unsure whether the virus caused the death, then declined to explain the confusion.

Adding to the complications, different jurisdictions are using distinct standards for attributing a death to the coronavirus and, in some cases, are relying on techniques that would lower the overall count of fatalities.

In Blaine County, Idaho, the local health authority requires a positive test to certify a death the result of coronavirus. But in Alabama, the state health department requires a physician to review a person's medical records to determine whether the virus was actually the root cause of death.

"This is in the interest of having the most accurate, and most transparent data that we can provide," said Karen Landers, a district medical officer with the Alabama Department of Public Health. "We recognize that different sites might do it differently."

So far, the state has received reports of 45 people with the coronavirus dying, but has only certified 31 of those deaths as a result of the virus.

Experts who study mortality statistics caution that it may take months for scientists to calculate a fatality rate for coronavirus in the United States that is as accurate as possible.

Some researchers say there may never be a truly accurate, complete count of deaths. It has happened before. Experts believe that widespread news coverage in 1976 of a potential swine flu epidemic - one that never materialized - led to a rash of deaths recorded as influenza that, in years prior, would have been categorized as pneumonia.

"We're still debating the death toll of the Spanish flu" of 1918-19, said Stéphane Helleringer, associate professor at the Johns Hopkins University Bloomberg School of Public Health. "It might take a long time. It's not just that the data is messy, but because the effects of a pandemic disease are very complex."



Sarah Kliff reported from Washington, and Julie Bosman from Chicago. Reporting was contributed by Mitch Smith in Overland Park, Kan., and Ali Watkins in New York. Susan C. Beachy contributed research from New York.