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Spotlight Investigative Journalism Fellowship

The danger in our salad bowls

Leafy green vegetables have become the leading cause of E. coli poisoning. And the federal government still lacks the means, and maybe the will, to take it on.

Nathan Parker slept with his son Lucas Parker on a mattress in the living room because of his medically fragile condition. Lucas Parker suffered severe permanent injuries after eating romaine lettuce contaminated with E. coli bacteria during a visit to California in 2018.
Nathan Parker slept with his son Lucas Parker on a mattress in the living room because of his medically fragile condition. Lucas Parker suffered severe permanent injuries after eating romaine lettuce contaminated with E. coli bacteria during a visit to California in 2018.Suzanne Kreiter/Globe staff

RICHMOND, BRITISH COLUMBIA — It was the vacation of a lifetime for three generations of the Parker family. For much of 2018, Nathan Parker and his wife, Karla Terry, plotted their road trip from this Vancouver suburb down the Oregon coast to their final destination: Disneyland.

No one was more thrilled than Lucas Parker, the endlessly energetic 2-year-old who knew Mickey Mouse’s hot dog dance by heart. When the big week finally came in early October, Lucas and his two siblings delighted in exploring Disneyland’s Tomorrowland and descending into the darkness of the Pirates of the Caribbean ride.

Then Lucas began to throw up.

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By the time his mother changed his diaper that early morning, it was bloody. “He was shaking. He was pale,” said Nathan Parker. “He looked just horrible.”

The Parkers immediately started the 22-hour drive home to seek medical help, but family members were so worried that they stopped at an emergency room in Olympia, Wash.

“My kid is limp in my arms,” he recalled. A doctor told him, “I suspect it’s E. coli.’’

The Parkers had no way of knowing, but Lucas was one of the first victims of a disease outbreak that would shake public confidence in a seemingly benign, even virtuous, vegetable: lettuce. Five bites of a salad the boy shared on the trip to Disneyland with his father nearly a week earlier were enough to infect him with the toxic bacteria.

Is the FDA ready for the next E. coli outbreak?
Leafy green vegetables have become the leading cause of E. coli poisoning. And the federal government may not be ready for the next outbreak. (Video by Caitlin Healy/Globe staff)

Over the next month, 61 more people in 16 states would be diagnosed with E. coli poisoning — all traced to romaine lettuce. Many more might have been sickened if not for drastic action by Scott Gottlieb, then commissioner of the Food and Drug Administration, who tweeted to a startled nation that they should stop eating romaine lettuce just two days before Thanksgiving 2018.

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It was a crisis that faded from the news almost as soon as it was safe to restock store shelves. Still, it should have been the wake-up call that mobilized the government to defeat this threat to food safety.

But the call was muted, and the response so far underwhelming.

More than a year after the Thanksgiving outbreak, the E. coli threat is as real as it ever was, and the government still lacks the means, and maybe the will, to take it on, a six-month Globe review finds. There have been four E. coli outbreaks traced to lettuce since September alone, sickening people in more than two dozen states. Since 2017, there are nearly 500 documented victims and six deaths from leafy green vegetables contaminated by E. coli. Because the disease is difficult to document, the actual numbers are likely many times higher.

In fact, leafy green vegetables now cause more E. coli outbreaks than any other food, including beef, but the government’s efforts to secure the safety of greens remains a pale shadow of its policing of red meat. The Globe review found that the FDA still sometimes seems more concerned with preventing panic than fully informing the public about health hazards in the food supply.

Despite the growing number of outbreaks, the agency remains protective of the growers, taking little enforcement action and sometimes shielding growers suspected of causing outbreaks from bad publicity. Consider:

■ The FDA has called little attention to the surge in E. coli outbreaks from leafy green vegetables. It has been slow to investigate or publicize risks and did not disclose one outbreak to the public until the Globe contacted agency officials about reports of E. coli poisonings. FDA officials insist they planned to disclose the early fall 2019 outbreak all along.

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■ The FDA has not punished any farm or distributor in connection with the seven outbreaks traced to lettuce since 2017 even though federal law prohibits the sale of contaminated foods. The agency concluded that three of the outbreaks were linked to a single California lettuce grower but declined to release the name.

■ The FDA staff monitoring lettuce production is just a small fraction of that detailed to the federal oversight of beef: There are 614 FDA field investigators responsible for leafy greens compared to 7,068 workers overseeing beef for the Department of Agriculture. Congress recently gave the FDA $8 million to better handle outbreaks, but the agency doesn’t want to talk about the state of its staffing. When the Globe tried to examine just how understaffed the agency is, officials redacted hundreds of pages of records discussing their internal problems.

■ The agency relies almost entirely on voluntary cooperation from the lettuce industry, an approach that has brought about some safety improvements. But FDA has asked relatively little of the industry and recently delayed implementing rules aimed at preventing E. coli contamination of irrigation water until 2022.

“There is no oversight,” said food safety lawyer Shawn Stevens, who previously represented beef powerhouse Cargill in cases brought by contamination victims and who sees the major differences between the regulation of meat and leafy greens. “There is no one watching (lettuce) being harvested or distributed or transported to the processing facility or being washed or being packaged.”

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FDA officials defend their performance, noting that pinpointing the source of E. coli contamination is complex, especially for lettuce. Many of the outbreaks appear unrelated to each other, they said, and investigators have not always been able to conclusively identify the source.

“We did not conclude in any of these outbreaks, which are not all related, how the romaine lettuce (or leafy greens) . . . became contaminated,” said spokeswoman Lyndsay Meyer. “We often are not able to explain the full route of contamination.”

Nathan Parker built an aquatic center for his son Lucas in their home. Nathan said the best days of Lucas’s childhood are behind him. “I still have dreams of him running around here,” said Nathan, but he knows that’s extremely unlikely.
Nathan Parker built an aquatic center for his son Lucas in their home. Nathan said the best days of Lucas’s childhood are behind him. “I still have dreams of him running around here,” said Nathan, but he knows that’s extremely unlikely.Suzanne Kreiter/Globe staff

The importance of closing that investigative gap is as clear as the potential consequences of E. coli poisoning are devastating. Fifteen months after the Parkers’ trip of a lifetime, Lucas still deals with the long-term consequences: He is legally blind. He cannot speak or move. He requires a feeding tube because he cannot swallow and his medical records show he suffers a litany of other serious conditions.

Nathan Parker now cares for his son full time. As Lucas rested on his chest in the family’s cramped apartment, the father of four wondered what he could have done differently. He thought he was eating sensibly, and encouraging his family to do the same. He never saw any warnings to avoid eating lettuce.

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“I had no reason to believe that I couldn’t eat salad,” said Nathan Parker. “It’s America’s best kept secret.”

Green gold

ACROSS 101,500 DUSTY and sun-soaked acres of Yuma, Ariz., and California’s Central Coast, farmers grow the greens that fill the salad bowls of much of the nation. Over the faint buzz of insects, row after meticulously planted row of romaine lettuce sprout and bloom like verdant bouquets. Once picked, they are sent to processors, where the leaves are soaked in sudsy baths, packaged, boxed, and shipped to restaurants and supermarkets.

The arrival of these delicate greens on menus and supermarket shelves is welcomed by consumers in these health-conscious times. US lettuce production has grown nearly 50 percent since 2000, reaching 4 billion pounds in 2018, according to federal figures.

Romaine lettuce has become a star among leafy greens, its crunchy leaves most often used in Caesar salad or as the bed for countless foods, from a scoop of chicken salad to a charcuterie platter.

But just as consumers have learned to love lettuce, so has a dangerous type of bacteria. A particular strain of E. coli called “Shiga Toxin producing E. coli” or sometimes STEC 0157:H7 for short, is a common contaminant, especially of romaine lettuce. Scientists have found that the thirsty plants, which grow close to the ground, offer easy access for E. coli to latch onto them through soil or by water. Once E. coli has landed on romaine’s leaves, it settles into the plant’s pores and rides along through the long journey from field to salad bowl.

Modern farming has made E. coli and lettuce a perfect match. Lettuce thrives in water-starved areas where finding any water and keeping that water clean are ongoing challenges. When water levels are low, contamination becomes even more of a problem, because irrigation is essential and E. coli often settles into sediments at the bottom of the canals that bring water to crops.

Romaine lettuce grew near Yuma, Ariz., one of the nation’s leading producers of leafy green vegetables. At least one recent E. coli outbreak has been traced to farms in the region.
Romaine lettuce grew near Yuma, Ariz., one of the nation’s leading producers of leafy green vegetables. At least one recent E. coli outbreak has been traced to farms in the region.Caitlin O’Hara/file 2016

Under the best of circumstances, E. coli is a maddening bacteria for investigators to trace; the Shiga toxin complicates the process further because it takes its time doing its dirty work. Lucas Parker, as is typical for those infected, did not get sick until a week after he ate contaminated lettuce. By that time, any traces of the contaminated lettuce have often been disposed of, making the path of contamination that much harder to trace.

Also, only a few of those infected become seriously ill, dampening the sense of regulatory urgency. The severity of symptoms varies widely. Some victims have mild diarrhea while a few become gravely ill. Case in point: Lucas Parker’s father, grandmother, aunt, and younger brother all had brief symptoms of vomiting or diarrhea after eating the same salad. But they recovered quickly and are fine.

Perhaps not surprisingly, the vast majority of victims are never even identified. The Centers for Disease Control estimates that 265,000 Americans are sickened by E. coli from all causes each year, though only a few thousand cases are confirmed.

Facing this formidable and many-layered challenge, the FDA deploys a modest, overworked team that struggles to handle the workload, especially during a contamination crisis.

A review of 413 pages of internal FDA e-mails during the October-November 2018 outbreak shows that the FDA team worked day and night and through the Thanksgiving holiday weekend to obtain basic information about the outbreak from the leafy greens industry, which still uses paper documentation for much of its produce tracking.

The agency was also, in that moment, still dealing with a previous E. coli outbreak caused by lettuce, tying up staff. On Nov. 27, 2018, FDA executive Jim Gorny, who had returned to FDA to help prevent illnesses caused by contaminated produce, wrote to colleagues, in a heavily redacted e-mail, “I have no resources to deploy.”

FDA spokeswoman Meyer, who responded on behalf of Gorny, said that because Gorny’s job is an advisory position, “he simply meant that he personally could not send anyone to assist” because he had no direct staff. However, Gorny declined to explain his comments.

“The FDA has a number of agents and staff, but nothing in terms of the number of field inspectors needed,” said Darin Detwiler, a Northeastern University dean with an expertise in food policy. His research has found staff shortages are a chronic problem.

Two days before Thanksgiving in 2018, Scott Gottlieb, then commissioner of the Food and Drug Administration, urged consumers to dispose of all romaine lettuce amid an outbreak of E. coli. It was a stark reminder of the perils of toxic bacteria in the US supply of produce.
Two days before Thanksgiving in 2018, Scott Gottlieb, then commissioner of the Food and Drug Administration, urged consumers to dispose of all romaine lettuce amid an outbreak of E. coli. It was a stark reminder of the perils of toxic bacteria in the US supply of produce.Drew Angerer/file 2017/Getty Images

The FDA is further hamstrung by what Gottlieb called the agency’s culture of caution, a fear that putting out a false alarm about an E. coli outbreak could damage public trust in the FDA — and needlessly alarm consumers. They want to be absolutely sure they have found the correct source before going public. But this cautiousness has a price.

In the E. coli outbreak that sickened Lucas in October 2018, the FDA waited three weeks after it first heard about the problem to announce anything. The outbreak finally came to national attention two days before Thanksgiving, when Gottlieb, fearful that millions of Americans were about to eat E. coli-contaminated salads with their holiday meals, tweeted that Americans should just throw away all their romaine lettuce. The health warning triggered a massive disposal of lettuce. Gottlieb felt he had no choice.

“This information was getting into the press,” said Gottlieb. “I thought it was important for the agency to have a voice in speaking to these issues.”

A beefy comparison

IN JANUARY 1993, Jack in the Box restaurants triggered one of the worst E. coli outbreaks in US history when workers mostly in the Seattle area did not follow newly created standards to cook its burgers. Detwiler, who was then living in Seattle, found himself caught in the crisis.

Detwiler’s toddler son, Riley, had never even eaten a hamburger. But he picked up E. coli in day care from another child whose parents both worked at Jack in the Box. Riley was one of four who died in the outbreak.

The tragedy upended Detwiler’s life, wrecking his marriage and turning him into an influential advocate for food safety. It also brought unprecedented pressure on the agency charged with keeping meat safe, the Department of Agriculture. New inspectors were hired, and a sophisticated tracking system called PulseNet was launched, bringing together data from 82 labs in all 50 states and accelerating identification of emerging outbreaks and their source.

It was a much-needed regulatory revolution — but it had little impact on the oversight of leafy green vegetables.

These changes “had nothing to do with produce,” said Detwiler. “I actually think that in terms of food safety, you’re better off eating ground beef than you are eating leafy greens today.”

Indeed, since the late 1990s, leafy green vegetables have overtaken beef as a source of E. coli poisonings. Data compiled by the Centers for Disease Control show that, from 2009 to 2018, almost twice as many people suffered E. coli poisoning from leafy green vegetables compared to beef.

Detwiler notes that most produce inspectors are concentrated overseas and at borders, forcing the FDA to delegate most monitoring to state agencies. Most farms are inspected every three years. By comparison, beef has a much more clear-cut system. Federal officials are assigned to individual plants to oversee daily inspections of the process.

After beef leaves the packing plant, the industry employs sophisticated tracking systems that enable investigators to more easily isolate the source of an outbreak without disrupting the nation’s entire beef supply anytime an outbreak occurs. By comparison, both FDA officials and lawyers involved with leafy green outbreaks note that farmers, distributors, restaurants, and retailers still keep paper files and have no computerized way to trace the source.

The Agriculture Department also discloses far more information about retailers that are selling contaminated beef so that customers have better information about whether their local supermarket has been affected. The FDA releases only limited information about retailers selling potentially contaminated produce, arguing that the disclosure could reveal “trade secrets” or information desired by competing stores. The FDA has not identified individual stores selling contaminated lettuce in any of the outbreaks.

But the lettuce industry never had a galvanizing event like the Jack in the Box outbreak to give urgency to the need for reforms. Detwiler predicts it’s only a matter of time. “Pathogens like E. coli, they do not discriminate,” he said.

Missed opportunities

EMERGENCY ROOM STAFF at New Jersey hospitals were the first to notice what would turn out to be the biggest E. coli outbreak linked to lettuce in a decade. In late March 2018, multiple patients with gastro-intestinal symptoms said they had eaten at a Panera restaurant, and doctors began asking other ER patients whether they, too, had visited the chain. Some had, including one woman who tested positive for E. coli.

The outbreak would officially sicken 240 people and kill five across 36 states, a toll that rivaled the Jack in the Box outbreak. But the FDA was slow to catch on that an outbreak was unfolding, first hearing about the growing number of illnesses on April 5, 2018, when a county health official in New Jersey confirmed to a reporter they were investigating two E. coli cases traced to a Panera. By then, the Centers for Disease Control had seen a rise in E. coli cases on PulseNet, but CDC officials said nothing to the FDA until April 4 because “the source of the illnesses was unclear at the time,” a CDC spokesman said.

Despite the specific warnings from New Jersey health officials, the FDA waited another six days before it said anything publicly. An FDA official explained to the Globe that they waited to make an announcement in part because “we did not have a specific location where the romaine was coming from.”

The delays didn’t stop there. The agency got a break in April when eight inmates at an Alaska prison got E. coli poisoning that was traced to some lettuce from Harrison Farms in Yuma, Ariz. That immediately narrowed the search for the cause of at least some poisonings, holding out the promise that, this time, FDA might move quickly.

But the FDA did not send field inspectors to the 140-mile stretch of Arizona farms until June 4, two months after their first call from the New Jersey Department of Health. Meyer, the FDA spokeswoman, said the agency initially did not have enough information to go on.

Karla Terry had her hands full with children, Seth, 4 months, Alex, 2, and Lucas, 3. Lucas became so gravely ill from eating contaminated romaine lettuce that doctors had prepared Terry and her husband, Nathan Parker, for his death. They had Lucas baptized and waited at his bedside. “He never really woke up from the coma,’’ Parker said.
Karla Terry had her hands full with children, Seth, 4 months, Alex, 2, and Lucas, 3. Lucas became so gravely ill from eating contaminated romaine lettuce that doctors had prepared Terry and her husband, Nathan Parker, for his death. They had Lucas baptized and waited at his bedside. “He never really woke up from the coma,’’ Parker said. Suzanne Kreiter/Globe staff

But she said the FDA treated the episode as “a major outbreak with all hands on deck,” including nearly two dozen workers in the field and more staff at headquarters.

Eventually, FDA officials found three samples of E. coli 0157:H7 in water within a mile of the Wellton irrigation canal that provides water for the lettuce fields in Yuma. The same strain of E. coli was found one mile upstream, next to a large lot where thousands of Holsteins cattle were fed.

Stephen Ostroff, then a top FDA commissioner overseeing the case, said agency investigators had to negotiate with the feedlot owners for access to the land and ended up with only six samples from the manure and water, an amount Ostroff called “inadequate to fully assess” whether E. coli was present.

A vice president of the company, Five Rivers Cattle Feeding, insisted that FDA investigators were welcome to take as many samples as they wanted and that the company cooperated fully.

Officials from Five Rivers as well as the National Cattlemen’s Beef Association went to FDA headquarters in September 2018 to press their case that the feedlot didn’t cause the E. coli outbreak. Ostroff, who attended the meeting, said industry officials thought there was considerable uncertainty about the cause.

In the end, Gottlieb concluded, mildly, that the cattle feed operation was “one potential source” that could have caused the outbreaks.

No one was ever penalized in the spring 2018 outbreak. No lettuce was ever officially recalled.

Some important changes, however, did follow that outbreak. The Leafy Greens Food Safety Task Force, composed of more than 100 industry representatives, called for longer distances between romaine lettuce fields and large-scale cattle feeding operations.

Protecting the source

AT LEAST SOME of the cases in the Thanksgiving outbreak — the one that sickened Lucas -- were eventually traced back to one California farm. It is a vast fifth-generation family business located roughly 75 miles north of Santa Barbara that local press reports have said employs hundreds of workers to tend to thousands of acres.

Adam Brothers had sent its harvested lettuce seven miles away to a distributor, United Foods, in Nipomo, Calif. Then United Foods shipped an order of romaine 11 miles away to Gino’s Pizza, which is where the Parkers placed their delivery order for salad and pizza.

The FDA found that the chemical tablets Adam Brothers used to sanitize its irrigation water had not dissolved, leaving the water dirty. Though investigators could not determine where the E. coli had come from, the farm’s failure to fully treat the water allowed the bacteria to survive, contributing to an outbreak that sickened at least 62 people in the US and another 29 in Canada, including Lucas.

Nonetheless, FDA took no action against Adam Brothers, and even allowed the farmers to announce their own recall of potentially tainted red and green leaf lettuce and cauliflower. The farm’s Dec. 13, 2018, announcement of an outbreak did not mention that Adam Brothers had been a source of the contamination. It did, however, mention other Adam Brothers vegetables subject to the recall, noting that “no illnesses have been reported” from eating those.

FDA spokesman Peter Cassell defended Adam Brothers’ recall statement in an e-mail, saying he did not find it misleading. Cassell’s FDA colleague, Meyer, reiterated that “Adam Brothers was cooperative and agreed to a voluntary recall” of other vegetables it grew. That meant “no additional action was needed.”

Adam Brothers officials declined to speak to the Globe, but one of the brothers, Peter Adam, seemed to take the whole episode in stride, telling a local television outlet that the recall was nothing special.

“This isn’t the first time we’ve been under the microscope,” Adam said in the February 2019 interview. “This is part of life in vegetable world in California today and maybe just in business in general in the United States.”

The produce industry took some additional steps.

In September, 100 public health and industry professionals released a report, facilitated by food producers, with specific suggestions on how to avoid outbreaks, encouraging growers to follow higher standards for issues such as the water they irrigate with. As of Jan. 1, the task force instructed all leafy green suppliers to place scannable labels on their products. Industry officials say the vast majority have complied.

Jennifer McEntire, vice president of food safety and technology for United Fresh, one of the organizations that worked on the report, stressed industry’s commitment to helping federal authorities solve the E. coli problem.

Contaminants, the report said, must be traced to their source and eliminated quickly, through the combined efforts of business and government. Otherwise, “we are preordained to repeat those results and ultimately may find ourselves in the middle of yet another outbreak.”

Nathan Parker delivered one of six morning medications through the feeding tube for his son Lucas.
Nathan Parker delivered one of six morning medications through the feeding tube for his son Lucas. Suzanne Kreiter/Globe staff

What does the public need to know?

ANOTHER OUTBREAK CAME very soon, posing a test of the FDA’s new commitment to protect consumers of leafy greens.

What followed was a repeat of the old patterns, with the FDA trailing a state agency — and the Globe — in taking full notice of the new threat.

The New York State Health Department confirmed to the Globe that it had identified one case tied to a multistate outbreak. Within hours of that announcement, a CDC spokesman confirmed to the Globe that the outbreak had grown to sicken 23 people across 12 states between July and September.

Still, the CDC issued no public warning, a spokesman said, because the “romaine lettuce eaten by sick people was past its shelf life and no longer available for sale.” The FDA took a similarly low-key posture, saying it made no sense to notify the public about an outbreak that was over.

“We don’t have anything specific to tell consumers,” an FDA official told the Globe. “We can’t point to a company and say their lettuce is bad.”

But the night before FDA officials believed the Globe was about to report on the outbreak, and the agency’s passive response, they changed course. FDA contacted the Safe Food Coalition, a group of consumer advocates and foodborne illness victims, to say it would soon announce that a recent outbreak had come and gone.

Frank Yiannas, a former Walmart executive and the current FDA deputy commissioner for Food Policy and Response, then personally called members of the foodborne illness community to say he had planned to announce the outbreak all along. Meyer reiterated that claim in a statement. “FDA was always planning to report, as we did, that an outbreak occurred,” the spokeswoman said. “It was simply not an urgent advisory.”

Since then, the FDA has faced three E. coli outbreaks affecting lettuce that state health departments in Maryland and Wisconsin helped them solve. Combined they sickened 193 people in 29 states. All three outbreaks were traced back to a single grower in Salinas — California’s largest growing region with nearly 60 percent of the state’s total lettuce acreage.

The FDA, citing lingering uncertainty, declined to identify the “common grower” when asked by the Globe.

“It’s still too early to determine whether this grower was in fact the source of this outbreak,” said FDA spokeswoman Meyer.

Karla Terry and Nathan Parker traveled with their children last month to have photos taken with Santa. Lucas (right) became uncomfortable and cried as they made their way through the Home Depot parking lot. They missed last year's holiday photo because Lucas was in the hospital battling the effects of the contaminated lettuce he ate.
Karla Terry and Nathan Parker traveled with their children last month to have photos taken with Santa. Lucas (right) became uncomfortable and cried as they made their way through the Home Depot parking lot. They missed last year's holiday photo because Lucas was in the hospital battling the effects of the contaminated lettuce he ate. Suzanne Kreiter/Globe staff

Lucas

SINCE LUCAS PARKER was discharged from the hospital in March 2019, he has rarely moved from his family’s couch. On a recent morning, Lucas had his right arm wrapped around his gold-colored Care Bear. His eyes flitted toward the sounds of the History Channel in the background, while Ginger, his grandma’s Chihuahua, and Bella, the Parkers’ cat, protectively encircled him. The only sounds Lucas seems to make are mournful, guttural cries when he needs help.

Lucas’s relatives search for hopeful signs: Lucas’s aunt asked him if he had a busy day and it looks as if he was nodding. Nathan Parker said Lucas lights up at the sounds of wrestling on television. His mother pressed a chocolate doughnut to his lips and he cooed.

Before his debilitating sickness, Lucas loved to watch Star Wars movies with his father, Nathan, who still props up a phone for Lucas to watch.
Before his debilitating sickness, Lucas loved to watch Star Wars movies with his father, Nathan, who still props up a phone for Lucas to watch. Suzanne Kreiter/Globe staff

The Parkers’ lawyer, Bill Marler, said he is getting as many as three calls a week about people who have contracted E. coli from eating romaine lettuce. Ninety percent of his E. coli cases now involve lettuce instead of ground beef. The damage has been so devastating that they have fetched settlements for more than $15 million.

But that number, while large, is far from adequate, given the number of victims and the cost of the medical care Lucas and others will require. Lucas, despite his dire condition, could live a long life. Will the expense and complexity of his care one day outrun his family’s capacity?

Nathan Parker wonders: What will happen to his broader family, when he can no longer care for his son?

“Everybody is gonna be affected by this in their own way,” he said. “This is like casting a stone in a pond and watching ripples. You know, those ripples just get bigger and bigger and bigger.”

Christine Haughney can be reached at christinehaughneydb@gmail.com.