Wednesday, February 24, 2010

Target Cancer A Roller Coaster Chase for a Cure

PHILADELPHIA — His patient, a spunky Italian-American woman in her 60s, was waiting in an exam room down the hall for the answer: Was the experimental drug stopping her deadly skin cancer?

But as Dr. Keith Flaherty read out the measurements of her tumors from the latest CT scan, he could not keep the distress from his voice.

“She’s worse,” he said to the clinical trial nurse at the University of Pennsylvania’s melanoma clinic.

Like the 17 other patients on the drug trial — the corporate lawyer, the receptionist with young children, the Philadelphia philanthropist — the woman known in the trial as Patient 18 was going to die, most likely within months.

In the exam room, her gratitude for his failed efforts to save her tore at his heart.

He had been so optimistic. A radical departure from standard chemotherapy, the drug was designed to reverse the effect of a genetic mutation particular to the patient’s tumors. The approach represented what some oncologists see as the best bet for attacking all types of cancer.

And as he returned to his office that autumn afternoon two years ago, Dr. Flaherty was already calculating the next step: he wanted to test the drug at a more potent dose before giving it to more patients in a larger trial. It would require retooling the drug in a costly and complicated task that might not work, and he would have to make his case to two companies that had already poured hundreds of millions of dollars into the drug and were eager to move it forward.

“This,” he insisted to colleagues, “is the best drug we’re going to get.”

Dozens of such “targeted” drugs are emerging from the laboratory, rooted in decades of research and backed by unprecedented investment by pharmaceutical companies, which stand to profit from drugs that prolong life even by weeks.

But putting them to their truest test falls to a small band of doctors committed to running experimental drug trials for patients they have no other way to heal.

At a time when cancer still kills one in four Americans, it is a job that requires as much hubris as heart. To chronicle the trial of the drug known as PLX4032 is to ride a roller coaster of breakthroughs and setbacks at what many oncologists see as a watershed moment in understanding the genetic changes that cause cancer.

Over three tumultuous years, Dr. Flaherty saw patients who drove hundreds of miles for their monthly dose, and one who arrived barely able to walk. Some took 32 pills a day. When it became clear they were not absorbing the drug, he asked them to take the pills with high-fat foods like hamburgers and eggs, which might help dissolve them.

At academic conferences, he clashed with other oncologists who warned that targeted therapy had almost never had long-lasting results. At Penn, he badgered laboratory researchers whose animal tests might provide early clues for how a drug would behave in his patients.

And always, he ended up on his BlackBerry, e-mailing, calling, cajoling the drug makers to commit even more resources to the new category of drugs he so deeply believed in.

A five-and-a-half-foot streak of outsize energy, Dr. Flaherty, 39, seemed buoyed by an innate optimism and a faith in the scientific logic underlying the approach.

But at his clinic, where he gave vials of pills to patients whose tumors were often erupting, black and bumpy across their arms and legs, he told them only what he believed to be true.

“This,” he said, “is our best shot.”

The Driver Gene

In many ways, Keith Flaherty had been training to run the trial of this drug since his residency in the late 1990s at Brigham and Women’s Hospital in Boston.

There he grew to despise chemotherapy, which rarely cured cancer in its advanced stages, even as he learned to dispense it. The mainstay of cancer treatment for half a century, the chemotherapy drugs attacked all fast-growing cells, poisoning those that grow fast normally as well as the cancerous ones.

Drawn to oncology for the reason other residents often rejected it, Dr. Flaherty found strength in the intensity of treating patients who knew that they, and he, were fighting for their lives.

But he also chose the field because advances in understanding cancer’s molecular biology convinced him it might finally be possible to cure the disease — and he wanted to have a hand in it.

Healthy cells turned cancerous, biologists knew, when certain genes that control their growth were mutated, either by random accidents or exposure to toxins like tobacco smoke and ultraviolet light. Once altered, like an accelerator stuck to the floor, they constantly signaled cells to grow.

What mattered in terms of treatment was therefore not only where a tumor originated, like the lungs or the colon, but also which set of these “driver” genes was fueling its growth. Drugs that blocked the proteins that carried the genes’ signals, some believed, could defuse a cancer without serious side effects.

Dr. Flaherty arrived at Penn for a fellowship in the fall of 2000 just as one of the first such drugs, Gleevec, was inducing complete remission in patients with a rare leukemia. Yet many oncologists remained skeptical that its success could be replicated in common cancers that were more aggressive and genetically complex.

And there was no guarantee that the pharmaceutical industry, which already viewed cancer as too fragmented a market, would invest in developing drugs tailored to what were probably dozens of driver genes that had yet to be identified.

Dr. Flaherty, however, was convinced that what he called the “targeted therapy revolution” was around the corner. It was the only real hope, he told friends, colleagues, medical students and whoever would listen, “because it is based on what makes cancer tick.”

A career that combined treating patients with testing drugs would be far less lucrative than private practice. Such doctors are not allowed to have a financial stake in a drug, for obvious reasons. But Dr. Flaherty, the son of two medical researchers, had always wanted to pursue research.

He accumulated an encyclopedic knowledge of the targeted drugs in development and gravitated to melanoma, where the absence of reliable treatments made patients eager to try experimental ones.

The cancer, which struck 70,000 Americans last year, is easily treatable in its earliest stages, but almost always fatal within a year once it spreads beyond the skin.

In early 2002, when Dr. Flaherty started seeing patients on his own, the available trials still centered on chemotherapy drugs, and he sought to soften recitation of their toxic side effects — nausea, anemia, infection, hair loss — by mocking his own lack of hair.

“I’ve got bigger problems than hair loss,” many patients said.

“Tell me about it,” the doctor replied, invariably eliciting laughter.

He wore bow ties under his lab coat, and told patients to leave their health to him. Yet when grateful families gave him money for research, or sent him bow ties to add to his collection, he felt like a fraud. “What I do is palliative care,” he told his wife, a primary-care physician, in a form of self-indictment.

So when an article in the journal Nature brought news of what was almost surely one of the driver genes in melanoma in the spring of 2002, Dr. Flaherty could hardly contain himself. British scientists analyzing hundreds of tumor samples, he read, had found the same gene mutated in more than half of melanomas, and smaller numbers of other cancers as well. It was called B-RAF.

Dr. Flaherty, who has a near-photographic memory, was not accustomed to rereading. But in his campus office that morning, he scrolled through the article on his computer again to be sure he had understood. The presence of the same B-RAF mutation in so many cancers, he thought, meant it was one of the biggest genetic smoking guns yet identified in cancer. A drug that blocked the protein made by the defective gene might have enormous consequences for patients — and he knew of one that just might work.

Dr. Flaherty raced to the melanoma clinic. “We have to jump on this,” he urged his mentor, Dr. Lynn Schuchter.

For a junior faculty member, he was more confident than he had a right to be, Dr. Schuchter thought. Yet his optimism was infectious.

She would make trials of drugs that homed in on B-RAF a top priority, she told him.

That first effort, however, was destined to fail.

Dashed Hopes

Possessed of an energy that even friends called manic, Dr. Flaherty was used to finding diffuse outlets for it. In medical school at Johns Hopkins, he had read the entire works of Proust and cultivated bonsai. In Philadelphia, he collected a library of first edition books; copied the entire works of Mozart, Bach and Beethoven onto CD; and restored by hand the 150-year-old home he had bought with his wife, Dr. Mira Kautzky.

Raised in an affluent part of Baltimore, an A- student who had avoided exerting himself for the extra grade at boarding school at Phillips Andover and as an undergraduate at Yale, he now told his wife, “I feel like I’m applying myself for the first time.”

And if she wished that his version of taking care of their two young daughters did not so often involve settling them in front of golf tournaments on TV while he pored over patient charts and wrote trial protocols — the girls became avid fans of the sport — she also understood what drove him.

Over the next four years, with the backing of his superiors at Penn, Dr. Flaherty enrolled several hundred patients in trials of the drug, developed by an academic pioneer in targeted therapy and now owned by Bayer.

He asked the trial nurses to work weekends processing blood and tissue samples. And he evangelized the targeted approach at scientific conferences, where he invariably found himself outnumbered by melanoma researchers devoted to a class of drugs that sought to harness the immune system to attack cancer.

While a single targeted drug was likely to hold off cancer for only a limited time, immunotherapy can be curative. But after decades of effort, the only such treatment approved for use in melanoma helped just a tiny fraction of patients.

“You’re swinging for the fences on every pitch,” Dr. Flaherty told the immune therapists. And, he thought to himself, they were mediocre batters at best.

But for all his self-confidence, Dr. Flaherty found himself sobbing uncontrollably one evening in late 2004 over a letter from the wife of a patient who had died, the latest of several patients on the targeted drug whom he had lost in recent weeks. The reminders of the hope and trust that people put in him, he told his wife that night, “can be overwhelming.”

To many of Dr. Flaherty’s colleagues, the failure of the Bayer drug indicated that melanoma would prove impervious to targeted therapy. And to many other oncologists, it was a blow to the notion that targeted therapy would work in any cancer as its proponents envisioned.

Dr. Flaherty brushed them off.

“We just had the wrong drug,” he insisted whenever he could. “The principle holds.”

But more often than not, when he gave his targeted therapy pep talks, he found himself talking to half-empty rooms, waiting, in awkward silence, for questions no one cared enough to ask.

PLX4032

While some concluded that Dr. Flaherty was toiling in vain, a small biotechnology company in Berkeley, Calif., called Plexxikon was keeping close track of his work.

Ever since the B-RAF mutation had been identified as so prevalent in melanoma tumors, the company’s scientists had been working on a drug aimed at it, and when they invited him for a visit in early 2006, Dr. Flaherty could not fend off a wave of excitement.

One reason the Bayer drug had failed, he believed, was because it blocked proteins in healthy cells as well as cancerous ones, inducing nasty side effects that limited how much of the drug patients could tolerate.

The drug Plexxikon called PLX4032 was different, designed to bind to the B-RAF protein only in cancer cells. Human tumors with the mutation, grafted into mice, Plexxikon’s chief scientist told Dr. Flaherty, had stopped growing when exposed to the drug. And no amount seemed to induce side effects in dogs or monkeys.

An investment in the drug by Roche, the Swiss pharmaceutical giant, shortly after Dr. Flaherty signed on to lead its first human trial alleviated his concern that Plexxikon might not have the wherewithal to pull it off.

But the partnership also raised the financial stakes. Roche was to dole out, a chunk at a time, nearly $700 million to Plexxikon as it passed certain milestones on the way to the hoped-for approval by the Food and Drug Administration. The first hurdle was the completion of the trial Dr. Flaherty was to run, known as Phase 1, in which the goal was to determine the highest dose humans could safely tolerate.

For both companies, Dr. Flaherty knew, time was money. By now, Gleevec, the drug that had proved so effective in a rare leukemia, was generating a billion dollars a year for the company that owned it, and other companies had taken note. Competing drugs that aimed to block the B-RAF protein, and others that might play a role in fueling melanoma, were under development.

Still, as the trial opened in December 2006, Dr. Flaherty insisted on an approach that slowed them down. The companies had stipulated that any cancer patient could participate, a standard practice to speed the process of settling on a safe dose before moving on to a larger, Phase 2 trial.

But in the case of a targeted drug like PLX4032, Dr. Flaherty believed, it made far more sense to give it only to the patients for whom it was made.

Whenever possible, Dr. Flaherty and his co-investigator, Dr. Paul Chapman of Memorial Sloan-Kettering Cancer Center, agreed, they would screen tumors first for the B-RAF mutation, and offer a spot on the trial for those who had it.

It might take longer to find the right patients. But it was the best way to see if the drug worked — or did not.

Falling Short

In patients whose cancer bubbled in black lesions on their skin, Dr. Flaherty and Dr. Chapman sliced off tumor samples themselves. For those whose tumors had mushroomed internally, they requested a sample from whichever hospital had removed them.

Always, they warned prospective participants to consider the health risks of taking a drug that had never been given to humans. Perhaps worst of all, Dr. Flaherty emphasized, they could be devoting precious last days to blood work and X-rays.

But more often than in any other trial he had led, patients waved aside the concerns.

“It’s like a rope you’ve been thrown when you’re drowning, that’s made just for you,” one patient said.

“Is my head going to fall off?” asked a Philadelphia patient in her 50s. “Then bring it on.”

Dr. Flaherty had nominated Dr. Chapman, 54, as his chief collaborator on the trial, despite his longtime allegiance to immunotherapy and outspoken skepticism that blocking B-RAF could keep melanoma at bay.

Dr. Chapman, a senior clinical researcher in melanoma, was an especially rigorous clinical researcher, Dr. Flaherty knew, and he believed Dr. Chapman would give PLX4032 its fairest chance.

But the Sloan-Kettering doctor’s lack of enthusiasm in the investigators’ first conference call with Dr. Keith Nolop, Plexxikon’s medical director, made Dr. Flaherty slightly uneasy. “I’m really looking forward to this study,” Dr. Flaherty said in what is considered a customary statement of enthusiasm at the beginning of a trial, waiting for Dr. Chapman to add a few words of support.

On the other end of the line, there was only silence.

“I’m assuming it’s not going to work,” he told Dr. Flaherty flatly. “I hope I’m wrong.”

Typically, Phase 1 trials are limited to a few dozen patients and end when the dose reaches the point where side effects like rashes and diarrhea make patients too uncomfortable.

Dr. Flaherty and Dr. Chapman started the first three patients on 200 milligrams per day. After two months with no side effects — and no response — they doubled it.

Two more months passed, still nothing. They gave three more patients 800 milligrams, the equivalent of the dose that made tumors stop growing in mice. Even shrinking tumors, the doctors knew, would not mean the cancer had been cured but might at least offer a reprieve.

Dr. Flaherty pounced on the scans when they arrived. In some patients, tumors had remained the same size. “Maybe we’re starting to see something,” he could not help thinking. But at the next set of scans, the disease had progressed. On conference calls, Dr. Nolop sometimes referred to those patients as “responders.”

“They’re not responders,” Dr. Flaherty gently corrected him: under the accepted definition, tumors had to shrink to qualify patients as responders.

By the time they had doubled the dose four times, Dr. Flaherty could not help wondering if the targeted therapy skeptics were right. Dr. Chapman, crisp and businesslike on the weekly calls, supplied no comfort. He pointed out new research that B-RAF was mutated even in benign moles, and therefore could not be the key driver in melanoma.

The woman known in the trial as Patient 18 was one of the three who took 1,600 milligrams — 32 pills a day, she complained mildly, was a lot of pills.

This drug “doesn’t look so hot,” Maryann Redlinger, the trial nurse, told the doctor, urging him to keep an emotional distance.

Already, the two doctors had seen some patients on the trial die.

“I am deeply sorry and disappointed that I fell short of what you and I wanted,” Dr. Flaherty told their relatives, in an endless series of condolence calls that never became routine.

The higher doses, Dr. Flaherty and Dr. Chapman realized, were not getting from the digestive tract into their patients’ bloodstreams. The Phase 1 trial had accomplished its official goal: it had established that the drug was safe at the maximum dose the body could absorb. Yet everyone involved in the trial had hoped to see the tumors shrink.

“We need to get more in,” Dr. Flaherty pressed on their next conference call. At the suggestion of a Roche scientist, the doctors instructed patients to take the drug with high-fat foods in hopes that would help it dissolve more readily, but to no avail. The only recourse was to try to reformulate the drug so that patients could absorb a higher dose, an unusual undertaking at this stage in testing.

The companies were already trying to make the drug more potent, but Roche scientists said the reformulation would require a feat of chemistry that might not succeed. And it would mean several months of delay.

“This looks like our dose,” Dr. Nolop ventured on a conference call in the fall of 2007, as Dr. Flaherty and Dr. Chapman recalled. “This is about as high as it can go.”

Dr. Flaherty saw no way to fight it.

By rights, it was time to move to a larger Phase 2 trial. Roche and Plexxikon, he knew, could make good money on a drug that provided as little as an extra month or two of life to melanoma patients, as it still stood a chance of showing it could do in a larger trial. Doctors, too, would welcome the ability to provide even that for their patients.

Then, over the phone line, came support from an unexpected quarter.

“This is not your dose,” Dr. Chapman said. “For all we know we’re 10 times, 100 times too low!”

They had seen, Dr. Chapman said, not a single side effect. And tumors were still growing in the very patients for whom the drug was intended. If they moved to Phase 2 now, he continued, they would never know if a higher dose of the drug could have shrunk those tumors. If the idea had been to test the hypothesis that blocking the B-RAF protein could stop the melanoma, he said, they had not done that yet.

Dr. Flaherty, on the phone in his office at Penn, all but pumped his fist.

In December 2007, the companies halted the trial. They would wait while Roche chemists tried to reformulate the drug.

The First Responder

Elmer Bucksbaum came to see Dr. Flaherty at the melanoma clinic in the spring of 2008. He was accompanied by his son-in-law, Marc Lovitz, whose own father had died of melanoma just one month after the diagnosis. Now Mr. Lovitz was trying to prepare his wife and mother-in-law for the likelihood that there would be nothing the doctor could do for Mr. Bucksbaum.

“We know he doesn’t have long,” he told Dr. Flaherty.

Dr. Flaherty examined the patient, an 89-year-old retired film editor who had moved from Florida to live with his daughter. While he waited for a tumor sample from Mr. Bucksbaum’s neck for B-RAF screening, Dr. Flaherty secured him a spot on an immune therapy trial.

By the time Mr. Bucksbaum returned, a few months later, Dr. Flaherty had received the new PLX4032 from Roche. It was, the company promised, 10 times as potent as the previous one, packaged in a way the body could more easily absorb.

Mr. Bucksbaum’s tumor had tested positive for the B-RAF mutation. But the other trial had given him colitis. He had been bedridden for weeks. He had lesions around his eyes and on his neck, on his liver and in his lungs. The doctor was not sure if his patient had the will to try another experimental therapy.

Instead, Dr. Flaherty described hospice, as he often did with patients who had reached this point, without using the loaded word.

“Look,” he said, “we could focus on the things we can do to make you feel as good as you can feel.”

“Isn’t there anything else?” Mr. Bucksbaum asked.

He took his first PLX pills on Sept. 30, 2008.

To speed the trial as it resumed, Dr. Flaherty worked with collaborators at four other cancer centers to bring in patients. Mark Bunting, 43, an airline pilot in Sandy, Utah, flew to the University of California, Los Angeles, on Oct. 8 to get his pills.

Randy Williams, a contractor in Jonesboro, Ark., drove nine hours to Houston to enroll that month. Rita Quigley, a triage nurse, received her pills in Nashville. At Sloan-Kettering, Dr. Chapman added a patient with a large tumor in his abdomen.

When Mr. Bucksbaum returned to Dr. Flaherty’s clinic at the end of October, his skin lesions were gone.

“That’s good news,” the doctor told him cautiously.

But external tumors came and went with melanoma treatments. The internal tumors were what mattered. The doctor would not know about those until he looked at the scans Mr. Bucksbaum brought in on a disk four weeks later.

The clinic was backed up that day, and it was close to 5 p.m. when Dr. Flaherty called in the trial nurse to read her the tumor measurements. For a moment, he thought he had opened the wrong file. He strained to see any tumor at all.

It would be at least a week before he knew if Mr. Bucksbaum was an aberration.

Courtesy: The NewYork Times

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