CATCHING DOPING ATHLETES Rajendrani Mukhopadhyay
ANALYTICAL CHEMISTRY PLAYS A KEY ROLE IN UNMASKING ATHLETES WHO TAKE PERFORMANCE-ENHANCING DRUGS.
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etting caught doping has destroyed various heroes in sports. There’s Ben Johnson, the Canadian sprint-
er who enjoyed a high-profile career during much of the 1980s. He set two world records for the 100-m sprint and won a gold and two bronze medals at the 1988 Olympic Games in Seoul. When Johnson won the Olympic gold medal and broke the world record, many newspapers flashed laudatory headlines, such as the Toronto Star’s “Benfastic”. But later, after Johnson tested positive for the anabolic steroid stanozolol, he was disqualified and lost the Olympic title and both world records. Other athletes have faced similar fates. More recently, accusations of taking performance-enhancing drugs have dogged sports figures such as cyclist Floyd Landis, sprinter Marion Jones, baseball players Barry Bonds and Jason Giambi, and Bulgarian tennis player Sesil Karatantcheva. The problem isn’t restricted to 5522
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just top-tier athletes. In 2004, the U.S. Senate held a congressional hearing about the abuse of performance-enhancing drugs by American teenagers. It was estimated that 175,000 teenage girls and 350,000 teenage boys were abusing steroids to improve athletic performance, appearance, and self-image. How do athletes get caught cheating? Chemical analyses aren’t the only way, but they do come into play. Away from soccer fields and racetracks, investigators at laboratories and anti-doping agencies around the world continuously work to ensure that athletes are free of performance-enhancing substances. They use a variety of analytical techniques to test hundreds of samples every week and are careful that their results catch cheating athletes and do not inadvertently accuse the innocent. The work is intense because investigators have to stay ahead of the deceitful athletes and coaches striving to beat the analytical detection schemes. © 2007 AMERICAN CHEMICAL SOCIETY
JUPITERIMAGES
Catch ’em any way you can The World Anti-Doping Agency (WADA) is the international organization, independent of the International Olympic Committee, that promotes, coordinates, and monitors the struggle against sports doping. WADA works with national anti-doping agencies to establish analytical criteria for the anti-doping laboratories. The laboratories aren’t expected to follow any fixed protocols to detect performance-enhancing drugs. The agencies only set detection standards. “We’ve not gone in the direction of the Environmental Protection Agency of standardized methods,” says Larry Bowers of the U.S. Anti-Doping Agency (USADA). “I’ve always chuckled and said if we had a book of standardized methods, the athletes would have a book of standardized ways to beat the standardized methods!” The agencies establish analytical criteria for all performanceenhancing drugs. The laboratories design and validate their methods on the basis of those analytical criteria. Oliver Rabin of WADA explains, “We clearly say, ‘We want a drug to be detected
at 2 ng/mL in urine or blood.’ It’s up to the labs to say, ‘Okay, we have to develop the method to reach WADA’s objectives.’ We accredit the anti-doping laboratories based on those objectives.” WADA has now accredited 34 laboratories worldwide. Currently, most of the methods in the laboratories are based on GC/MS and LC/MS. Don Catlin, who is with the Anti-Doping Research Institute and is the former director of the University of California Los Angeles (UCLA) Olympic Analytical Laboratory, says that LC/MS only recently got added to the laboratories’ armamentarium when it helped to uncover the designer anabolic steroid tetrahydrogestrinone (THG) in the infamous Bay Area Laboratory Co-operative (BALCO) scandal (box on p 5525). Now, “a lot of us are converting over to LC/MS where possible,” says Catlin. “By and large, anabolic steroids are going to run on GC/MS and LC/MS in probably all the labs. There is a little bit of screening done by immunoassay.” For the immunoassay screenings, the anti-doping agencies require absolute stringency. “The data that’s produced from the labs is really forensic in nature, and we’re talking about potenA U G U S T 1 , 2 0 0 7 / A N A LY T I C A L C H E M I S T R Y
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tially having a major impact on someone’s career,” says Bowers. “Immunoassays traditionally have been viewed as having the potential for cross-reactivity, so we’ve tried to do two things.” First, the agencies have stressed the importance of knowing what is recognized on an analyte by a given antibody. Second, analytical labs must have a validation process in which two antibodies that recognize different epitopes on the molecule are used in two separate runs in an immunoassay test. The double run ensures that any interference from cross-reactivity with other molecules doesn’t affect the result.
A few of their favorite drugs Substances abused in sports cover the gamut of chemical compounds—anabolic steroids, stimulants, hormones, even wholeblood transfusions. Hormones such as human chorionic gonadotropin (hCG), secreted during pregnancy, and luteinizing hormone (LH) are detected by immunoassays. When taken by men, hCG mimics LH’s effects. LH usually travels from the pituitary via the blood to the testes, where it triggers testosterone production. The synthetic versions of the hormones taken by cheating athletes boost their production of testosterone, an anabolic agent that helps to build muscle. Unfortunately, hCG is also secreted by some cancers. “We’ve had a couple of occasions, about three now, where we’ve picked up a nasty tumor ahead of the athlete knowing about it,” says David Cowan at King’s College London. Synthetic testosterone holds an allure for cheating athletes because it’s identical to natural testosterone. MS can detect testosterone in urine, but the spectra of the natural and synthetic hormones look the same. During the 1980s and 1990s, Catlin, who then worked at the UCLA Olympic Analytical Laboratory, and his colleagues figured out a way to distinguish between the two. Synthetic testosterone isn’t made from scratch. Pharmaceutical manufacturers perform partial synthesis in which a precursor plant compound, typically from yams, is converted into testosterone in a few steps. The plant compound has a different carbon isotope ratio from human testosterone. Catlin and colleagues developed a test, based on the carbon isotope ratio, that can discern the atomic differences between synthetic and natural testosterone. Because the concentrations of testosterone in urine are very low, in practice investigators look at the carbon isotope ratio of its metabolites. The Olympic Movement Anti-Doping Code acknowledged the test in 1999. The method caught Justin Gatlin, the U.S. sprinter who won gold medals in the 2004 Olympic Games, and it has been used to evaluate accusations of doping against Floyd Landis, the win-
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ner of the 2006 Tour de France. Recombinant erythropoietin (EPO), a drug first developed by Amgen in the 1980s, is designed to help people who are undergoing chemotherapy or who have chronic renal failure. However, because it boosts the production of red blood cells and thus increases the body’s oxygen-carrying capacity, EPO is abused in sports. Cyclists caught with EPO and other drugs reduced the 1998 Tour de France to the “Tour de Shame”. Lance Armstrong, a seven-time winner of the Tour de France, has been dogged by accusations of taking EPO, though he has never tested positive for the substance. The assay for EPO is based on isoelectric focusing (Nature 2000, 405, 635). Because the sugars on synthetic and natural EPO differ, they cause the two varieties of the hormone to migrate to different positions on the gel, resulting in different bands. But the method can only detect EPO if the athlete is tested within 2–5 days of taking the drug. Because of the innately complex nature of the test and the 3 days it takes to complete, “many of us are working to try to convert that technique over to [a] hard-core MSbased technique,” says Catlin. Insulin is an anabolic agent and produces glycogen. Recently, a method consisting of immunoaffinity chromatography with subsequent LC/MS analysis was developed by Mario Thevis at the German Sport University Cologne and colleagues to detect long-acting synthetic versions of insulin in urine (Anal. Chem. 2007, 79, 2518–2524). Because the hormones are synthetic, “they are modified—there are different amino acid sequences,” says Thevis. “That’s what we can differentiate with mass spectrometry.” Single compounds may not cut it for some cheaters. Blood substitutes, called hemoglobin-based oxygen carriers, are used in acute medical cases or for military purposes. Like whole blood, they can be abused by athletes, who transfuse synthetic or whole blood into their bodies to boost their oxygen-carrying capacity.
Choice of sample Much of the testing for sports doping is carried out on samples of urine. Catlin explains, “When the Olympics are going on, we will do blood. During the Olympics, everything is focused on a 2-week period, and all kinds of support and facilities are available so we can do blood. But it’s very difficult to do blood day in and day out.” Until recently, doubts have plagued the blood tests. Bowers says that for a while it was thought that religious or ethnic prohibitions would hamper blood collection in some cultures. But “in the last few years, we’ve seen that’s not the case,” he says. Another concern “was the potential of causing a hematoma or that
The 2003 BALCO scandal
kind of thing in athletes that might somehow impact the performance.” The reluctance to use blood tests has diminished but persists. Collecting blood can be a challenge in those sports with professional leagues because some unions are skeptical about blood sampling. But for some performance-enhancing drugs, urine testing is simply not an option because the substance doesn’t make its way into urine. “Blood has to be used for the detection of human growth hormone and transfusions of blood and synthetic blood,” says Costas Georgakopoulos at the Doping Control Laboratory of Athens. Some investigators are trying to develop a urine-based test for human growth hormone, but others question whether this can be done.
The art of sample collection Anti-doping laboratories operate differently from conventional academic ones in a key way: sample collection. “This is one of the few areas of analytical chemistry in which the job of the chemist does not begin with the selection of sample,” says Francesco Botrè at the Anti-Doping Laboratory of Rome. “We don’t select the sample. Somebody else collects the sample for us.” Designated inspectors are assigned to collect urine or blood samples from athletes. One reason to have inspectors who are independent of the laboratories collect samples is to avoid any possibility of bias in the analyses, lest a laboratory technician be a rabid fan of a particular soccer or baseball team. Because the stakes in sports can be so high, specific regulations have to be followed to ensure that an athlete doesn’t try to manipulate or switch samples. Inspectors have to observe the sample collection and be alert for physical manipulations of samples to mask cheating. The attempts include switching a cup of tainted urine with a drug-free one and using prosthetic devices that hold artificial urine. (For an enlightening example, look up “Whizzinator” on the Internet.) On occasion, all water sources to the collection area are cut off so the urine can’t be diluted with tap water.
BALCO was a service for blood and urine analysis and food supplements. But federal agencies started getting tips that Victor Conte, the founder and owner of BALCO, and his cronies were providing high-end athletes and their coaches with designer steroids. Federal investigators spent nights in the dumpsters behind BALCO, looking for empty vials and package inserts, and produced evidence that BALCO dealt in EPO and steroids. USADA also received a spent syringe with a tiny drop of liquid from a locker room floor; an anonymous source said the syringe contained a BALCO product (the source later turned out to be Gatlin’s coach, Trevor Graham). The agency rinsed the syringe out with methanol and gave the rinse to Catlin, who was at the UCLA Olympic Analytical Laboratory at the time. Catlin and colleagues analyzed the rinse by GC/MS and LC/MS/MS and identified THG, known by athletes as “The Clear”. “Don did a great job of working on the identification of the compound,” says Bowers. “We also had some other consultants looking by NMR to verify 3D structures, and we had a group to do some primate drug administration.” In addition, they carried out receptor studies to ensure that THG bound to the androgen receptor. Because the stakes were high, extreme caution was exercised. Bowers recalls, “At one point, we had one of our staff scientists traveling around the country with a vial of material, hand-delivering it, because we didn’t have much and we didn’t want to risk losing it.” Once the evidence was collected, the legal action started. “I remember sitting in my office before we did the first case of Dwain Chambers,” the British 100-m champion, says Bowers. “In the press, reports were out that nobody knew if the stuff was really a steroid or not, if it worked or not. I was sitting there with 3 inches of paper on my desk that answered all of those questions. I thought, ‘Well, you’ll see at the hearing whether or not we know those things!’” Chambers received a 2-year ban and was barred for life from participating in the Olympics. Barry Bonds, Jason Giambi, Marion Jones, and other American athletes also got embroiled in the scandal. The probe eventually found Conte, Bonds’s trainer Greg Anderson, BALCO vice president James Valente, and track coach Remi Korchemny all to be guilty. Chemist Patrick Arnold pleaded guilty for supplying BALCO with THG. Federal agents charged Arnold with distributing steroids through BALCO from 2000 to 2003—he had, at one point, wired a large sum of money to China for ingredients to produce drugs in his Illinois laboratory. Arnold was previously known for introducing the steroid precursor androstenedione to the U.S. That chemical came into the limelight in 1998, when St. Louis Cardinals slugger Mark McGwire admitted he used it while breaking baseball’s single-season home-run record.
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Manipulations can go the chemical route. Sometimes cheating athletes will ingest, along with the drugs, other substances that have similar chromatographic retention times, to mess up the analysis. A classic approach is to take diuretics to make the urine very watery and its constituents very dilute. Athletes taking hormones have been known to dump proteases into the urine sample to disintegrate the protein. The samples, once collected, are sent to the laboratories—during the Olympics, rules stipulate that the laboratories need to be located within 60 km of the competition site. “The samples arrive in [the] laboratory and they are identified by a numerical code, but there is no way for us to trace the identity of the athlete to that code,” says Botrè. Once the samples are in the laboratory, they are fiercely guarded. “There is an entire chain of custody concerned with the integrity of the sample in order to prevent manipulation by anybody,” says Georgakopoulos.
Let the analysis begin! Each athlete’s sample comes to the laboratory split into two bottles, labeled A and B. Sample A is tested immediately, whereas sample B is stored at –20 °C. Because banned substances in sports number in the hundreds, investigators in the anti-doping laboratories don’t search for specific compounds in samples unless they have a reason to do so. Rather, they carry out surveillance, first looking for physical signs of doping and certain classes of compounds. “We may start with testing the acidity of the sample and the density of the sample,” says Cowan. For the remainder of the surveillance, LC/MS or GC/MS is used to search for large classes of compounds. “For example, if you know what an anabolic steroid looks like, you can say, ‘I don’t care about the side chains but just the core of it. If I see a compound that’s related to this core, it might be a drug of abuse,’” says Thevis. This means the screening methods require certified reference standards. “In the best case, it’s a purified standard of the compound, or it’s urine obtained after a controlled administration of that drug by some authorized supplier,” explains Botrè. “We have pretty large libraries for reference and good databases,” says Cowan. “One of the things about the human sport establishment is there is a pretty good network of labs. When Don Catlin’s group identified THG, I knew about it pretty early on. I had a sample of the material pretty quickly.” If sample A tests positive for a prohibited drug and the laboratory is certain that the result isn’t a false positive, the laboratory draws up a report that identifies the drug in the sample and
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gives it to the relevant anti-doping agency. The agency matches the code on the sample to the name of the athlete and informs the athlete of the test result. The party under suspicion inevitably disputes it. “It never happens that the athlete says, ‘I tried to cheat, but congratulations, you’re very smart. This is a wonderful analysis and shows that the anti-doping system works splendidly,’” Botrè drily notes. This is where sample B comes in. The athlete, usually accompanied by lawyers and scientific experts, goes to the laboratory to witness a repeat of the entire analytical procedure to ensure that it’s carried out correctly and fairly. The athlete confirms that the vial containing his or her sample B is sealed and untampered with. The laboratory staff member opens up the vial and repeats the test. If sample B also tests positive for the drug, then the athlete is presumed to be guilty of doping, and legal action is pursued. Experts emphasize that they want to avoid false positives at all costs. “Of course, we want to be as efficient as possible in catching cheating athletes, but we always work with the premise that a false positive is something we never want to see and never want to have,” says Thevis. “If we have doubts about a result, we always report it as negative. Nowadays, the elite athletes earn such large amounts of money that they can afford arbitration in court. That’s something we certainly want to avoid—not only because of the money but also to protect those who aren’t cheating from being falsely accused.” Cowan agrees. Avoiding false positives in the analyses is “what makes it somewhat different from a clinical chemistry environment, where you don’t want false negatives. The patient may be sick, but it’s best to risk extra screening on a person who’s not sick,” he says. “In the sports system, we can’t risk falsely accusing someone.” The other factor that makes a doping analysis more complicated is that it’s often a one-shot deal. “With a clinical patient, it’s possible to do multiple sampling, but generally with the sports cases, it’s a single shot with the single sample you collect,” says Cowan. “There are some exceptions, as in the case of testosterone where you have to do multiple samples, but mainly it’s going to be the result from a single sample. It’s critical that it be analytically accurate.” So the work that goes into a suspicious sample is exhaustive. “When we call a positive case, we have to be exactly on target,” says Catlin. “We have to have a mass spectrum and retention time. We have to have controls and a lot of details to make sure
Anything to win The word “doping” is thought to derive
had ingested brandy and raw eggs and in-
introduced in 1974, so the International
from the Dutch word, dop, for an alcoholic
jected strychnine into his body to boost his
Olympic Committee added anabolic
drink that Zulu warriors consumed to en-
chances of winning the competition.
steroids to its list of prohibited substances
hance their fighting capabilities. The word
The problem grew worse with the in-
in 1976. This caused an increase in the
came into common use early in the 20th
vention of synthetic hormones and stimu-
number of disqualifications in the late
century, although it originally meant the
lants, which have made their way into dop-
1970s, especially in those sports that are
illegal drugging of racehorses.
ing since the 1950s. The Danish cyclist
based largely on strength, such as throw-
Knud Enemark Jensen died during compe-
ing events and weight lifting.
However, boosting one’s performance by taking foreign substances goes back as
tition at the 1960 Rome Olympic Games—
far as the ancient Greeks, who used spe-
the autopsy revealed amphetamine. In
in some countries complicated anti-doping
cial diets and stimulating potions to
1967, cyclist Tom Simpson died during the
control in the 1970s and 1980s. State-sanc-
strengthen themselves. In the 19th century,
Tour de France. These incidents increased
tioned drug use has since been confirmed
strychnine (one of the bitterest substances
the pressure on sports authorities to intro-
in some cases. Top sports officials of the
known), caffeine, cocaine, and alcohol
duce drug tests.
1970s and 1980s from the former German
Suspicions of state-sponsored doping
were consumed by cyclists and other en-
During the 1970s, most international
durance athletes. At the 1904 Olympics in
sports federations started drug testing.
of trials since the 1990s. They stand ac-
St. Louis, the American athlete Thomas
However, anabolic steroids were becom-
cused of ruining the health of their athletes
Hicks won the marathon but then col-
ing more widely used because no way ex-
by forcing them to ingest performance-en-
lapsed. It took hours to revive him—he
isted to detect them. An accurate test was
hancing drugs.
we can prove our case. We prepare documentation packages that are up to 50–100 pages long, showing what we did and how we did it. There’s a lot of work to prove a positive.”
Tracing biomarkers Some experts have suggested that a different tack from the existing structure may prove useful in eliminating doping in sports. They point out that the present system has a rather unpleasant element of “cops and robbers” to it. “The principal focus of the current anti-doping system is one of catching cheaters after the fact,” says Paul Scott at the Agency for Cycling Ethics. He says it would be better to have a system where athletes can go to the starting line or onto the field with a record proved to be clear of doping rather than having suspicions of cheating hover over them while they compete. Investigators such as Catlin and Scott are advocating following biomarkers in samples voluntarily provided by athletes over extended periods of time. The biomarkers can be compounds that are endogenous but have synthetic counterparts that are abused in sports. EPO, human growth hormone, and testosterone are typical examples. A sudden increase in an athlete’s biomarker levels could be an indicator of substance abuse, and the athlete would be flagged before competition. “You want to sit in front of your TV, watch a marathon, and be confident that everyone’s clean. You can’t do that today,” says Catlin. “I’m wondering if there’s a way to induce a shift so that
Democratic Republic have faced a series
athletes take charge and clean it up themselves. Many athletes are clean, but they can’t prove it. The whole point of this [new] system is trying to support the athletes who do compete clean and never will cheat.” The scheme would take into account the natural peaks and dips in a person’s biomarker levels over time. The importance of this provision is illustrated by the case of Eero Mäntyranta, who won three gold medals for cross-country skiing at the 1964 Winter Olympics in Innsbruck (Austria). Throughout his career, he was suspected of blood doping because his red blood cell count was >20% higher than those of other athletes. Thirty years later, scientists tested 200 members of his family and discovered that 50 of them, including Mäntyranta, had a rare genetic mutation that increased their red blood cell counts. Scott also points out that physical stress brought on by training and exercise can trigger changes in biomarker levels that have nothing to do with doping. Some of these changes might trigger false-positive results. By regularly tracking the levels of biomarkers in athletes over a long period of time, investigators will better know how the profiles change in response to a range of parameters. But a lot needs to be done to bring the biomarker system up to speed. “For hormones such as testosterone, we’ve got a lot of good data. We’re already comfortable with incorporating the training stress score and the athlete’s testosterone levels and being able to predict exogenous testosterone and other anabolic agent use,” says Scott. But, for example, “the human growth A U G U S T 1 , 2 0 0 7 / A N A LY T I C A L C H E M I S T R Y
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hormone has a typically wider range of variability. It’s going to take longer to establish a proper protocol. Little is known [about] how human growth hormone moves under stress. We’re going to have to do research as we do the project.” The biomarker profile projects aren’t meant to supplant the anti-doping system now in place. “The current anti-doping system can never tell someone that they’re innocent. Sports really need some positive messages with anti-doping. Athletes would like to say, ‘Hey, I’m clean, and here’s years’ worth of evidence,’” says Scott. “But in the background, you still need the current punitive model of anti-doping, if nothing else, to serve as a check against what we’re doing.”
Getting more sophisticated Experts say that staying ahead of dishonest athletes is one of the biggest challenges they face. The BALCO affair illustrated the level of sophistication in the doping underworld, where chemists, physicians, athletes, and coaches are in cahoots. The investigators are well aware that they are racing against the cheaters to stay abreast of discoveries in areas such as pharmacology and human physiology. “They and we watch the scientific literature fairly closely,” says Bowers. “For example, selective androgen receptor modulators, the so-called SARMs, are molecules that are not steroids, but they affect the steroid receptor in ways that it acts like it’s bound to a steroid. When that information began to be published, suddenly on some Internet sites for bodybuilders in Eastern Europe some of the structures of those molecules started showing up.” Bowers says he’s even more concerned about the kind of information generated by research on the genome and the development of targeted therapeutics based on genomics. “A good example would be myostatin, a protein that was discovered to down-regulate muscle growth,” he says. “There are some cows in Belgium, called Belgian blues, that are deficient in that protein, and they get hugely muscular.” The cows, Bowers explains, led researchers to identify the gene and its protein. Pharmaceuticals are now being developed that will block the action of myostatin. “That’s something that could potentially be used to enhance performance,” he says. Beyond genome-based therapeutics lurks the danger of gene therapy being abused in sports. Experts worry that athletes will go to the extreme lengths of having an extra genetic copy of human growth hormone, EPO, a growth factor, or anything along those lines inserted into their bodies to boost performance. “We know that in the future it would be a very attractive way to dope for some athletes,” says Rabin. “We’re currently working on different approaches and different concepts to ensure that cutting-edge technologies are applied to doping detection in the future.” 5528
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The pharmaceutical industry is also carefully watched by the investigators to keep up with all the new drugs released into the market. Even the illegal pharmaceutical laboratories are tracked. Rabin points out that some of the drugs that BALCO supplied “were, in fact, substances described in the literature back in the 1960s which had never been developed as pharmaceutical products. They were results of pharmaceutical companies creating thousands of molecules to select one or two that would make it into the market. It shows some old substances which have never been developed can be the inspiration for some rogue chemist.” As increasing numbers of compounds are added to WADA’s list of prohibited substances, experts worry about overload. “How many substances can you keep track of or detect at the same time?” asks Rabin. “That’s where we have some technical constraints.” Some of the limitations lie in the sample quantity—there’s only so much urine an athlete can produce for sample collection, and the investigators have to make the best of all the analyses with the limited volume. The detection capability of the current methods and their ability to screen for many compounds also can be restricting factors. “I think we are obligated to start looking into more general analytical technologies, like using TOFMS or bioassays, in order to detect members of entire families of designer steroids,” says Georgakopoulos. Breakthroughs in instrumentation help. “One of the reasons why we had so many positive cases in the 2004 Olympic Games was because they used the latest equipment with higher sensitivity than the [instruments] that were used before,” says Rabin. “The athletes thought it was OK to let their bodies stay clear of drugs for 2–4 days, but in fact, with the new equipment, we were able to pick up drugs for a longer time after administration!” But despite all the effort devoted to identifying, detecting, and analyzing drugs abused in sports, experts say that testing alone won’t keep sports drug-free. They note, as learned from the BALCO case, that it’s helpful for them to collaborate with law-enforcement agencies to cast a wider net and catch cheaters via routes other than testing. The education of athletes and teenagers also plays a critical role—they need to understand that sports are only worthwhile when competitors stay within the boundaries of their innate abilities and that performance-enhancing drugs have serious health-destroying side effects. Experts say it’s critical to nurture the spirit of sportsmanship and not turn sports into a battle of the chemists. Rajendrani Mukhopadhyay is a senior associate editor of Analytical Chemistry.
