Audrey Eldridge brings an inhaler with her whenever she gets in the pool. An elite Masters swimmer from Colorado Springs, she swims between 3,000 and 4,000 meters per day. She notices respiratory effects that can strike depending on the conditions where she’s swimming.
Eldridge hasn’t been diagnosed with asthma, but many elite swimmers have been. In fact, studies have shown a statistically significant link between professional swimming and the respiratory ailment. Professional swimmers like the ones who will dive into the pool at the Summer Olympics this week in Rio de Janeiro can log upward of 10,000 meters per day during training. That’s a lot of time spent exposed to the chemicals in and around swimming pools.
It takes a lot of chemicals to make pool water safe for swimming. Untreated water can accumulate harmful Escherichia coli and Salmonella bacteria and protozoans such as Cryptosporidium parvum and Giardia lamblia. So the disinfection chemicals are necessary for killing pathogens, but at the same time, they don’t just float around inertly in the water: Many of them react with organic material in the water—dirt, sweat, urine, and even skin moisturizers—to form disinfection by-products (DBPs).
The water in pools has to be disinfected to make it safe for swimming. But the disinfectants added to pools aren’t just killing harmful microbes. They’re also reacting with organic matter in the water to form unwanted disinfection by-products. Most of the precursors to those by-products are brought into the water by swimmers themselves. Read on to learn more about where these by-products come from and how they can affect swimmers’ health.
Anybody who goes to a pool is going to be exposed to these DBPs—in the water in the pool or in the air around it. According to studies of drinking water, many of these chemicals can be considered toxic at certain levels. In swimming pools, though, it’s not clear how much exposure to the compounds is enough to cause health effects. What is clear is that elite swimmers and people who work in and around pools are the most vulnerable.
The most common compounds used to disinfect swimming pools are forms of chlorine. Other disinfectants include bromine, ozone, and ultraviolet radiation. They all kill microbes by reacting with and disrupting the function of biomolecules the organisms need for survival. The various disinfectants can be used alone or in combination.
Combinations of disinfectants might be needed because some pathogens are resistant to chlorine. Cryptosporidium—a protozoan that goes by the nickname “crypto” and causes intestinal disease—is more often than not the microbe that causes illness in recreational swimmers, says Ernest R. (Chip) Blatchley III, an environmental engineer at Purdue University who studies water treatment and DBPs. Crypto is resistant to chlorine but sensitive to UV radiation, which doesn’t kill the protozoan but makes it unable to reproduce.
“If you couple UV and chlorine together, you have a strategy that can take care of virtually any microbial pathogen that might be present in pools,” Blatchley says.
UV radiation can’t be used directly in the pool, though, because it would put swimmers at risk for skin cancer. Therefore, the radiation source has to be hidden away inside the water recirculation and filtration system.
“In most pools, water is withdrawn by a gutter system. That water then goes through a treatment system that’s outside the pool. It often involves a sand filter, rechlorination, and maybe pH adjustment,” Blatchley explains. “After treatment, that water is injected right back into the pool.” When UV radiation is used, it is usually applied after filtration and before chlorine injection and pH adjustment.
There is a drawback, however, to using UV radiation as a disinfectant, Blatchley says. The UV radiation breaks nitrogen-chlorine bonds in some DBPs, producing radicals that can help form even nastier by-products such as cyanogen chloride, a toxic agent that can attack respiratory organs (Environ. Sci. Technol. 2013, DOI: 10.1021/es400273w).
“UV systems improve water quality unambiguously in terms of microbiology,” Blatchley says. “In terms of chemistry, there are some compounds whose concentration will go up and some compounds whose concentration will go down” as a result of UV treatment. Overall, the radiation improves the chemistry and microbiology of swimming pools, but there are certain chemicals that you still need to worry about, he adds.
And those chemicals have a chance to accumulate because pools generally recirculate their water. “The water is recirculated over months in a pool,” says Christian Zwiener, a chemist at the University of Tübingen who studies DBPs. The only water that regularly gets replaced in pools is the water lost to evaporation and the water used to flush out the sand filter in the recirculation system, Zwiener explains. That’s enough to comply with the German standard for pool water treatment, which requires replacing 30 L per bather per day to avoid accumulating chemicals. The analogous voluntary standard in the U.S. calls for replacing 15 L per bather per day.
Maarten Keuten, an engineer at Delft University of Technology who studies pools, estimates that about 1% of the water in a pool is lost and replaced each day. That means it takes about 100 days for much of the water in a pool to be replaced—100 days during which DBPs are accumulating.
But how do those DBPs form in the first place? Some building blocks for making the chemicals are already in the tap water that’s used to fill the pool. But most of them are brought along for the ride on or in people using the pool. Some DBP precursors are on the skin: Think hair, skin cells, dirt, or personal care products. Others are in sweat.
But the biggest contributor to DBPs in pools is urine. Researchers estimate that swimming pools contain an average of 30 to 80 mL of urine for each person that’s jumped in. Some of that is released accidentally or without the person realizing.
But for elite swimmers, peeing in the pool is an accepted part of the culture. Eldridge, the Masters swimmer, confirms that peeing in pools is commonplace in elite competitive swimming. It’s a frequent topic of conversation and joking among swimmers.
Practices can last for hours, Eldridge says, and swimmers chug water during stops between intervals. Swimmers rarely leave the pool during that time. “Do you really think that all these people in the pool, exerting at the level they are, drinking as much as they are, don’t have to pee in two hours?” she asks.
Olympic swimmers Michael Phelps and Ryan Lochte have both been captured on video admitting to peeing in the pool and seeing nothing wrong with it. A quick YouTube search turns up multiple such videos highlighting their cavalier attitudes.
That urine contains a lot of urea, a nitrogen-laden molecule that reacts with chlorine in pool water to form a DBP called trichloramine. This resultant chemical—not the chlorine itself—helps give indoor pools their distinctive odor and has been associated with respiratory symptoms.
Keuten divides the sources of human-introduced DBP precursors into three main categories.
“The first part is the loose dirt that is easily rinsed off when people jump into the pool. It’s released within one minute,” Keuten says. This dirt consumes about 30% of the chlorine in the pool water during disinfection, assuming that all of the free chlorine in the water is used up by forming DBPs.
The second category is sweat. The amount that people sweat in pools depends on both the water temperature and their level of activity. In one study, Keuten tested the effect of water temperature on sweating by measuring the sweat production of people wearing water-filled rain suits and exercising on a submerged cross-trainer (Water Res. 2014, DOI: 10.1016/j.watres.2014.01.027). The concept is similar to the activity known as aquaspinning, in which people ride a stationary bicycle submerged in water. (Yes, that’s really a thing.)
In another experiment in the same study, Keuten studied sweat production in swimmers. One group was composed of recreational swimmers exercising at light to moderate levels. In the other group, triathletes swam vigorously. The amount of sweating was measured by weighing the swimmers before and after swimming.
In cold water, “you don’t sweat because the water is cooling your body down and your core temperature doesn’t rise,” Keuten says. Around 27 or 29 °C, “the cooling effect of the pool water is not enough, and your core temperature starts rising.”
In recreational swimmers, sweat is a minor contributor to DBPs, about 5 to 10%, Keuten says. For athletic swimmers it’s much higher—about 40% of chlorine consumption and DBP formation can be attributed to precursors in sweat, which also contains urea.
The third major category is urine. This one is the hardest to pin down because people can be cagey when asked about it. Keuten estimates that peeing in the pool contributes to about 30% of DBP formation. For recreational swimmers, the percentage is probably higher—about 45%—simply because they don’t sweat as much and therefore, percentage-wise, more of their urea gets excreted through urine.
In another study, Keuten provided a shower cabin for people at an outdoor pool to use. People coming straight from home showered in the cabin for two or five minutes, and Keuten collected and analyzed the water that rinsed off participants and drained from the cabin floor (Water Res. 2012, DOI:10.1016/j.watres.2012.04.012).
Later in the day, he asked people lying around the pool to shower again. Participants had been lying around the pool or on the grass, where they had been sweating and picking up dirt.
“Even when they had been showering or swimming earlier in the day, after one hour of lying around they were as dirty as they had been when they first came in,” Keuten says. “It was an eye-opener for me. Outdoor pools really should focus on the personal hygiene of swimmers, not just the first time they jump in, but every time they jump in.”
It’s a delicate balancing act, putting enough disinfectant in a pool to kill pathogens but not putting so much in that excess chlorine reacts to produce high levels of DBPs. Complicating matters is the fact that the level of chlorine needed throughout the day can fluctuate.
There are literally hundreds of—maybe even more—different DBPs in swimming pools. The most abundant of these are trihalomethanes, such as trichloromethane, more commonly known as chloroform; haloacetic acids; and chloramines, especially trichloramine. Haloacetic acids are not volatile, but the rest of the DBPs can be found in the air around swimming pools.
Blatchley uses a method called membrane-introduction mass spectrometry (MIMS) to measure volatile DBPs from the air around swimming pools and at the air-water interface. In MIMS, the compounds undergo a process called pervaporation that allows them to diffuse through the membrane and be swept straight into the mass spectrometer.
MIMS can detect compounds only at microgram-per-liter or higher concentrations, so anything it detects is at a pretty high concentration compared with other DBPs. Blatchley’s team regularly sees the same 11 volatile DBPs—including trihalomethanes, chloramines, and halocyanogens—in almost every swimming pool sample it analyzes.
“Of the volatile DBPs formed in swimming pools, trichloramine is usually cited as the most volatile and has been linked to various adverse human health effects,” Blatchley says. All three of its chlorine atoms are in the +1 valence state. “That molecule is a fairly aggressive oxidant.”
Blatchley points to the heavy corrosion of stainless steel and other metals around pools. “Trichloramine undoubtedly contributes to that corrosion,” he says. “If you have a compound that has the ability to be that aggressive in corroding even stainless steel, it doesn’t sound like something particularly good to be inhaling.”
Volatile DBPs such as trichloramine are the compounds most likely to contribute to respiratory problems in swimmers—if those problems are indeed caused by chemical exposure. And swimming itself probably hastens the athletes’ exposure.
Speaking like a true chemist, Blatchley says: “Swimmers are usually right at the gas-liquid interface.” They’re kicking and splashing, right at the water surface, doing the things that swimmers do, he explains. “Whether they’re competition swimmers or children playing in the water, the majority of the mechanical energy imparted to the water takes place right there.” All that churning of the water speeds up the transfer of DBPs into the air.
But some DBPs aren’t volatile, and others are at low concentrations. Better instruments are allowing scientists to see more and more of those other DBPs. Susan D. Richardson, a water chemistry expert at the University of South Carolina, uses two-dimensional gas chromatography coupled with quadrupole time-of-flight mass spectrometry to identify those DBPs. The two GC columns in Richardson’s instrument allow her and her group to separate many components that would otherwise be difficult to resolve. In one case of water from a brominated pool, the researchers saw more than 19,000 resolved peaks in their chromatogram.
But Richardson and her colleagues can identify only a fraction of the compounds represented by those peaks. “Most of these things are not in the mass spec libraries,” Richardson says. She did, however, identify previously unknown DBPs, including two new brominated imidazoles and other nitrogen-containing DBPs.
Some of the DBPs causing the multitude of chromatogram peaks may be never-before-seen contaminants from new drugs that are peed out by swimmers or new personal care products that rinse off their skin. But “most of them have probably been there the whole time” and had just not been detected, Richardson says.
Xing-Fang Li, a DBP expert at the University of Alberta, has also found previously unobserved DBPs in swimming pools. She found eight halobenzoquinones in swimming pools at concentrations between 19 and 299 ng/L (Environ. Sci. Technol. 2013, DOI: 10.1021/es304938x). The question was where they were coming from. The concentrations in the pool were significantly higher than those in either the input tap water or urine from swimmers. That meant halobenzoquinones must be coming from somewhere else.
When Li and her group did laboratory disinfection studies of several widely available lotions and sunscreens, they found that high levels of halobenzoquinones would accumulate, making those personal care products the likely culprits. The benzoquinones likely come from phenyl-containing molecules in the personal care products.
Benzoquinone is a known carcinogen. Toxicity data collected from cell-based assays show that halobenzoquinones are more damaging than benzoquinones, Li says. They produce a much greater amount of reactive oxygen species in cells, resulting in damage to DNA and proteins, she says.
Knowing that DBPs can cause such effects in cells naturally leads to concerns about the chemicals’ effects on human health. Studies about the effects of DBPs on swimmers “have been focused on highly exposed groups, such as professional swimmers and workers, or vulnerable groups, such as infants and children,” says Cristina M. Villanueva, an epidemiologist who heads the water pollution program at ISGlobal, the Barcelona Institute for Global Health.
“It has been described in many studies that the prevalence of asthma is high among swimmers,” Villanueva says. But the nature of the association is harder to determine. Did those swimmers develop asthma because they swim, or do they swim because they have asthma? One of the complicating factors is that doctors recommend swimming as a sport suitable for people with asthma.
And the effects on children are even less clear. Belgian researchers have shown in a series of studies that swimming as a young child is related to increases in respiratory symptoms and asthma (for example, Environ. Health Perspect. 2006, DOI: 10.1289/ehp.8461). But other scientists couldn’t replicate those results in later studies, Villanueva says. Some of those later studies have even found a protective effect in which children who are exposed to swimming at an early age are less likely to develop asthma. “The children who went to the pool may even have better lung function” than other children, Villanueva says. “The topic of children is not clear at all. It is still quite controversial,” she says.
Villanueva and her colleagues have also tried to determine whether there is a connection between swimming and increased incidence of bladder cancer (Am. J. Epidemiol. 2007, DOI: 10.1093/aje/kwj364). In that study, they saw a twofold increase in bladder cancer among people with long-term exposure to trihalomethanes at pools.
But, Villanueva says, “there’s only one study reporting this. That’s not enough to conclude anything.” She notes that studies have shown that long-term exposure to trihalomethanes in drinking water is associated with an increased risk of bladder cancer, “but there is very little evidence on swimming pools.”
In a recent study led by Villanueva, researchers studied the conditions that might increase how readily swimmers take DBPs inside their bodies. To do that, they measured four trihalomethanes in swimmers’ exhaled breath and trichloroacetic acid in their urine as markers of DBP exposure (Environ. Res. 2016, DOI: 10.1016/j.envres.2016.05.013). The team took samples before and after the swimmers exercised in a chlorinated pool for about 40 minutes.
They found that the levels of trihalomethanes and trichloroacetic acid—standard DBPs used as indicators for all disinfection by-products—both went up after swimming.
So the more you exercise and the harder you breathe, the more DBPs you’re likely to take up. And the more people that pee in the pool, the more likely it is for there to be high DBP levels.
Professional swimmers are the most likely to be affected by DBPs, both because of the amount of time they spend around pools and because of their propensity to pee in the pool. They’re also the ones who are best positioned to do something about it.
“High-profile swimmers have a real opportunity to take a position of leadership and responsibility,” Blatchley says.
And the best way to do that is to change the culture. “The best thing that swimmers could do to improve the swimming environment for themselves and for everybody else who uses the pool—the lifeguards and other people who are walking around on the pool deck—is to practice commonsense hygiene,” Blatchley says. That means taking a shower before getting in the pool and refraining from peeing in it.
That won’t eliminate all DBPs, especially among competitive swimmers who sweat a lot when they’re in a pool, he says. But taking a shower reduces things like “skin moisturizing factor,” a group of organic compounds, including urea, that allow skin to stay hydrated. “Even if you’re ‘clean,’ you’re going to be rinsing off things that would otherwise be rinsed off when you hop in the pool.”
And no one is suggesting that people give up swimming. “Swimming is the only sport that I know of that you can do within a few weeks after you are born and you can keep on doing until the day you die, without overloading your muscles or joints,” Keuten says. “Swimming is healthy, and research will make it even better.”
With some of that research in mind, maybe the swimmers in Rio will think twice before they decide to pee in the pool.