Leading Article
Sports Medicine 3: 235-241 (1986) 0112-1642/86/0007-0235/$3.50/0 © ADIS Press Limited All rights reserved.
Exercise and Malignancy Roy J. Shephard School of Physical and Health Education and Department of Preventive Medicine and Biostatistics, University of Toronto, Ontario
The two most common causes of death in adult life are cardiovascular disease and various forms of malignancy. Much has been written on exercise and cardiovascular disease [see Shephard (1981-86) for reviews], but our knowledge of exercise and the risks of malignancy is extremely limited (Polednak 1976). Paffenbarger et al. (1985) did not observe any obvious relationship between exercise and malignancy in their longitudinal study of former Harvard alumni; their data explored both university participation and current activity. In contrast, Polednak (1972, 1976) indicated that former 'letter holders in major university sports had a slightly above average risk of dying from neoplasia'. Before concluding that a specific type of sports participation caused this phenomenon, it is necessary to evaluate several alternative hypotheses, including selection of the university athlete (by the bodybuild needed for the sport and by an excess ofcardiac deaths in non-athletes), the impact of the athletic environment (trauma, ultraviolet-radiation, and exposure to noxious chemicals) and lifestyle effects (diet, smoking habits, alcohol consumption and the health behaviour of the athlete versus the non-athlete).
1. Overall Impact 1.1 Animal Experiments
In contrast to human data, animal studies (Hoffman et al. 1960;Newton 1965;Rusch & Kline
1944) suggest beneficial effects of enhanced physical activity in retarding the subsequent growth of tumours (although most reports discuss experimentally-induced rather than spontaneous lesions). An early paper by Milone (1928) claimed that exerciseretarded sarcoma growth in rats. Rusch and Kline (1944) likewise noted that physical exercise retarded the growth of fibrosarcomas in albino mice. Sivertsen and Hastings (1938) found that a combination of dietary restriction and 2 hours of running per day reduced the incidence of mammary gland tumours in albino mice from 88 to 16%. Other reports confirmed that the growth of Walker256 tumour was faster in restrained than in unrestrained rats (Hoffman et al. 1960), and that progression of Ehrlich's adenocarcinoma was decreased when albino mice were allowed unrestrained ambulation (Suchorukich 1959). In theory, exercise might act by modifying energy balance, but at least one report has suggested that benefit is independent of any effect on bodyweight (Edington et al. 1972). Unfortunately, there remain serious difficulties in applying the results of animal research to humans. While the intensity of physical activity may mimic that of an athlete, many inbred species of laboratory animals have a high incidence of terminal carcinogenicchange. Laboratory diets are also very different from those eaten by either the human athlete or the free-living animal. Finally, there are obvious obstacles to a matching of both initial
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Exercise and Malignancy
age and the duration of any exercise or dietary manipulation relative to the slow time course of human malignancies. 1.2 Human Studies There is little possibility of direct human experimentation and thus most of the human evidence is drawn from epidemiological studies, with all of their inherent limitations. The first human study was apparently by Sivertsen and Dahlstrom (1921). They reviewed the occupations of 3135 men who died of malignant tumours, and found a lower incidence in occupations that demanded heavy musculoskeletal activity. However, at the time of their study, it is probable that cigarette smoking was more popular among the sedentary upper socio-economic groups than in labourers; tobacco addicts among the latter group would have chewed tobacco or smoked a pipe rather than cigarettes. Taylor et al. (1962) have also supported the concept of an association between malignancy and a sedentary job. Burian (1954) made a retrospective analysis of 160 patients with malignant gastric tumours, and found that only 11% had been active gymnasts or athletes in the past. At first inspection, this seems a low proportion of active individuals, but in fact it may be a fairly high incidence for a population where most people are inactive. Schmid (1975) examined postmortem data on 780 Czechoslovakian athletes who died a non-accidental death; 27.9% of this group had been treated for malignant tumours, with necropsy confirmation of the diagnosis. Carcinomas accounted for 86.4% of the neoplasms. Data were also accumulated from several other studies, with malignancies accounting for 8.8 to 18.4% of deaths (table I). Schmid offers no explanation as to why he found such a high incidence of malignancies (a 5-fold increase over earlier authors in the case of soccer), and unfortunately no data is provided for age-matched controls. Polednak (1976) obtained death certificates on 8393 men who had spent 2 or more years at Harvard College from 1860-89. The incidence of fatal malignancy among former athletes was as reported
in most of the earlier studies with the exception of Schmid. Polednak (1972, 1976) included agematched controls, demonstrating a small but statistically significant disadvantage among those who had participated in major sports (baseball, football, track, crew, ice-hockeyand tennis). However, there are obvious limitations with the use of death certificates. A further important weakness in the data is that the controls had also applied for athletic locker space indicating that although they did not receive an athletic 'letter', there is no proof that they were any less active than those involved in the major sports. Moreover, Polednak (1976) was unable to provide data on either exercise or lifestyle behaviour in the 40 to 50 years that followed completion of the individual's university education.
2. Influence
0/ Athletic Selection
One immediate difficulty in comparing the incidence of malignancy between athletes and nonathletes, or between active and inactive occupations is that of self-selection. In general, both the athlete and the heavy worker choose to become involved in regular physical activity, and often this selective pressure is enhanced by the coach or the personnel manager. 2.1 Bodybuild American sports such as basketball and football attract subjects with extreme bodybuilds. Likewise, in industry, obese men gravitate to sedentary jobs (Morris et al. 1956),while the astute mine manager recruits heavily-muscled miners (Wyndham 1966). The impact of constitution upon the risk of cancer may have been overstated, since immigrants to the US quickly assume a mortality typical of their new environment (Haenszel 1961). Nevertheless, animal experiments suggest that obesity increases the risk of some neoplasms (Heston & Vlahakis 1962), while bodysize also influences susceptibility to lung tumours (Bloom 1964). In humans, it is not always clear whether excess body mass should be attributed to fat or to muscle.
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Exercise and Malignancy
Table I. Incidence of fatal malignancy in various classes of athlete (based largely on data accumulated by Schmid 1975)
Type of athlete
Sample size
Incidence of fatal
Reference
malignancy % Gymnasts Rowers
232
8.8 9.4
Bickert (1929)
32
Soccer players
100
9.0
Mervennee (1944)
Cricketers Track and field athletes
99 110 130 100
10.1
66
14.0
Montoya et al. (1956)
200 105 780
44.5 13.3 27.9
Schmid (1975)
Major athletes Minor athletes
845 1776
15.2 13.3
Polednak (1976)
Controls
5772
12.3
Rowers Rugby players University 'letter holders' Soccer players Gymnasts All athletes
However, death from certain types of tumour seems more prevalent in those who are 'overweight' (Tannenbaum 1940). Tumours where this effect has been demonstrated include endometrial cancer (Damon 1960) and breast cancer in females (Valaoras et at. 1969) but not prostatic cancer in males (Greenwald et at. 1974). The general relationship between malignancy and weight for height has a U-shaped form (Dyer et at. 1975). Polednak (1976) attempted to match major athletes with non-athletes of similar bodysize. Unfortunately, 31 of the athletes were too large to find a control of comparable height and body mass. A total of 650 athletes were matched to within 3cm and 3kg. In this sample, the disadvantage of the athletes persisted (incidence of 19.2 versus 16.6%), but was no longer statistically significant. Weight and age of death from neoplasia were negatively correlated for major athletes (r = -0.24, p < 0.01), but not for minor athletes or non-athletes. 2.2 Other Aspects of Selection Athletes may also be selected because of hormonal or psychological characteristics. A high level
Rook (1954)
13.6 18.4 12.0
of androgen secretion may contribute to both the muscular development and the aggressiveness of a football player. While administration of synthetic androgens and oestrogens can have a substantial effect upon the incidence of some type of cancer, Greenwald et at. (1974) found no evidence ofa relationship between morphometric masculinity and prostatic cancer. On the other hand, Polednak (1976) noted that the risk ofa prostatic malignancy was particularly high among athletes (table II). Mood-state can plainly influence the course of the disease and the age of death once carcinogenic change has occurred (Pearson 1978). Exercise has an immediate mood-elevating effect (Shephard 1983) in both the healthy person and the cancer victim. However, it is also likely that the depressed person will avoid sport and physical activity, and there may be importance in the suggested linkage between jogging, mood-state, T-lymphocyte function, and risk of carcinogenesis (Simonton 1978).
3. Environmental Effects 3.1 Trauma Many forms of athletic participation carry a fairly high injury rate. This could conceivably in-
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Exercise and Malignancy
Table II. Mortality rates from malignant neoplasms at specific sites (based on death certificate data of Polednak 1976) Site
Mortality rate from malignant neoplasm (%)
major athletes
nonathletes
Mouth and pharynx
0.7
0.5
Digestive tract
5.4
4.9
Respiratory tract
1.5
1.4
Breast and genito/urinary
4.4
3.1
Lymphatic/haemopoietic
1.1
1.1
Other/unspecified
1.5
0.9
fluence the rate of cell regeneration and thus increase the risk of malignant change. There are at least 2 potential fallacies in seeking an effect of trauma: firstly, development of a neoplasm may have sharpened the patient's memory of an earlier injury, and secondly, there may have been substantial exposure to X-irradiation as a consequence of injury. A case study of meningiomas by Walsh et a1. (1969) suggested that head injury might be a factor predisposing to such malignancies, and this hypothesis was confirmed in a case-control study of women with intracranial meningiomas (PrestonMartin et a1. 1980). A further case-control study of 105 male meningiomas (Preston-Martin et a1. 1983) found a significant excess in the number of boxers (p = 0.03), serious head injuries (p = 0.01) and xray treatments of the head (p = 0.02) among the patients. The history of boxing was volunteered in the context of a more general question about sports participation, lessening the likelihood of enhanced memory. Moreover, 4 cases and no controls volunteered the information that they had at one time been professional or serious amateur boxers. A second area vulnerable to injury in some forms of sport is the scrotal sac. Both horse-riding and cycling seem associated with an increased in-
cidence of testicular seminoma (Coldman et a1. 1982). This effect persists after control for such variables as crypto-orchidism, juvenile-onset inguinal hernia, age and year of diagnosis (table III). It remains arguable that the specific activity and/or related trauma has provided a trigger to diagnosis, moreover, while both cycling and horse-riding expose the testes to direct and persistent trauma, they cause contact with dyes and water-proofing chemicals used to treat the leather of saddles. The risk from trauma thus remains suggestive but unproven. 3.2 Ultraviolet Radiation Many sports are played out of doors, and thus involve the participant in an increased exposure to ultraviolet radiation (Epstein 1985; Hanke 1985). Because of cooling by water, wind and spray, the risks are particularly great with those swimming and sailing in hot climates. Unfortunately, only a small proportion of the population are aware of this risk (Draugsvold 1980), and few realise that shallow water offers little protection against bright sunlight. The hazard seems particularly acute in Australian swimmers; Schmid (1975) noted only 30f218 malignant tumours of the skin in his study of Czechoslovakian athletes. Polednak (1976) had only a 1.5%incidence of 'other or unspecified' tumours Table III. Risk of testicular seminoma in relation to selected sports (based on data of Coldman et al. 1982) Variable and sport
Odds ratio
Significance
Cycling
1.99
0.037
Horse-riding
3.31
0.006
Motor-cycling
1.04
NS
Soccer
1.11
NS
4.56
0.008
Cycling
+ horse-riding
Groin injury while horse-riding
0.079
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Exercise and Malignancy
and commented that most of the excess that he found was in the prostate or the colon. 3.3 Chemical Hazards
There have been reports that large doses of androgen will induce hepatic carcinoma (Daniel & Bennett 1977; Johnson 1975). The widespread abuse of steroids by athletes - particularly those involved in power sports - could thus be increasing the risk of hepatic tumours. Frasier (1973) found no effect. But given the time course of steroid abuse, and the likely latency of the hepatic carcinoma, this may become of greater importance in the future. It is not always easy to distinguish between primary and secondary tumours, but even in 1975 Schmid reported that 10 of 218 tumours among athletes were thought to have originated in the liver. Among soccer players (a group who have reputedly abused steroids) 4 of 89 tumours had a hepatic origin. Polednak (1976) also noted an excess of 'other digestive' tumours (3.8 versus 3.3%) in major athletes. Participation in sport may lead to incidental contact with hazardous chemicals. The issue of the materials used to treat leather has been noted above. A particular hazard in some older facilities, e.g, pools and gymnasia, is an exposure to asbestos fibres (Penman 1980). While exercising, the respiratory minute volume is increased manyfold, and there is a corresponding increase in the quantity of carcinogenic urban pollutants that are inhaled. The problem is exacerbated by a shift from nasal to oronasal breathing (Niinimaa et al. 1980) so that the normal mechanism for the filtration of particulate matter and soluble vapours from the inspirate (Oberst 1961) is largely bypassed.
4. Lifestyle Factors 4.1 Smoking Habits
Given the powerful influence of cigarette smoking (US Surgeon General 1982) and alcohol consumption (Bright-See 1985) upon various forms of malignant disease, participation in physical activ-
ity and sport could modify the risk of carcinoma by altering personal lifestyle. Karvonen et al. (1974) noted that cross-country ski champions lived 4 to 5 years longer than their contemporaries, and they attributed much of this benefit to the fact that the majority of skiers were lifelong non-smokers. Morgan et al. (1976) found that participants in the Masters' track and field events were rarely current smokers and that involvement in distance running events had apparently helped many of the athletes to quit a cigarette habit. However, the key to such abstinence seems lifelong sports involvement. Montoye et al. (1956) observed that by the "time they reached middle-adult life, the number of cigarette smokers was greater among the Athletic letter holders from Michigan State University than among non-athletic controls. Likewise, there was a higher proportion of regular drinkers of alcohol among the former athletes. The magnitude of these differences in lifestyle was relatively small, and it is not surprising that Polednak (1976) found no significant excess of either respiratory (1.5 versus 1.4%) tumours or digestive (5.4 versus 4.9%) malignancies among major athletes. However, Schmid (1975) reported that 54 of 218 malignancies were in the respiratory system of former Czech athletes (25% of all tumours). Coldman et al. (1982) questioned testicular melanoma patients about their smoking habits, including the number of cigarettes smoked and years of smoking, but they found no differences between patients with a history of cycling, horseback riding or soccer playing and matched controls. 4.2 Diet
Athletic participation modifies both the quantity and the quality of the diet. While some female gymnasts and figure skaters eat less than a desirable amount of food, the typical 'letter winner' at a major US university has a high energy, proteinrich diet. In contrast, the middle-agedjogger is often a very health conscious individual, eating a prudent diet with a high fibre and vitamin content. There have been suggestions, not unanimously ac-
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Exercise and Malignancy
cepted, that such discrepancies could have an important influence upon the risk of carcinoma (Burkitt 1978; Harris 1979). One factor with an adverse impact upon the meat-eaters is the use of nitrites in preservation, with the potential for formation of nitrosamines (Ishida et al. 1975; Koestner et al. 1975). A second adverse influence may be the use of oestrogens in fattening livestock. In contrast, a high fibre diet appreciably reduces the risk of gastrointestinal carcinoma. Schmid (1975) found about 37% of tumours in Czech athletes were occurring in the gastrointestinal tract. This compares closely with the 40% found for non-athletes (Polednak 1972) and the 36% for major athletes in his US study. Some studies of animals have suggested that a high overall energy expenditure has an adverse effect upon life-expectancy, possibly by increasing the endogenous production of mutagenic free radicals (Shephard 1978). 4.3 Health Behaviour Schlueter (1982) noted that women who exercised regularly were less informed about breast cancer than their sedentary counterparts. She advanced the hypothesis that the practice of other forms of health behaviour may have reduced belief in the susceptibility to cancer. Possibly for this reason, her sample of exercisers did not practice selfexamination of the breast more frequently than controls. However, it is more usual to find exercise clustering with other positive health practices (Blair et al. 1985), and Turnbull (1978) did find an association between breast self-examination and regular exercise.
5. Conclusion Given the many possible factors influencing the risk of malignancy, it is unlikely that there will ever be a simple answer to the question: does regular exercise increase or decrease the chances of death from cancer? On the other hand, a better understanding of the variables involved permits the encouragement of positive features of sport such as
improved lifestyle, while guarding against some of the more obvious negative aspects of vigorous activity, e.g. increased exposure to ultraviolet light, urban air pollutants, and x-rays (in the event of physical injury).
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Author's address: Professor R.J. Shephard, Director, School of Physical and Health Education, 320 Huron Street, Toronto, Ontario M5SlAI (Canada).