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Early Cardiovascular Mortality in Professional Football Players: Fact or Fiction?

      Abstract

      Present data about the increased incidence of early cardiovascular disease and mortality in National Football League (NFL) players is conflicting. These findings are particularly concerning given the escalating weight of current football players at the high school, collegiate, and professional levels. Recent studies have confirmed that heavier former NFL linemen have an increased prevalence of cardiovascular disease compared with an age- and sex-matched reference population. Former linemen had a higher prevalence of obesity, lower high-density lipoprotein cholesterol, increased left ventricular mass and left atrial area, and the metabolic syndrome, compared with nonlinemen. There have been sparse data on the cardiovascular health of current players. A recent analysis of one team demonstrated that the cardiometabolic syndrome and its individual components were significantly more common in linemen versus nonlinemen. Because current heavier NFL players already have evidence of the cardiometabolic syndrome and its individual markers, careful medical evaluation of former and active players is warranted to reduce their risks. This medically and ethically indicated intervention, however, might limit interpretation of future longitudinal studies designed to assess mortality endpoints.

      Keywords

      Since the 1990s, American football has become the most popular spectator sport in the US, with millions of fans attending or viewing grade school, high school, collegiate, semi-professional, and professional games. This popularity has carried over to the athlete as well. Mueller estimates that there were 1,800,000 total football participants in the US for the 2007 football season.
      • Mueller F.O.
      • Colgate B.
      Annual survey of football injury research 1931-2007.
      • The average weight of football players at the high school, collegiate, and professional levels, has steadily increased over the past 2 years.
      • The increased weight of current players is concerning because studies, though fraught with methodological flaws, have demonstrated increased risk of the metabolic syndrome and possible early cardiovascular death in former players.
      • Current heavier professional football linemen already demonstrate evidence of the cardiometabolic syndrome and its individual components.
      The price of increased popularity and participation is increased scrutiny and responsibility. Football is a collision sport and obviously fraught with the risk of injury and death. With singular dedication to achieve success, bigger, stronger, and faster is today's mantra for the athlete. The strategies to achieve these goals have further complicated the medical risk associated with football. Fortunately, catastrophic injury rates as reported by Mueller in the Annual Survey of Football Injury Research have stabilized since the 1990s.
      • Mueller F.O.
      • Colgate B.
      Annual survey of football injury research 1931-2007.
      Musculoskeletal injury rates, however, remain notable at all levels of play,
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      and the increase in participation should only continue to result in increased injuries.
      Recently, cardiovascular disease has become prominent in the discussion of risks to football athletes. As a result of concerns about early mortality in National Football League (NFL) players, the NFL Players Association requested that the National Institute for Occupational Safety and Health (NIOSH) formally evaluate the health status of 6848 retired NFL players who played from 1972-1988. In 1994, Baron
      • Baron S.
      • Rinsky R.
      National Institute for Occupational Safety and Health
      NFL Mortality Study.
      reported that the NIOSH review demonstrated football players overall had a standard mortality ratio of 0.54, corresponding to a 46% decreased rate of death compared with the “general population of males of similar age.” Despite the lower overall mortality risk among all NFL players, the NIOSH study revealed that offensive and defensive linemen had a 52% greater risk of dying from heart disease than “the general population.” Cardiovascular mortality of linemen was 3 times that of nonlinemen. Furthermore, players in the “largest body size” category, 64% of all linemen, had a 6-times greater risk of developing heart disease than those of “normal size.”
      The NIOSH analysis was limited, as the sample population was of convenience, and the study group contained predominantly young men, with few individuals beyond the age of 50 years. The average age of death was not known and will not be known for many years. The NIOSH study did not investigate risk factors other than obesity in their assessment of cardiovascular risk among players. Therefore, it is possible that other factors such as hypertension and dyslipidemia in heavier linemen contributed to the increased cardiovascular risk in this subgroup. Thus, the lower mortality risk among all NFL players noted in the study might be confined to the apparently healthier nonlinemen who were not overweight or obese.
      This report temporarily dispelled the concern that football players die at a younger age. In 2005, an NFL lineman collapsed and died in the locker room following a game. An autopsy report revealed the cause of death to be ischemic heart disease.
      • Hargrove T.
      • et al.
      Supersized in the NFL: many ex-players dying young.
      This catastrophic event, along with other cases of sudden cardiac death in active and retired professional football players, sparked concern about players' health and mortality risk. The Scripps Howard News Service in 2006 reported that football players were more than twice as likely as baseball players to die before the age of 50 years.
      • Hargrove T.
      • et al.
      Supersized in the NFL: many ex-players dying young.
      The Scripps analysis also demonstrated that 28% of “obese” NFL players died before their 50th birthday, in comparison with 13% of players who were not obese. Twenty-two percent of deaths among NFL players were attributed to cardiovascular disease. Offensive and defensive linemen had a 52% greater risk of dying from heart disease compared with “the general population.”
      • Hargrove T.
      • et al.
      Supersized in the NFL: many ex-players dying young.
      While the analysis suffered from limitations of a retrospective methodology and lack of precise definitions, the observations could not be ignored.
      Nicholas et al
      • Nicholas S.J.
      • Nicholas J.A.
      • Nicholas C.
      • et al.
      The health status of retired American football players: Super Bowl III revisited.
      in 2007 supported the primary conclusion reached by the NIOSH study. Nicholas found that current SF-36 (widely accepted questionnaire comprising 36 separate questions about physical and mental health) scores of 36 former players from the 1969 Super Bowl winning team were similar to age- and sex-matched population norms. These data may not be entirely applicable to current players, as the average weights of NFL players, particularly linemen, have steadily increased over the past 2 decades. Furthermore, the analysis may be somewhat biased, as the information was obtained through a survey format.
      To further investigate the cardiovascular health of former players, Miller et al
      • Miller M.A.
      • Croft L.B.
      • Belanger A.R.
      • et al.
      Prevalence of metabolic syndrome in retired National Football League players.
      studied the metabolic syndrome and its individual components in 510 retired football players. In this study, metabolic syndrome was defined as body mass index (BMI) >30 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      and 2 or more of the following parameters: systolic blood pressure ≥130 mm Hg, diastolic blood pressure ≥85 mm Hg, or treatment for known hypertension; high-density lipoprotein (HDL) cholesterol <40 mg/dL; fasting plasma glucose ≥100 mg/dL or a history of type 2 diabetes; or fasting triglycerides ≥150 mg/dL. BMI >30 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      , reduced HDL, elevated fasting glucose, and the metabolic syndrome were significantly more prevalent in linemen compared with nonlinemen. Miller evaluated a former player population for cardiovascular risk factors and did not analyze whether current players have the same cardiovascular risk factors. Furthermore, this study did not demonstrate that the higher prevalence of the metabolic syndrome among heavier linemen necessarily translated into an increased cardiovascular mortality.
      Croft et al
      • Croft L.B.
      • Belanger A.
      • Miller M.A.
      • et al.
      Comparison of National Football League linemen versus nonlinemen of left ventricular mass and left atrial size.
      compared echocardiographic characteristics between linemen and nonlinemen among 487 retired NFL players. Retired linemen had significantly increased left ventricular mass and left atrial area compared with nonlinemen. Furthermore, BMI, player position as a linemen, and systolic blood pressure were all independent predictors for increased left ventricular mass. The investigators hypothesized that these “cardiac adaptations may contribute to the higher incidence of cardiovascular disease in retired linemen.”
      Recently, Mayo Clinic physicians reported that 82% of 233 retired NFL players <50 years of age had either plaque or carotid narrowing on neck Doppler studies.
      Retired NFL players at increased risk for heart problems Science Daily.
      Adjusted for age, sex, and race, this finding placed them in the 75th percentile for carotid disease. Although this study does not pertain specifically to cardiac risk, it does demonstrate increased atherogenesis in young retired NFL players.
      While the above studies have scientific weaknesses limiting possible inference of a casual relationship, the higher rate of heart disease among former linemen is concerning, particularly because the average weight of NFL players has increased. The Scripps Howard News Service report showed that the average weight of players has increased by 10% since 1985 to an average of 248 pounds in 2006.
      • Hargrove T.
      • et al.
      Supersized in the NFL: many ex-players dying young.
      The number of NFL players who weighed 300 pounds or more has increased from 39 in 1992 to 552 in 2005. The high prevalence of presumed obesity, defined traditionally as a BMI >30 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      , in the NFL also has been described by Harp et al.
      • Harp J.B.
      • Hecht L.
      Obesity in the National Football League.
      The authors evaluated 2168 NFL players from the 2003-2004 season. Fifty-six percent of players had a BMI ≥25 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      , and 26% had a BMI ≥30 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      . The percentage of NFL players with a BMI ≥30 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      was more than double the percentage among 20-39-year-old men in the National Health and Nutrition Examination Survey (NHANES).
      Legitimate concerns, however, have been raised that BMI may not be an accurate measure of obesity in muscular athletes. Waist circumference and waist-to-height ratio have been postulated to be better indicators of obesity in this population than BMI, and more accurately predict risk for cardiovascular disease.
      • Vega G.L.
      • Adams-Huet B.
      • Peshock R.
      • et al.
      Influence of body fat content and distribution on variation in metabolic risk.
      • Gelber R.P.
      • Gaziano J.M.
      • Orav E.J.
      • et al.
      Measures of obesity and cardiovascular risk among men and women.
      While the above studies investigated the health of former NFL players, there has been little research investigating the cardiovascular health of active NFL players. This is particularly germane given the increasing size of current players. In an analysis of 52 players, George et al
      • George C.F.
      • Kab V.
      • Levy A.M.
      Increased prevalence of sleep-disordered breathing among professional football players.
      demonstrated that current linemen had increased blood pressure compared with other players. The higher prevalence of hypertension in linemen may be multi-factorial. Strength training has been shown to increase arterial stiffness and decrease compliance.
      • Bertovic D.A.
      • Waddell T.K.
      • Gatzka C.D.
      • et al.
      Muscular strength training is associated with low arterial compliance and high pulse pressure.
      Nonsteroidal anti-inflammatory drug use, common in athletes, has been associated with hypertension.
      • Antman E.M.
      • Bennett J.S.
      • Daugherty A.
      • et al.
      Use of nonsteroidal anti-inflammatory drugs: an update for clinicians: a scientific statement from the American Heart Association.
      Sleep-disordered breathing also is more common in linemen and associated with increased blood pressure.
      • George C.F.
      • Kab V.
      • Levy A.M.
      Increased prevalence of sleep-disordered breathing among professional football players.
      Finally, increased salt intake and supplements in athletes, and the disproportionate number of black players in the NFL may play a role in the noted increased frequency of hypertension.
      • Androgue H.J.
      • Madias N.E.
      Sodium and potassium in the pathogenesis of hypertension.
      Selden et al
      • Selden M.A.
      • Helzberg J.H.
      • Waeckerle J.F.
      • et al.
      Cardiometabolic abnormalities in current National Football League players.
      have previously described the waist-to-height ratio >0.5, triglycerides-to-HDL ratio >3.5, and the presence of the cardiometabolic syndrome and its individual markers in 69 current active NFL players from one team. Triglycerides-to-HDL ratio >3.5 was used as a marker of insulin resistance.
      • Kannel W.B.
      • Vasan R.S.
      • Keyes M.J.
      • et al.
      Usefulness of the triglyceride-high-density lipoprotein versus the cholesterol-high-density lipoprotein ratio for predicting insulin resistance and cardiometabolic risk (from the Framingham Offspring Cohort).
      • Cordero A.
      • Laciaustra M.
      • Leon M.
      • et al.
      Comparison of serum lipid values in subjects with and without the metabolic syndrome.
      • McLaughlin T.
      • Abbasi F.
      • Cheal K.
      • et al.
      Use of metabolic markers to identify overweight individuals who are insulin resistant.
      In this study, the cardiometabolic syndrome was defined by the presence of 3 or more of the following markers: blood pressure ≥130/85 mm Hg; fasting glucose ≥100 mg/dL; triglycerides ≥150 mg/dL; waist circumference ≥100 cm; and HDL cholesterol ≤40 mg/dL. Blood pressure ≥130/85 mm Hg and glucose ≥100 mg/dL were significantly more prevalent among active players than an age- and sex-matched reference population from the NHANES 1999-2002, although cardiometabolic syndrome prevalence was similar in both groups. In a subgroup analysis, the cardiometabolic syndrome, waist circumference ≥100 cm, and waist-to-height ratio >0.5 were significantly more common in the linemen subgroup versus the nonlinemen. A small sample of convenience and other confounding variables limited the conclusions of this study.
      In a separate analysis, the same authors evaluated the presence of alanine aminotransferase (ALT) ≥30 IU/L in this same group of current NFL players from one team (accepted for publication). ALT is often used as a surrogate marker for the presence of nonalcoholic fatty liver disease in the appropriate setting.
      • McKimmie R.L.
      • Daniel K.R.
      • Carr J.J.
      • et al.
      Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for Type 2 diabetes.
      • Ioannou G.N.
      Implications of elevated serum alanine aminotransferase levels: think outside of the liver.
      Recent studies have demonstrated that an elevated ALT is a biomarker for the future development of diabetes, the metabolic syndrome, and coronary heart disease even after adjustment for adiposity and relevant metabolic parameters.
      • Ioannou G.N.
      Implications of elevated serum alanine aminotransferase levels: think outside of the liver.
      • Ioannou G.N.
      • Weiss N.S.
      • Boyko E.J.
      • et al.
      Elevated serum alanine aminotransferase activity and calculated risk of coronary heart disease in the United States.
      • Schindhelm R.K.
      • Dekker J.M.
      • Nijpels G.
      • et al.
      Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study.
      • Goessling W.
      • Massaro J.M.
      • Vasan R.S.
      • et al.
      Aminotransferase levels and 20-year risk of metabolic syndrome, diabetes, and cardiovascular disease.
      • Vozarova B.
      • Stefan N.
      • Lindsay R.S.
      • et al.
      High alanine aminotransferase is associated with decreased hepatic insulin sensitivity and predicts the development of type 2 diabetes.
      ALT levels were collected from all players. Forty-seven percent of linemen had an ALT ≥30 IU/L, compared with 12% of nonlinemen. An elevated ALT was significantly associated with the following components of the cardiometabolic syndrome: blood pressure ≥130/85 mm Hg and waist circumference ≥100 cm. ALT ≥30 IU/L also was significantly associated with a marker of insulin resistance, triglycerides-to-HDL ratio >3.5. Thus, an elevated ALT may potentially serve as a marker for the future development of ischemic heart disease, obesity, insulin resistance, and liver disease in current football players, as demonstrated in other populations.
      • Ioannou G.N.
      Implications of elevated serum alanine aminotransferase levels: think outside of the liver.
      • Ioannou G.N.
      • Weiss N.S.
      • Boyko E.J.
      • et al.
      Elevated serum alanine aminotransferase activity and calculated risk of coronary heart disease in the United States.
      • Schindhelm R.K.
      • Dekker J.M.
      • Nijpels G.
      • et al.
      Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study.
      • Goessling W.
      • Massaro J.M.
      • Vasan R.S.
      • et al.
      Aminotransferase levels and 20-year risk of metabolic syndrome, diabetes, and cardiovascular disease.
      • Vozarova B.
      • Stefan N.
      • Lindsay R.S.
      • et al.
      High alanine aminotransferase is associated with decreased hepatic insulin sensitivity and predicts the development of type 2 diabetes.
      The study must be interpreted with caution because of a small convenience sample population. Since acceptance of this manuscript, Tucker et al,
      • Tucker A.M.
      • Vogel R.A.
      • Lincoln A.E.
      • et al.
      Prevalence of cardiovascular disease risk factors among National Football League players.
      in the best study to date, recently reported a “lower prevalence of impaired fasting glucose, less reported smoking, a similar prevalence of dyslipidemia, and a higher prevalence of hypertension” in current NFL players compared to their reference population. This large convenience study involving several teams demonstrated increased size, as measured by BMI, to be associated with “increased blood pressure, low density lipoprotein cholesterol, triglycerides, and fasting glucose”; and also to be associated with decreased HDL cholesterol.
      Despite limitations, the above studies reported that former and current heavier NFL players have some evidence of the cardiometabolic syndrome and its individual components. While longitudinal studies are warranted to definitively answer the question of increased cardiovascular risk, careful medical evaluation of active and retired players is now even more warranted. Those athletes found to be at risk for future cardiovascular complications can undergo interventions including both behavioral and medical therapy. This is particularly important after their playing careers have concluded, when their risk increases from decreased physical activity and an associated decrease in HDL levels. Present retirees who exercise report lower body weights, lower BMI, and lower prevalence of hypertension, similar to the general population.
      Center for the Study of Retired Athletes
      News.
      While previous studies have pertained to NFL players, there has been little scientific investigation of the health risks of high school- and collegiate-level football players. Like NFL linemen, high school football linemen also have an increased incidence of a high BMI. Laurson et al
      • Laurson K.R.
      • Eisenmann J.C.
      Prevalence of overweight among high school football linemen.
      found that 9% of high school linemen had a BMI ≥35 kg/m
      • Dick R.
      • Ferrara M.S.
      • Agel J.
      • et al.
      Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
      . Forty-five percent of linemen were overweight, compared with 18.3% of age- and sex-matched individuals from the NHANES. A separate study involving 215 high school linemen found a mean percent body fat of 25.7% by skin-fold measurement.
      • Gomez J.E.
      • Ross S.K.
      • Calmbach W.L.
      • et al.
      Body fatness and increased injury rates in high school football linemen.
      Thus, obesity does appear to play a role in the increased incidence of a high BMI among high school linemen.
      At the collegiate level, the average weight of linemen at the University of Oklahoma in 2008 was 281 pounds, compared with 253 pounds in 1988.
      • Keith A.E.
      Fattened up for football.
      In addition, Buell et al
      • Buell J.L.
      • Calland D.
      • Hanks F.
      • et al.
      Presence of metabolic syndrome in football linemen.
      recently demonstrated presence of the metabolic syndrome in 34 of 70 (49%) current collegiate linemen. The linemen also were noted to have a high incidence of elevated total cholesterol-to-HDL cholesterol ratio and C-reactive protein levels, both adverse biomarkers for heart disease.
      In summary, although musculoskeletal injuries will remain primary to football, the long-term ramifications of obesity and its associated health risks in football players remain controversial and currently unanswered. Early studies did not suggest an increased mortality, but they may not be scientifically valid or applicable to current players. Recent data suggest increased cardiovascular risk factors in present players, particularly the heavier linemen.
      There is an obvious need for future longitudinal studies to assess risk factors for cardiovascular disease in both current and former football players. To achieve sound scientific conclusions, both independent and dependent variables need to be formally evaluated in the context of confounding variables. Future studies should consider genetics and family history of the athletes, race, players' diet, exercise regimens, in-season versus off-season programs, sleeping patterns, medications, supplements including the use of ergogenic aids, comorbidities, and behavioral habits of players, such as smoking and substance abuse. Athlete cooperation and compliance is essential. Interventions to treat risk factors in players should be initiated when identified. These treatments are certainly indicated but, unfortunately, place necessary limitations in the study design of future investigations.
      Furthermore, the design of future studies should be well planned. Although there are multiple measures for obesity, such as waist-to-height ratio, BMI, waist circumference, and percent body fat, the most reliable and reproducible measurements are required. Finally, outcome measures need to address the as-yet unanswered question of whether cardiovascular morbidity and mortality is increased in specific subsets of professional football players.

      References

        • Mueller F.O.
        • Colgate B.
        Annual survey of football injury research 1931-2007.
        (Accessed February 17, 2009)
        • Dick R.
        • Ferrara M.S.
        • Agel J.
        • et al.
        Descriptive epidemiology of collegiate men's football injuries: National Collegiate Athletic Association Injury Surveillance System, 1988-1989 through 2003-2004.
        J Athl Train. 2007; 42: 221-233
        • Baron S.
        • Rinsky R.
        • National Institute for Occupational Safety and Health
        NFL Mortality Study.
        (Accessed September 1, 2008)
        • Hargrove T.
        • et al.
        Supersized in the NFL: many ex-players dying young.
        Scripps Howard News Service Online. January 31, 2006;
        • Nicholas S.J.
        • Nicholas J.A.
        • Nicholas C.
        • et al.
        The health status of retired American football players: Super Bowl III revisited.
        Am J Sports Med. 2007; 35: 1674-1679
        • Miller M.A.
        • Croft L.B.
        • Belanger A.R.
        • et al.
        Prevalence of metabolic syndrome in retired National Football League players.
        Am J Cardiol. 2008; 101: 1281-1284
        • Croft L.B.
        • Belanger A.
        • Miller M.A.
        • et al.
        Comparison of National Football League linemen versus nonlinemen of left ventricular mass and left atrial size.
        Am J Cardiol. 2008; 102: 343-347
      1. Retired NFL players at increased risk for heart problems.
        (Accessed September 1, 2008)
        • Harp J.B.
        • Hecht L.
        Obesity in the National Football League.
        JAMA. 2005; 293: 1061-1062
        • Vega G.L.
        • Adams-Huet B.
        • Peshock R.
        • et al.
        Influence of body fat content and distribution on variation in metabolic risk.
        J Clin Endocrinol Metab. 2006; 91: 4459-4466
        • Gelber R.P.
        • Gaziano J.M.
        • Orav E.J.
        • et al.
        Measures of obesity and cardiovascular risk among men and women.
        J Am Coll Cardiol. 2008; 52: 605-615
        • George C.F.
        • Kab V.
        • Levy A.M.
        Increased prevalence of sleep-disordered breathing among professional football players.
        N Engl J Med. 2003; 348: 367-368
        • Bertovic D.A.
        • Waddell T.K.
        • Gatzka C.D.
        • et al.
        Muscular strength training is associated with low arterial compliance and high pulse pressure.
        Hypertension. 1999; 33: 1385-1391
        • Antman E.M.
        • Bennett J.S.
        • Daugherty A.
        • et al.
        Use of nonsteroidal anti-inflammatory drugs: an update for clinicians: a scientific statement from the American Heart Association.
        Circulation. 2007; 115: 1634-1642
        • Androgue H.J.
        • Madias N.E.
        Sodium and potassium in the pathogenesis of hypertension.
        N Engl J Med. 2007; 356: 1966-1978
        • Selden M.A.
        • Helzberg J.H.
        • Waeckerle J.F.
        • et al.
        Cardiometabolic abnormalities in current National Football League players.
        Am J Cardiol. 2009; 103: 969-971
        • Kannel W.B.
        • Vasan R.S.
        • Keyes M.J.
        • et al.
        Usefulness of the triglyceride-high-density lipoprotein versus the cholesterol-high-density lipoprotein ratio for predicting insulin resistance and cardiometabolic risk (from the Framingham Offspring Cohort).
        Am J Cardiol. 2008; 101: 497-501
        • Cordero A.
        • Laciaustra M.
        • Leon M.
        • et al.
        Comparison of serum lipid values in subjects with and without the metabolic syndrome.
        Am J Cardiol. 2008; 102: 424-428
        • McLaughlin T.
        • Abbasi F.
        • Cheal K.
        • et al.
        Use of metabolic markers to identify overweight individuals who are insulin resistant.
        Ann Intern Med. 2003; 139: 802-809
        • McKimmie R.L.
        • Daniel K.R.
        • Carr J.J.
        • et al.
        Hepatic steatosis and subclinical cardiovascular disease in a cohort enriched for Type 2 diabetes.
        Am J Gastroenterol. 2008; 103: 3029-3035
        • Ioannou G.N.
        Implications of elevated serum alanine aminotransferase levels: think outside of the liver.
        Gastroenterology. 2008; 135: 1851-1854
        • Ioannou G.N.
        • Weiss N.S.
        • Boyko E.J.
        • et al.
        Elevated serum alanine aminotransferase activity and calculated risk of coronary heart disease in the United States.
        Hepatology. 2006; 43: 1145-1151
        • Schindhelm R.K.
        • Dekker J.M.
        • Nijpels G.
        • et al.
        Alanine aminotransferase predicts coronary heart disease events: a 10-year follow-up of the Hoorn Study.
        Atherosclerosis. 2007; 191: 391-396
        • Goessling W.
        • Massaro J.M.
        • Vasan R.S.
        • et al.
        Aminotransferase levels and 20-year risk of metabolic syndrome, diabetes, and cardiovascular disease.
        Gastroenterology. 2008; 135: 1935-1944
        • Vozarova B.
        • Stefan N.
        • Lindsay R.S.
        • et al.
        High alanine aminotransferase is associated with decreased hepatic insulin sensitivity and predicts the development of type 2 diabetes.
        Diabetes. 2002; 51: 1889-1895
        • Tucker A.M.
        • Vogel R.A.
        • Lincoln A.E.
        • et al.
        Prevalence of cardiovascular disease risk factors among National Football League players.
        JAMA. 2009; 301: 2111-2119
        • Center for the Study of Retired Athletes
        News.
        (Accessed September 1, 2008)
        • Laurson K.R.
        • Eisenmann J.C.
        Prevalence of overweight among high school football linemen.
        JAMA. 2007; 297: 363-364
        • Gomez J.E.
        • Ross S.K.
        • Calmbach W.L.
        • et al.
        Body fatness and increased injury rates in high school football linemen.
        Clin J Sports Med. 1998; 8: 115-120
        • Keith A.E.
        Fattened up for football.
        People. 2008; 70: 93-96
        • Buell J.L.
        • Calland D.
        • Hanks F.
        • et al.
        Presence of metabolic syndrome in football linemen.
        J Athl Train. 2008; 43: 608-616