Sports medicine encompasses many aspects of an athlete’s health care. Preparticipation and periodic evaluation of athletes is an important area of sports medicine that helps to identify and treat the conditions that may predispose to injury or death. One of the goals of the preparticipation physical examination is to diagnose any occult disease process before it leads to sudden death while performing strenuous sports activities.
Sudden Death in Athletes
Ever since Pheidippides collapsed and died after running from Marathon to Athens in 490 BC, the sudden death of an athlete has been a tragic event that causes significant emotional and social impact on the general public and medical community (22). The incidence of sudden death in athletes varies widely in different series reported in the literature. It ranges from 0.46 cases per 100,000 person-years in France (21), to 0.61 cases per 100,000 person-years in the United States (24), to 1.9 deaths per 100,000 person-years in Italy (7), to 2.6 events per 100,000 person-years in Israel (43). The incidence of sudden death is higher in male athletes (21,24,27,30). Cardiac causes are responsible for the majority of cases, reportedly from 56% (24) to as high as 85% to 95% of cases (10,29,30). Recently, Harmon et al. (17) reported on the incidence of sudden cardiac death based on a National Collegiate Athletic Association database. The incidence of sudden cardiac death was approximately 1:43,000 (2.3 deaths per 100,000) student-athletes per year, which was significantly higher than the previously reported estimates. They questioned the accuracy of previous estimates, which were based on the public media reports and catastrophic claims data, by showing that media reports identified only approximately 50% of cases.
In the United States, hypertrophic cardiomyopathy (HCM) and congenital coronary artery anomalies are considered to be the most common causes of sudden death in young athletes (22,30). In marathon runners older than 30 years, Roberts and Maron (25,39) reported that coronary atherosclerotic disease represented the most common cause of sudden death. In contrast to the study by Roberts and Maron, Corrado et al. (10) found right ventricular cardiomyopathy (or arrhythmogenic right ventricular dysplasia) as the most common underlying pathology of sudden death of athletes in the Italian population. The difference may be attributed to a more homogenous population in Italy compared with the heterogenous population in North America.
In an autopsy-based study of a U.S. military population, Eckart et al. (11) found sudden unexplained death represented 41% of cases of sudden deaths followed by atherosclerotic disease (23%) and HCM (13%) in the age group younger than 35 years. As discussed previously, these recent studies have called into question the traditional thinking regarding both the incidence and causes of sudden cardiac death. We agree that further studies are needed to confirm the findings of Eckart et al. (11) and Harmon et al. (17). Cardiovascular causes of sudden death in athletes according to the American Heart Association (AHA) in the United States are listed in Table 1.
Recommendations for Preparticipation Cardiovascular Screening
In 2007, the AHA recommended a 12-element preparticipation cardiovascular screening of competitive athletes that included various components of history and physical examination (Table 2). A positive finding in one or more elements of this 12-element screening tool is a trigger for further cardiovascular evaluation.
Diagnostic Accuracy of Cardiac Physical Examination
The diagnostic accuracy of cardiac auscultation varies widely among clinicians. Mangione et al. (19) found that the diagnostic accuracy of cardiac auscultation ranged from 0% to 56.2% for cardiology fellows (median = 21.9%) and from 2% to 36.8% for medical residents (median = 19.3%). Studies in family practitioners, academic internists, and general internists all demonstrate a proficiency of no more than 40% in recognizing basic heart murmurs (36,40). Cardiologists — who only represent 5% of practicing physicians — are the only group that routinely recognizes the majority of abnormal heart murmurs (12).
Role of Cardiac Auscultation in Preventing Sudden Cardiac Death in Athletes
Corrado et al. (8) prospectively studied 20 years of preparticipation evaluations for sudden deaths among athletes and nonathletes younger than 35 years in Italy from 1979 to 1996. HCM was detected in 22 athletes (0.07%) at examination and accounted for 3.5% of the cardiovascular reasons for disqualification from sports. Only 2 (0.09%) of these 22 athletes were referred for echocardiographic study after finding a cardiac murmur on physical examination. Other reasons for referral included a positive family history in three athletes and an abnormal electrocardiogram (ECG) result in the rest of the athletes.
Similarly, another study from Italy retrospectively studied the screening for HCM in 34,910 young military men and found 19 patients with HCM. The estimated prevalence of HCM was 0.05%, which was comparable to that reported in competitive athletes. Of the 19 recruits with HCM, the reasons for referral for echocardiographic examination were electrocardiographic abnormalities in 11, systolic murmur in 3, systolic murmur and electrocardiographic abnormalities in 2, and a family history of HCM or HCM-related sudden death in 3 (34).
In a retrospective study of 158 cases of sudden cardiac death (30) in competitive athletes, only 4 (3%) of 115 athletes who underwent a preparticipation examination were suspected to have cardiac disease on the basis of history and physical examination.
Studies that evaluated the addition of ECG to routine examination also provided data regarding the sensitivity and specificity of history and physical examination. Fuller et al. (13) evaluated the addition of ECG to the preparticipation history and physical examination to improve detection of potentially serious cardiac abnormalities in 6,000 athletes. Outcome measures were detected in 22 athletes or 1 in 255. Cardiac history led to detection of outcome measures in zero athletes, auscultation/inspection in 1 of 6,000 athletes (severe aortic insufficiency), blood pressure measurement in 1 of 1,000 athletes, and the ECG in 1 of 350 athletes. None of the 6,000 athletes were found to have HCM. Fuller et al. concluded that the ECG was a much more effective screening tool than history and auscultation/inspection in detecting serious cardiovascular abnormalities.
Another prospective study that compared preparticipation examination by history and physical examination with a strategy that included history, physical examination, and ECG in young competitive athletes found that screening with history and examination alone correctly detected less than half of the athletes with potentially significant cardiac findings (2).
Although physical examination, including cardiac auscultation, is easy to perform in mass screening, the data mentioned previously demonstrate the low sensitivity and specificity of standard history and physical examination in detecting significant occult cardiac pathology in mass screening protocols.
Factors contributing to this low sensitivity and specificity include the following:
- The absence of physical stigmata (murmur) in many cardiac conditions, e.g., in ion channelopathies, anomalous coronary artery, or coronary artery disease, although suspicion about these conditions can be raised by specific questions in the personal and family history. Even in disease processes associated with a murmur, e.g., HCM, resting supine cardiac auscultation may not identify the murmur since more than two-thirds of patients do not have resting outflow gradients. However, dynamic auscultation may unmask the murmur of dynamic outflow obstruction.
- Preparticipation physical examination being performed by a variety of health care workers with varying levels of expertise (14,35) including family physicians, orthopedic physicians, cardiologists, nurse practitioners, athletic trainers, and chiropractors.
- Inadequacy of the preparticipation screening process used by many colleges and universities across the United States (15,38).
Lately, improvements in state-approved preparticipation history and physical examination screening questionnaires have been noted. However, many states also have increased the number of nonphysicians performing preparticipation screening examinations (15).
Role of Electrocardiography as a Screening Tool
The low sensitivity of history and physical examination in detecting the causes of sudden death in athletes has generated interest in utilizing other cardiovascular screening tools like electrocardiography or echocardiography (18) at mass screening levels. The role of electrocardiography as a screening tool in addition to the history and physical examination is still an area of active debate (6). In 2006, a population-based study from Italy by Corrado et al. (7) demonstrated that the incidence of sudden cardiovascular death in young competitive athletes declined substantially after the implementation of a national screening program. Based on the 20-year experience of a national screening program in Italy, the European Society of Cardiology recommends a 12-lead ECG as a part of preparticipation examination (9). Recently, Steinvil et al. (43) questioned the role of ECG as a part of preparticipation examinations and reported that mandatory ECG screening of athletes had no apparent effect on their risk for cardiac arrest. Their study used a 12-year sample as compared with a 2-year sample used in the study of Corrado et al. (7). Although the addition of ECG to history and physical examination improves the overall sensitivity of preparticipation cardiovascular screening in athletes, it is associated with an increased rate of false-positive results (2). The United States has not adopted the ECG as a part of preparticipation examination on the basis of the cost-to-benefit ratio and a lack of physician infrastructure (31). Auscultation has been a diagnostic technique for almost 200 years and, in association with a careful history, is still the most cost-effective screening tool available for preparticipation examinations at the present time.
Cardiac auscultation to identify heart murmurs is one of the four components of physical examination as recommended by the AHA. A good cardiac auscultation technique can be helpful in identifying the various abnormal heart sounds related to different cardiac disease processes. Some important components of this technique are listed in the following section (42):
- Ambient noise must be minimized.
- Auscultation in sitting, recumbent, and left lateral decubitus positions.
- Carotid upstroke should be utilized to time systole to identify heart sounds and characterize the murmurs as systolic versus diastolic.
- Maintaining a consistent approach to cardiac auscultation from patient to patient.
Murmurs should be characterized on the basis of timing, character, location, intensity, and response to various dynamic maneuvers like squat to stand and Valsalva.
- The listening sequence can be from the cardiac apex or right sternal border.
- The first and second heart sounds should be identified first.
- The later focus should be to identify the extra heart sounds, gallops, and murmurs.
Emerging Concepts on the Nature of Auditory Skills
There is a general agreement that cardiac auscultation is an important part of any sports preparticipation physical examination. However, the ability of clinicians to detect accurately abnormal heart murmurs generally is disappointing. Studies in family practitioners (40) and academic internists (37) demonstrate a proficiency of only 40% in recognizing basic heart murmurs. Cardiologists — who represent 5% of practicing physicians — are the only group that consistently recognizes abnormal heart murmurs (12), and yet, they are not the predominant group performing preparticipation examinations.
Whenever 95% of learners are failing to master a skill, it raises the question of whether that skill is being taught properly. When one contemplates the underlying cause for this lack of proficiency, it leads to a basic question: how does any normal-hearing adult learn to recognize a new sound like a heart murmur?
The answer to that question is psychoacoustics. This field is defined as the scientific study of the perception of sound. It is a basic science endeavor in which researchers record electroencephalograms (EEG) of subjects while they listen to known and unknown sounds through a set of headphones. In an important article in this field, Atienza et al. (1) exposed normal-hearing subjects to a new sound and recorded their EEG during this learning process. Results demonstrated that when the brain begins to recognize a new sound, it forms a new wave on the EEG called a “mismatched negativity wave.” Once it appears on the EEG, this wave grows progressively larger over the next several days. Atienza et al. (1) found that there was a fourfold range of repetition required for normal-hearing subjects to master each new sound. In their study, 1,000 to 4,000 repetitions of the new sound were played, resulting in an improvement in proficiency from 10% at the beginning of the study to 85% by the end of the study.
Our group was intrigued by this concept about how the brain learns a new sound and decided to conduct a proof-of-concept study with medical students to see if this psychoacoustic approach would apply to the learning of heart murmurs. We recruited 50 second-year medical students who listened to several hundred repetitions of the following four heart murmurs: aortic stenosis, aortic regurgitation, mitral stenosis, and mitral regurgitation. We tested the medical students on their ability to recognize these murmurs at a pretest after they heard 250 repetitions of each of those four murmurs and again after they heard 500 repetitions of each murmur. The results demonstrated that the medical students recognized only 18% of these murmurs at the pretest but improved to 73% after 250 repetitions and improved further to 84% after hearing 500 repetitions of each murmur (3). An auscultation proficiency of 84% is comparable to that of most practicing cardiologists (12); however, whether medical students demonstrate this level of auscultatory proficiency with live patients has not been tested.
In the course of our study, we learned two important things about teaching auditory recognition of heart murmurs. First, we learned it was important to not vary the murmur being learned. The rationale for this consistency in the sound being learned is that the brain is creating an auditory template of that sound. If the brain hears a variation of the sound, it disrupts the formation of that auditory template. Accordingly, for our study, we used exactly the same example of mitral regurgitation for all 500 repetitions. We followed the same procedure for the other three murmurs in our study.
We further realized that this degree of repetition was a crucial element missing in the current method of instruction in cardiac auscultation. Namely, learners are never given sufficient repetition to form an auditory template of each heart murmur. Consequently, they never master heart murmurs in medical school or in their subsequent medical training. It is not surprising that they become residents and even attending physicians without this basic clinical skill.
The fact that auscultation proficiency improves dramatically with intensive repetition may seem counterintuitive at first. However, this is because there is an entrenched bias in medical education toward teaching auscultation as if it were an intellectual skill. This approach has been based on the mistaken assumption that the auditory recognition of heart murmurs can improve with greater understanding of the pathophysiology of these sounds. That is, if students have a better understanding of the etiology of these sounds, they would be able to recognize them when they hear them in their patients. In fact, studies based on this assumption have been uniformly disappointing (20). On the other hand, once auscultation is seen as a technical skill, then the dramatic response to repetition makes sense.
To confirm that this approach would work with practicing physicians, we conducted a cardiac auscultation workshop at the annual scientific meeting of a general internal medicine society. During the workshop, 150 clinicians listened to 400 repetitions of each of the five basic heart murmurs over a 90-min time frame. Their scores improved to 80%, demonstrating that cardiac auscultation is an auditory skill that can be mastered in relatively little time with intensive repetition (4).
In order to allow our readers to test this approach for themselves, we have created two sample audio files that provide approximately 200 repetitions of two different heart murmurs. The first is an innocent murmur, the most common murmur heard in any medical population. The second murmur is HCM, arguably the most important pathologic murmur to recognize during a preparticipation examination. These two audio files can be downloaded here (see Audio File, Supplemental Digital Content 1, Innocent Murmur, at http://links.lww.com/CSMR/A1, and Audio File, Supplemental Digital Content 2, Hypertrophic Cardiomyopathy, at http://links.lww.com/CSMR/A2). Each audio file should be heard twice to achieve proficiency.
This sound undoubtedly will be the most common murmur heard in any preparticipation cardiac examination, occurring in up to 50% of normal individuals. This murmur is systolic, grade 1 or 2, and peaks in early to mid systole. It finishes before the second heart sound and may be heard in the fourth left intercostal space, as well as the aortic and pulmonic areas (see Audio File, Supplemental Digital Content 1, Innocent Murmur, at http://links.lww.com/CSMR/A1). This murmur is due to the increased flow of blood across the normal aortic or pulmonic valve in early systole and, by definition, has no associated cardiovascular abnormalities. For example, no delayed carotid impulse, no diastolic murmur, and no opening snap or ejection click is heard. This murmur will increase with maneuvers that raise the cardiac output such as anxiety or a brief exercise like a few sit-ups.
The clinician should be comfortable in recognizing this murmur and reassure the athlete of its benign nature. No further cardiac testing is required for individuals found to have an innocent murmur. In order to master this murmur, it is important to hear it between 400 and 500 times.
HCM is a genetic disease that is defined by the finding of left ventricular hypertrophy in the absence of any other identifiable cause. HCM is inherited in an autosomal dominant pattern with a wide variety of clinical manifestations. Classically, HCM has been described as having marked asymmetric hypertrophy of the interventricular septum. We now know that HCM can involve any wall of the myocardium (5). HCM variants include apical, basal septal, lateral wall, and concentric (neutral) hypertrophy. In addition, the right ventricle has been identified now as developing hypertrophy in a subset of patients with HCM (32).
Many clinicians immediately think of a murmur when considering examination findings of HCM. However, often, patients with HCM present without the outflow tract murmur that characteristically is associated with HCM. Approximately one-third of patients with HCM have a resting murmur, another third have a provocable murmur, and the remaining patients have no murmur at all (23,33,41).
HCM is common and is said to occur in approximately 1 in 500 people worldwide. Echocardiographic studies in the United States and Asia indicate a prevalence ranging from 0.16% to 0.29% (16,26,28,44). HCM is the leading cause of sudden cardiac arrest in the young (30) and often goes unnoticed despite its high prevalence. When evaluating patients for sports participation, features of HCM should be sought after with diligence. HCM presentations are as variable as its hypertrophy patterns, which highlights the importance of a careful examination and consideration of additional testing depending on the degree of suspicion from the history and physical examination. Additional testing may include an ECG, an echocardiogram, and, in some cases, cardiac magnetic resonance imaging. If the diagnosis is in question, referral to a center with expertise in HCM as defined by the Hypertrophic Cardiomyopathy Association (www.4hcm.org) should be considered.
The classic physical examination description of HCM often revolves around auscultation and the presence of left ventricular outflow tract obstruction. Examination of a patient with possible HCM should include arterial and carotid pulsation and palpation of the apical impulse, in addition to auscultation. With this in mind, we will describe the comprehensive findings on physical examination in patients with HCM (36).
The examination typically begins with palpation. The classic carotid pulsation is brisk and may be bifid. The bifid carotid pulse is the result of a rapid upstroke followed by a midsystolic drop from premature aortic valve closure. This is followed by a secondary late arterial wave from relief of the outflow tract obstruction.
The point of maximal impulse or “apical” impulse reflects the presence of increased myocardial hypertrophy. When abnormal, it will be a sustained thrust that continues throughout most of systole. Similar to the carotid pulse, the apical impulse may be bifid. The initial impulse is from a forceful atrial contraction against a stiff left ventricle with the second impulse reflecting left ventricular hypertrophy. In some individuals with a thin body habitus, a third impulse may be palpable. The trifid impulse or so-called triple ripple occurs in late systole and may occur if severe outflow tract obstruction is present. A systolic thrill may be palpable from severe mitral regurgitation or from outflow tract obstruction at the apex or the lower left sternal border, respectively, in those with a thin body habitus.
Cardiac auscultation begins with a heart sound assessment. The first heart sound typically is normal. The second heart sound usually is split normally, although patients can develop a paradoxical split second heart sound due to the presence of a left bundle branch block or severe left ventricular outflow tract obstruction. A third or fourth heart sound may be heard. The fourth heart sound is found in those with severe hypertrophy, while a third heart sound frequently is heard in young patients in early diastole and is the result of early rapid filling in young patients. This is not unique, however, to HCM, as this can be seen in otherwise healthy young athletic hearts as well.
Cardiac auscultation continues with assessment of a resting murmur and provocation of occult murmurs. The left ventricular outflow tract obstruction murmur is a harsh crescendo–decrescendo murmur that peaks in mid to late systole (see Audio File, Supplemental Digital Content 2, Hypertrophic Cardiomyopathy, at http://links.lww.com/CSMR/A2). The murmur is located primarily at the left sternal border and ends prior to the second heart sound. It may radiate across the precordium but rarely radiates to the carotids, a feature that may help distinguish it from valvular aortic stenosis.
Mitral regurgitation may be audible as a separate holosystolic murmur at the apex. The absence of an aortic diastolic decrescendo murmur is an important feature because this would suggest another disease or an HCM “mimic,” such as a discrete subvalvular membrane.
Provocative murmurs should be performed routinely to identify the presence of a dynamic murmur, as well as to differentiate the murmur of HCM from that of valvular aortic stenosis and mitral regurgitation. One such maneuver is the Valsalva maneuver. During the strain phase of the Valsalva maneuver, there is a decrease in the left ventricular volume, which leads to an increase of the dynamic gradient and the intensity of the murmur. However, because of the variability in the performance of this maneuver, the classic response of the murmur to the Valsalva maneuver may not occur in all patients. Perhaps the most reliable method for diagnosing a dynamic left ventricular outflow tract obstruction is the response of the murmur to the stand-squat-stand maneuver. This maneuver results in immediate changes to afterload and preload. From the standing position to a prompt squat, there is an increase in both afterload and preload, resulting in a marked reduction in the intensity of the murmur. As the patient rises from the squatting to the standing position, afterload is reduced immediately, with a resultant increase in murmur intensity (see Audio File, Supplemental Digital Content 2, Hypertrophic Cardiomyopathy, at http://links.lww.com/CSMR/A2). In addition, for the following five beats, the murmur intensity will increase progressively as preload to the left side of the heart is now reduced. Other maneuvers can be employed to change the intensity of the murmur by altering the preload, afterload, or contractility. These may include simple exercise, leg raising to increase preload, or, in rare instances, bedside administration of inhaled amyl nitrite to decrease afterload and increase heart rate.
Cardiac auscultation remains an important part of the preparticipation examination. New insights into the nature of auditory learning have shown that intensive repetition is necessary to master common heart murmurs. The most common murmur heard during preparticipation screening is an innocent murmur, while one of the most important pathologic murmurs is that of HCM. Maneuvers that bring out the murmur of HCM are important to perform to unmask occult disease.
The authors declare no conflict of interest and do not have any financial disclosures.
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