ORIGINAL RESEARCH

Cardiovascular and Musculoskeletal Assessment of Elite US Volleyball Players Christopher K. Davis, MD, PhD,*† Dan A. Dyar, MA, RDCS,† Lisa A. Vargas, RDCS,† and Paul D. Grossfeld, MD*† Key Words: aortic dilation, athlete’s heart, Marfan syndrome

Objective: The aim of this study was to characterize the cardiovascular and musculoskeletal systems of elite volleyball players, including aortic dimensions. Previous studies have shown that the upper limit of normal aortic sinus diameter for male and female athletes is 4 and 3.4 cm, respectively.

Design: Cross-sectional analysis. Setting: United States Olympic Volleyball Training Facility and Rady Children’s Hospital San Diego. Participants: Seventy (37 male) members of the US national volleyball team.

Main Outcome Measures: Athletes underwent evaluation that included medical and family histories, targeted physical examinations specifically focusing on abnormalities present in Marfan syndrome (MFS), and transthoracic echocardiograms. Cardiac chamber and great artery size, valve function, and coronary artery origins were assessed. Results: Three male athletes (8%) had an aortic sinus diameter $4 cm, one of whom also had an ascending aorta .4 cm. Two female athletes (6%) had aortic sinus diameter $3.4 cm, and another had an ascending aorta of 3.4 cm. There were no other intracardiac or arterial abnormalities. Individual musculoskeletal characteristics of MFS were common among the athletes but not more frequent or numerous in those with aortic dilation.

Conclusions: The prevalence of aortic root dilation in this population of athletes was higher than what has previously been reported in other similar populations. Further study is needed to determine whether these represent pathological changes or normal variations in tall athletes. Clinical Relevance: This study adds to the existing knowledge base of athlete’s heart, with specific attention to aortic dimensions in elite volleyball players. The data are relevant to similar athletes’ medical care and to preparticipation cardiac screening in general. Submitted for publication June 2, 2014; accepted September 29, 2014. From the *Division of Cardiology, Department of Pediatrics, University of California San Diego, San Diego, California; and †Division of Cardiology, Rady Children’s Hospital San Diego, San Diego, California. Supported in part by a grant from the National Marfan Foundation to P. D. Grossfeld. The authors report no conflicts of interest. Corresponding Author: Christopher K. Davis, MD, PhD, Division of Cardiology, Department of Pediatrics, 3020 Children’s Way, MC 5004, San Diego, CA 92123 ([email protected]). Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

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INTRODUCTION The past 2 decades of research has led to a significant increase in the understanding of the cardiovascular system of athletes.1–3 In particular, characteristics of the aortas of athletes, including the size of the aortic root and ascending aorta, have been more thoroughly described.4–6 Nevertheless, there remains a paucity of data on elite athletes in particular sports. Elite volleyball players are typically tall and relatively thin, and long arms often provide a distinct advantage in the sport. This body type overlaps with that seen in pathological conditions such as Marfan syndrome (MFS). Indeed, the tragic death in 1986 of US Olympian Flo Hyman, who died of aortic dissection having had undiagnosed MFS, highlighted the difficult distinction between normal and pathological conditions in athletes with body types well suited for volleyball. A large analysis of competitive Italian athletes5 concluded that even in tall athletes, aortic sinus (root) dimension of .4 cm in males and .3.4 cm in females is uncommon and likely pathologic. The overall prevalence of sinus dilation was ;1%, and many of those athletes with sinus dilation who were discovered during their competitive years showed further dilation with time, even after they stopped competing. Only 2 of the 27 athletes with sinus dilation were volleyball players. A recent meta-analysis of aortic root size in athletes6 revealed that the 95th confidence limit for sinus dimensions of male and females athletes was 3.3 and 2.7 cm, respectively. This analysis included a small number of volleyball players. An upper limit of normal dimension for the aortic sinuses was not formulated, although it was noted that there is a “plateauing of aortic dimensions with increasing height, further emphasizing the importance of not dismissing markedly enlarged aortas in large athletes as a result of athletic training or body size alone.” With this background, we sought to determine cardiovascular characteristics in a group of elite US volleyball players, with special attention to aortic dimensions and possible associations with signs of connective tissue disorders.

METHODS Seventy-one athletes from the US National volleyball team (38 males) were evaluated. One male athlete was not included in this study because of the presence of bicuspid Clin J Sport Med  Volume 25, Number 6, November 2015

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Clin J Sport Med  Volume 25, Number 6, November 2015

aortic valve. The remaining 70 were evaluated with directed medical histories, physical examinations, and transthoracic echocardiograms. Medical histories and examinations were specifically targeted toward identifying characteristics of connective tissue disease and MFS in particular. Arm span/ height ratio, upper body/lower body ratio, and presence of other features in the modified Ghent criteria7 identifiable by physical examination were recorded. An evaluation for dural ectasia and ectopia lentis was not performed. Athletes were asked specifically whether previous diagnoses of myopia, pneumothorax, and/or scoliosis had been made. Informed consent for testing was obtained from each of the subjects. The Institutional Review Board of the University of California San Diego approved the study. Echocardiograms were performed using a Vivid-i ultrasound machine (GE Healthcare, Pittsburgh, Pennsylvania). Parasternal long and short axis and apical views were performed to measure left ventricular and atrial dimensions, examine all 4 valves, and measure the main pulmonary artery and aorta. Left ventricular and atrial dimensions were measured by m-mode imaging. Coronary artery origins were sought and identified when possible and confirmed by color Doppler imaging. Aortic dimensions were measured from parasternal long axis images in mid-systole at the moment of maximum expansion, perpendicular to the long axis of the vessel, from leading edge to leading edge. The main pulmonary artery was measured in a short axis view at the midpoint between pulmonary valve annulus and bifurcation of the branch pulmonary arteries. All dimensions were standardized to body surface area, and Z-scores were calculated using a commercially available database. A single investigator (a pediatric cardiologist and experienced echocardiographer) who was blinded to the identification of the athletes interpreted each echocardiogram. The relationship between aortic dimensions and height of each athlete was assessed using standard correlation. A P value of ,0.05 was considered significant.

RESULTS General and Musculoskeletal Characteristics Demographic characteristics of the athletes are presented in Table 1. None had a known personal or family history of connective tissue disorders. Twenty-four of the 70 athletes (34%) had at least 1 characteristic of MFS on physical examination based on Ghent criteria, but none had more than 2 characteristics. Of the athletes who had dilation of the aortic root or ascending aorta, 2 of the 6 (33%) had 1 musculoskeletal characteristic of MFS, a percentage nearly equal to the entire group. Sixteen athletes (23%) had upper body/lower body ratio ,0.85 and 4 of the 70 (6%) had arm span/height ratios $1.05, indicating the inherent selection for this body type in elite volleyball players.

Cardiovascular Characteristics Cardiac dimensions are presented in Table 2. Left ventricular, left atrial, and pulmonary artery dimensions were normal (defined as Z-score #2) in all except 1 male athlete Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

Aortic Dilation in Volleyball Players

TABLE 1. Subject Demographics and Prevalence of Individual Marfan Characteristics Males (n = 37) Mean 6 SD Age (yrs) Height (cm) Weight (kg) BSA (m2)

28.7 198.2 93.9 2.26

6 6 6 6

3.5 8 9 0.15

Females (n = 33) Mean 6 SD 29.4 184.1 76.5 1.98

6 6 6 6

3.7 7.4 5.9 0.1

Number From Each Group

Number From Each Group

1 5

3 9

2 0 1 0

2 0 3 0

Arm span/height $1.05 Upper body/lower body ,0.85 Scoliosis Pectus deformity +Thumb or wrist sign +Facial features BSA, body surface area.

who had a left ventricular end-diastolic diameter of 6.5 cm (with normal ventricular function). Coronary artery origins (confirmed by color Doppler analysis) were confirmed to be normal in all athletes. All athletes had normal valve anatomy and function (no mitral or tricuspid prolapse, no stenosis, and no more than mild insufficiency of any single valve). Three male athletes (8%) had an aortic sinus diameter $4 cm (4, 4.2, and 4.3 cm), one of whom also had an ascending aorta of 4 cm (Figure 1). The corresponding Z-scores of the aortic sinus diameter for those 3 athletes were 2, 3.4, and 3.6, respectively. A fourth male athlete had an aortic sinus diameter of 3.8 cm, with a corresponding Z-score of 2.2 because of his relatively smaller body surface area. Two female athletes (6%) had aortic sinus diameter $3.4 cm (3.5 and 3.6 cm) and another had an ascending aorta of 3.4 cm. The corresponding Z-scores of the dilated sinuses were 1.9 and 2.1, respectively, and the corresponding Z-score of the dilated ascending aorta was 2.1. The relationships between height and aortic dimensions (sinuses and ascending aorta) are shown in Figures 2 and 3 for males and females, respectively. There was no significant correlation between height and aortic dimensions for either gender, other than a weak correlation between height and TABLE 2. Mean (SD, Range) Values (in Centimeters) of Cardiac Dimensions Males LVEDD LVESD Left atrium MPA Aortic annulus Aortic sinuses (root) Ascending aorta

5.7 3.5 3.8 2.7 2.4 3.4 3

(0.4, (0.3, (0.4, (0.3, (0.2, (0.4, (0.4,

4.9-6.5) 2.7-4.3) 2.7-4.4) 2-3.3) 2-2.8) 2.7-4.3) 2.5-4)

Females 5.2 3.1 3.5 2.6 2.1 2.9 2.8

(0.3, (0.3, (0.3, (0.3, (0.1, (0.3, (0.3,

4.8-6) 2.5-3.8) 3-4) 2.2-3.1) 1.9-2.4) 2.4-3.6) 2.1-3.4)

LVEDD, left ventricular end-diastolic diameter; LVESD, left ventricular end systolic diameter; MPA, main pulmonary artery.

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FIGURE 1. Modified parasternal long axis echocardiographic view of a male athlete with dilation of the aortic sinuses (4.3 cm) and sinotubular junction. Depth markers on the right edge of the image are 1 cm apart. Lines are drawn from leading edge to leading edge of the aorta. AoS, aortic sinuses; LA, left atrium; LV, left ventricle; RV, right ventricle; STJ, sinotubular junction.

FIGURE 2. Aortic dimensions in male players. Relationship between height and (A) aortic sinus diameter, and (B) ascending aorta diameter showing no significant correlation for these variables.

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Clin J Sport Med  Volume 25, Number 6, November 2015

Aortic Dilation in Volleyball Players

FIGURE 3. Aortic dimensions in female players. Relationship between height and (A) aortic sinus diameter, and (B) ascending aorta diameter. There is a significant but weak correlation for the ascending aorta only.

ascending aorta diameter in females. This was due in large part to the presence of a much smaller ascending aorta in the shortest athlete tested.

DISCUSSION This study demonstrates a relatively high incidence of aortic dilation in this group of elite volleyball players. These findings occurred in the absence of significant dilation of either the left ventricle or of the pulmonary artery, and none of the athletes had obvious systemic connective disease, suggesting that the aortic dilation was an isolated finding. The key clinical question is whether the larger aortas in these athletes are due to true aortopathy or are a result of some combination of body type and effect of training regimen in elite volleyball. Based on previous studies that included volleyball players and other tall competitive athletes, it seems reasonable to use the established cutoffs for normal aortic sinus dimensions (4 cm for males and 3.4 cm for females). Using these values, Pellicia et al5 identified several athletes with aortic dilation that likely had aortopathy, based on longitudinal follow-up demonstrating further dilation over time even Copyright © 2015 Wolters Kluwer Health, Inc. All rights reserved.

after cessation of competitive athletics. Kinoshita et al4 studied 1929 Japanese athletes, 26 of whom were volleyball players. The prevalence of aortic sinus dilation (.4 cm) was only 0.26% for the entire group but was 1.2% for basketball players and ;4% for volleyball players (1 of 26). Thus, even among many elite athletes, including tall ones, the overall prevalence of aortic sinuses .4 cm in men and .3.4 in women is low. The prevalence in this study is the highest yet recorded. The sizes of cardiac structures are closely related to height and body surface area if considered over a wide range of those anthropometric variables.4,5,8–10 However, there is a well described plateau of aortic dimensions at the high end of the height spectrum. At heights .185 cm and body surface area .2.2 m2, there is no significant relationship between body size and aortic size.11 In a study of 182 tall men and women (nonathletes, all .95th percentile for height), there was no anthropometric variable that was strongly correlated with aortic size.11 Furthermore, there was only 1 individual in that study with an aortic sinus diameter .4 cm. This study shows that among very tall athletes, height does not correlate strongly with aortic size, and the athletes with dilated aortas were not among the tallest within the group. Importantly, the www.cjsportmed.com |

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CONCLUSIONS

prevalence of aortic dilation was much higher among the athletes in this study than in the nonathletes in the study by Reed et al.11 This suggests that the combination of frequent and intense athletic training in tall athletes could produce a relatively high prevalence of aortic dilation. This notion is partially supported by an analysis of strength-trained athletes by Babaee Bigi and Aslani,12 which demonstrated larger aortic dimensions in these athletes than in controls. Furthermore, there was a direct correlation in that study between duration of training and aortic size. Importantly, however, the athletes tested were specifically strength trained, and other studies13 have shown that endurance-trained athletes have smaller aortas on average than do strength-trained athletes. Training for the US volleyball team includes weight lifting, but intense and prolonged strength training is not emphasized. The metaanalysis of aortic root size in athletes did show that athletes of all types have larger aortic roots than controls,6 further supporting this notion that intense and prolonged training of various types may enlarge athletes’ aortas. Alternatively, there may be some factor inherent in athletic individuals, which is associated with a larger aortic root, and that training has less of an effect. This hypothesis could be tested with measurements of the same athletes after cessation of regular training. Many of the athletes in this study (34%) met at least one of the musculoskeletal criteria of the revised Ghent nosology,7 the most common finding being an upper body-to-lower body ratio of ,0.85. The high prevalence of these findings highlights the overlap between some athletes—elite volleyball players in particular—and individuals with connective tissue disease such as MFS. There was no particular association between the presence of musculoskeletal findings and aortic dilation, suggesting that the presence of only 1 MFS finding is not helpful in identifying athletes who may have aortic dilation. This can only be accomplished with an imaging study, raising the question of whether screening for aortic dilation should be included in preparticipation screening protocols for these athletes. Although the prevalence of aortic dilation was fairly high in this group, unless it can be proven that this dilation represents actual aortic pathology, and that screening could reduce the risk of untoward events, this cannot be definitively recommended. However, it remains important for practitioners to recognize the physical characteristics of MFS and to be aware of the overlap of body types between those with pathology and those who are athletically advantaged in a sport such as volleyball. There are several limitations to this study. First, the relatively small sample size may have led to prevalence numbers that are not representative of all similar athletes. Second, the cross-sectional design does not allow for longitudinal tracking of individual athletes’ findings, especially with either further training or cessation of competition and intense training. Finally, there was only 1 investigator who interpreted the echocardiograms, thus exposing the data to possible inaccuracy because of interobserver variability and/or measurement error.

1. Maron BJ, Pellicia A. The heart of trained athletes. Cardiac remodeling and the risks of sports, including sudden death. Circulation. 2006;114: 1633–1644. 2. Baggish AL, Wood MJ. Athlete’s heart and cardiovascular care of the athlete. Circulation. 2011;123:2723–2735. 3. Pluim BM, Zwindermna AH, van der Laarse A, et al. The athlete’s heart, a meta-analysis of cardiac structure and function. Circulation. 1999;100: 336–344. 4. Kinoshita N, Mimura J, Obayashi C, et al. Aortic root dilation among young competitive athletes: echocardiographic screening of 1929 athletes between 15 and 34 years of age. Am Heart J. 2000;139:723–728. 5. Pelliccia A, Di Paolo FM, De Blasiis E, et al. Prevalence and clinical significance of aortic root dilation in highly trained competitive athletes. Circulation. 2010;122:698–706. 6. Iskander A, Thompson PD. A meta-analysis of aortic root size in elite athletes. Circulation. 2013;127:791–798. 7. Loeys BL, Dietz HC, Braverman AC, et al. The revised Ghent nosology for the Marfan syndrome. J Med Genet. 2010;47:476–485. 8. Pfaffengenberger S, Bartko P, Graf A, et al. Size matters! Impact of age, gender, height, and weight on the normal heart size. Circ Cardiovasc Imaging. 2013;6:1073–1079. 9. Devereux RB, de Simone G, Arnett DK, et al. Normal limits in relation to age, body size, and gender of two-dimensional echocardiographic aortic root dimensions in persons $15 years of age. Am J Cardiol. 2012;110: 1189–1194. 10. Roman MJ, Devereux RB, Kramer-Fox R, et al. Two-dimensional echocardiographic aortic root dimensions in normal children and adults. Am J Cardiol. 1989;64:507–512. 11. Reed CM, Richey PA, Pulliam DA, et al. Aortic dimensions in tall men and women. Am J Cardiol. 1993;71:608–610. 12. Babaee Bigi MA, Aslani A. Aortic root size and prevalence of aortic regurgitation in elite strength trained athletes. Am J Cardiol. 2007;100: 528–530. 13. D’Andrea A, Cocchia R, Riegler L, et al. Aortic root dimensions in elite athletes. Am J Cardiol. 2010;105:1629–1634.

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Elite US volleyball players have a higher than expected prevalence of dilation of the aortic sinuses and ascending aorta. This dilation can occur in isolation, without other cardiac structures similarly dilated, and in the absence of MFS, although individual musculoskeletal features of MFS are common in these athletes. Long-term follow-up of these athletes is essential for the determination of the cause of the aortic dilation (ie, the relative contribution of training vs inherent vascular characteristics) and of the clinical significance regarding the risk of further dilation and dissection.

ACKNOWLEDGMENTS The authors thank all of the players for their participation. They also acknowledge the head trainers, Aaron Brock and Jill Wosmek, along with the rest of the medical, coaching, and support staff of the US National Volleyball teams for their support.

REFERENCES

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Cardiovascular and Musculoskeletal Assessment of Elite US Volleyball Players.

The aim of this study was to characterize the cardiovascular and musculoskeletal systems of elite volleyball players, including aortic dimensions. Pre...
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