Abstract
Background:
Lumbar disk degeneration (LDD) occurs frequently in athletes. Researchers have found that LDD occurs mainly in the lower disks (L4/L5 and L5/S1) in the general and athletic populations. However, a retrospective study showed a high prevalence of LDD in the upper lumbar disks (L1/L2), especially in elite gymnasts.
Purpose:
To investigate the effect of competition level on the prevalence and incidence of LDD in the upper lumbar disks (L1/L2).
Study Design:
Cross-sectional study; Level of evidence, 3; and cohort study; Level of evidence, 2.
Methods:
We conducted 2 studies to evaluate the effect of competition level on the prevalence and incidence of LDD in Japanese collegiate gymnasts. In study 1, a cross-sectional study of 298 collegiate gymnasts was conducted between 2011 and 2015. Competition levels were categorized as regional, national, and international, and T2-weighted magnetic resonance imaging (MRI) was used to evaluate LDD. Chi-square testing was applied to assess differences in the prevalence of LDD and spinal levels among the 3 competition levels. In study 2–-a prospective cohort study–-LDD progression and its related risk factors were investigated in 51 collegiate gymnasts. Baseline lumbar MRI scans and measurements of physical function (generalized joint laxity and finger-floor distance test) were performed in March 2014. Follow-up lumbar MRI scans were obtained 2 years later, in February 2016. Logistic regression analyses were performed to investigate the relationship between competition level and LDD progression.
Results:
In study 1, the prevalence of at least 1 degenerated disk in the regional, national, and international groups was 44.2% (19/43), 44.7% (98/219), and 52.8% (19/36), respectively (P = .655). The prevalence of LDD at L1/L2 in the international group was significantly higher than that in the other 2 groups (P = .018). In study 2, the presence of LDD at L1/L2 was associated significantly with international-level competition (adjusted odds ratio, 47.8; 95% CI, 2.75-830.50).
Conclusion:
In Japanese collegiate gymnasts, competing at the international level was found to be a risk factor for LDD at L1/L2.
Keywords: gymnastics, intervertebral disk degeneration, magnetic resonance imaging, risk factor
Lumbar disk degeneration (LDD) occurs frequently in athletes. Recently, Abdalkader et al 1 found that elite athletes have a high prevalence of LDD, as detected using magnetic resonance imaging (MRI) in athletes in the 2016 Rio de Janeiro Summer Olympics games. Many studies have previously reported the presence of an association between LDD and low back pain (LBP) in athletes. 8,14 Therefore, there is a need to clarify the risk factors for LDD to prevent LBP in elite athletes.
Several researchers have found that LDD occurs mainly in the lower lumbar disks (L4/L5 and L5/S1) in elite athletes. 1,4,8,15 In contrast, Swärd et al 21 found that LDD at the L1/L2 level was common among elite male gymnasts. Moreover, a recent study found that elite swimmers had more LDD in the upper lumbar disks (L1/L2) but tended to have less LDD in the lower lumbar disks. 6 Although the location of LDD reflects the characteristics of a particular sport, the cause of LDD in the upper lumbar disks in elite athletes remains unclear.
As described above, a previous study by Swärd et al 21 found a high prevalence of LDD in the upper lumbar disks (L1/L2) in elite gymnasts. However, this study had a small sample size and cross-sectional design. In contrast, Koyama et al 13 found that LDD occurred in both the upper (L1/L2, L2/L3, and L3/L4) and the lower (L4/L5 and L5/S1) disks in collegiate gymnasts. However, this study included both international- and regional-level gymnasts. Therefore, competition level may play a role in the occurrence of LDD. To clarify whether competition level directly relates to the prevalence of LDD at L1/L2 in gymnasts, it is necessary to conduct a prospective study.
This study aimed to investigate the effect of competition level on the prevalence and incidence of LDD in the upper lumbar disks (L1/L2). We hypothesized that the prevalence of LDD at L1/L2 would be significantly higher in international-level gymnasts and that the competition level of gymnasts would be a risk factor for LDD at L1/L2.
Methods
We conducted 2 studies to determine the prevalence of LDD at different competition levels (study 1) and to investigate the progression and risk factors (including competition level) related to LDD (study 2) in Japanese collegiate gymnasts. Study 1–-a cross-sectional study–-was conducted between 2011 and 2015; study 2–-a prospective cohort study with a 2-year follow-up–-was conducted between March 2014 and February 2016. The study protocol was approved by the ethics committee of our institution, and all gymnasts provided written informed consent before participation. Information regarding the purpose of the study, potential risks, and protection of the rights of the participants was provided to all gymnasts.
Participants
Study 1
The All-Japan Student Gymnastics Federation comprises 65 teams (about 1100 gymnasts). Two gymnastics teams were recruited. The participants were 298 Japanese collegiate gymnasts (203 men and 95 women; mean age, 20.0 ± 1.1 years; mean gymnastics experience, 13.0 ± 3.7 years). These teams trained regularly, 4 hours per day for 6 days per week. Gymnasts who had previously undergone lumbar surgery were excluded.
Study 2
We recruited 1 gymnastics team from the All-Japan Student Gymnastics Federation. A total of 53 gymnasts (33 men and 20 women) who regularly trained 4 hours per day for 6 days per week participated in the baseline evaluation. Among these gymnasts, 2 did not participate in the follow-up study because they had retired from gymnastics. Figure 1 shows the participant enrollment for both studies.
Figure 1.
Flow diagram of studies 1 and 2.
In both studies, the gymnasts were divided into 3 groups based on performance at the regional, national, or international level, according to the competition levels previously described by Kikuchi et al. 10 Gymnasts at the international level had participated in world championships, including the Olympic Games, or had placed first in Japanese national championships.
Patient Characteristics
In both studies, the characteristics of the gymnasts (age, height, weight, body mass index) were determined. Information on years of gymnastics experience was obtained from questionnaires. Moreover, all gymnasts were asked about their current experience with LBP (yes or no) and were asked to score their LBP on a 10-point visual analog scale, in which a score of at least 5 was considered to indicate the presence of LBP. 18
MRI Procedures
In both studies, MRI scans (AIRIS II; Hitachi) were performed using a 0.3-T unit that used surface coils with a body coil in the supine position. The imaging protocol consisted of a T2-weighted fast spin-echo sequence in the midsagittal plane, including (at least) L1 to S1, with a repetition time of 3000 ms and an echo time of 125 ms.
LDD was defined as the reduced signal intensity of the intervertebral disks from L1/L2 to L5/S1. The grading system for the degree of LDD was based on the Pfirrmann classification, 19 in which grades 1 and 2 indicate normal disks and grades 3, 4, and 5 indicate degeneration. 8,9,13,14 Because an orthopaedic spinal specialist often makes a diagnosis based on images, the MRI scans from each gymnast were examined by 2 experienced orthopaedic surgeons (K.H. and M.T.) specializing in spine disorders. Both orthopaedic surgeons were blinded to the descriptive and clinical data of the gymnasts. If there were any discrepancies between the orthopaedic surgeons, they were discussed before the final grading. The kappa score for interobserver agreement of the Pfirrmann disk degeneration grading was 0.918, indicating strong agreement.
Study 2: Baseline Evaluation
The initial evaluation included descriptive parameters and assessment of LDD using MRI for a prospective study. Baseline data were collected for physical function measurements, such as generalized joint laxity (GJL) and finger-floor distance (FFD).
Study 2: Physical Function Measurements
GJL is known to be related closely to orthopaedic injuries and disease. 3,16,17,20 The criterion used most widely for detecting GJL is the Beighton score, which requires the performance of 5 maneuvers for a total of 9 points (4 bilateral and 1 unilateral). 2 The Beighton score measurements were as follows: (1) passive dorsiflexion of the little fingers >90°; (2) passive apposition of the thumb to the flexor aspect of the forearm; (3) hyperextension of the elbows >10°; (4) hyperextension of the knees >10°; and (5) forward flexion of the trunk, with the knees straight, so that the palms of the hands rest easily on the floor.
The FFD is used to assess the mobility of the spine in the overall motion of bending forward. From an upright standing position on a table with a height of 40 cm, participants were asked to reach for the tabletop with maximum forward bending and full extension of the knee joint. The FFD was measured from the fingertips to the tabletop. If the fingertips extended below the level of the table, the FFD was recorded as a negative value.
All participants underwent physical function measurements (GJL and FFD tests) at baseline. Each examination was performed by the same examiner (K.K.).
Study 2: Endpoint Assessments at 2-Year Follow-up
The degree of LDD in the participants was determined using the modified Pfirrmann classification. 22 Grades 1 and 2 were classified as normal disks and scored as 0. For each higher degree of LDD, the score increased by 1 point. A sum score (range, 0-15) of LDD for the 5 lumbar disks was obtained by adding each lumbar disk score.
Statistical Analysis
In both studies, characteristics and physical function of the gymnasts were analyzed using 1-way analysis of variance, post hoc least significant difference test, chi-square test, and Fisher exact probability test for multigroup comparison. The chi-square test was used to assess differences in the prevalence of LDD and spinal level among the regional, national, and international level groups. In addition, in study 1, the relationship between LDD and LBP was assessed using the chi-square test.
In study 2, to investigate the relationship between competition level and LDD progression, logistic regression analyses were performed after adjusting for sex, weight, and years of gymnastics experience. These independent variables were chosen because variables with P < .05 were retained in each model and previous studies have reported that sex and weight affect LDD. Although there was a significant difference in height for the 1-way analysis, there was a high correlation between height and weight via Pearson correlation coefficient (r > 0.8). To avoid multicollinearity weight was used for the analysis. Hence, weight was used for the analysis. For all comparisons, a P value of <.05 was considered statistically significant. All statistical analyses were performed using IBM SPSS Statistics 23.0 software for Windows (SPSS IBM).
Results
Patient Characteristics (Study 1)
The characteristics of the 298 gymnasts in study 1 are summarized in Table 1. There were 43 gymnasts in the regional group, 219 in the national group, and 36 in the international group. According to univariate analysis, the international group was significantly associated with shorter height (P < .01), lower weight (P < .05), and more years of experience (P < .01) compared with the regional group. However, no significant differences in height, weight, or experience were observed between the international and national groups (P = .31, .06, and .18, respectively).
Table 1.
Characteristics of Study 1 Participants (n = 298) a
| Variable | Regional (n = 43) |
National (n = 219) |
International (n = 36) |
P |
|---|---|---|---|---|
| Sex, male:female, n | 32:11 | 148:39 | 23:13 | .136 |
| Age, y | 19.9 ± 1.1 | 20.0 ± 1.1 | 20.1 ± 1.1 | .817 |
| Height, cm | 165.1 ± 8.0 | 161.5 ± 7.3 b | 159.3 ± 8.2 c | <.01 |
| Weight, kg | 59.4 ± 7.6 | 57.0 ± 7.6 | 54.4 ± 7.6 b | <.05 |
| BMI | 21.7 ± 1.5 | 21.8 ± 1.5 | 21.4 ± 1.6 | .319 |
| Experience, y | 8.1 ± 4.1 | 13.7 ± 3.0c | 14.4 ± 3.2 c | <.01 |
| Low back pain, n (%) | 2 (4.7) | 33 (15.0) | 6 (16.7) | .167 |
a Data are reported as mean ± SD unless otherwise indicated. BMI, body mass index.
b Significantly different from regional group (P < .05).
c Significantly different from regional group (P < .01).
Prevalence of LDD (Study 1)
In study 1, the prevalence of LDD in the regional, national, and international groups was 44.2% (19/43), 44.7% (98/219), and 52.8% (19/36), respectively (P = .655). The prevalence of LDD was not associated with the competition level. In addition, we evaluated 1490 lumbar intervertebral disks (L1-S1) and found that 13.4% (199/1490) disks were degenerated. Comparison of the prevalence of LDD at each spinal level among the 3 groups revealed that L1/L2 was degenerated significantly more frequently in the international group (P = .018) (Table 2).
Table 2.
Prevalence of LDD at Each Lumbar Vertebral Level in Study 1 a
| Disk Level | Regional (n = 43) |
National (n = 219) |
International (n = 36) |
P |
|---|---|---|---|---|
| L1/L2 | 1 (2.3) | 12 (5.5) | 6 (16.7) | .018 b |
| L2/L3 | 1 (2.3) | 14 (6.4) | 5 (13.9) | .115 |
| L3/L4 | 2 (4.7) | 20 (9.1) | 6 (16.7) | .183 |
| L4/L5 | 7 (16.3) | 50 (22.8) | 6 (16.7) | .492 |
| L5/S1 | 13 (30.2) | 50 (22.8) | 6 (16.7) | .354 |
a Values are presented as n (%). LDD, lumber disk degeneration.
b Significant difference among the 3 groups (P < .05).
Relationship Between LDD and LBP (Study 1)
The prevalence of LBP in the gymnasts of study 1 was 13.8% (41/298). Table 3 shows the prevalence of LDD in the gymnasts with and without LBP. The prevalence of LDD was not associated with LBP, as determined using the chi-square test.
Table 3.
Relationship Between LDD and LBP in Study 1 a
| LDD | ||||
|---|---|---|---|---|
| Yes (n = 136) | No (n = 162) | χ2 | P | |
| LBP | 22 | 19 | 1.233 | .267 |
| No LBP | 114 | 143 | - | - |
a LBP, low back pain; LDD, lumbar disk degeneration. Dashes indicate not available.
Patient Characteristics (Study 2)
In study 2, the mean age of the 51 participants was 19.3 ± 0.8 years, and the mean gymnastics experience was 13.1 ± 3.3 years. There were 7 gymnasts in the regional group, 37 in the national group, and 7 in the international group. At baseline, height was significantly shorter in the international group than in the regional group (P < .05), and the years of experience in the international and national groups were significantly more than those of the regional group (P < .05 for both groups). However, there were no significant differences in the GJL or FFD among the 3 groups (Table 4).
Table 4.
Characteristics and Physical Function at Baseline in Study 2 Participants (n = 51) a
| Variable | Regional (n = 7) |
National (n = 37) |
International (n = 7) |
P |
|---|---|---|---|---|
| Age, y | 19.6 ± 1.4 | 19.3 ± 0.6 | 19.4 ± 0.8 | .605 |
| Height, cm | 167.4 ± 8.5 | 160.6 ± 7.6 | 156.5 ± 9.7 b | <.05 |
| Weight, kg | 60.6 ± 10.8 | 56.7 ± 8.2 | 53.3 ± 8.1 | .291 |
| BMI | 21.5 ± 2.1 | 21.8 ± 1.5 | 21.6 ± 1.6 | .816 |
| Experience, y | 9.4 ± 5.4 | 13.4 ± 2.5 c | 15.6 ± 1.6 c | <.01 |
| Beighton score, point | 1.7 ± 1.3 | 2.5 ± 1.5 | 1.9 ± 1.9 | .293 |
| FFD, cm | -20.3 ± 3.9 | -23.4 ± 4.9 | -25.6 ± 6.1 | .144 |
a Data are reported as mean ± SD unless otherwise indicated. BMI, body mass index; FFD, finger-floor distance.
b Significantly different from regional group (P < .05).
c Significantly different from regional group (P < .01).
Changes During the 2-Year Interval
At baseline MRI evaluation, 23 of the 51 gymnasts in study 2 (45.1%) had 1 or more degenerated disks. At the 2-year follow-up MRI evaluation, 24 gymnasts (47.1%) had 1 or more degenerated disks. Table 5 shows the degree of LDD at each spinal level according to modified Pfirrmann score at baseline and follow-up. For the international group, the degree of LDD was highest at L1/L2 (Figure 2).
Table 5.
Degree of LDD at Baseline and Follow-up in Study 2 a
| Regional (n = 7) | National (n = 37) | International (n = 7) | ||||
|---|---|---|---|---|---|---|
| Disk Level | Baseline | Follow-up | Baseline | Follow-up | Baseline | Follow-up |
| L1/L2 | 0 | 0 | 1 | 4 | 2 | 6 |
| L2/L3 | 0 | 0 | 3 | 4 | 1 | 2 |
| L3/L4 | 0 | 0 | 7 | 7 | 2 | 2 |
| L4/L5 | 1 | 2 | 11 | 10 | 0 | 0 |
| L5/S1 | 1 | 1 | 12 | 12 | 1 | 1 |
a Values are presented as modified Pfirrmann score (range, 0-15), where grades 1 and 2 (normal) = 0 points, grade 3 = 1 point, grade 4 = 2 points, and grade 5 = 3 points. LDD, lumbar disk degeneration.
Figure 2.
Progression of LDD at L1/L2 on sagittal T2-weighted MRI scans in gymnasts competing at the international level. (A) At baseline. (B) Two-year follow-up MRI scan showing a reduction in signal intensity of the intervertebral disk at L1/L2 (black arrow). LDD, lumbar disk degeneration; MRI, magnetic resonance imaging.
Logistic Regression for Predicting LDD occurrence
Using logistic regression analysis of study 2 data, we further examined the significant risk factors along with confounding factors. The presence of LDD at L1/L2 was significantly associated with competition level (adjusted odds ratio [OR], 47.8; 95% CI, 2.75-830.50; P = .008) (Table 6). Although competition level was a risk factor for LDD progression of the entire lumbar spine according to the crude OR (10.4; 95% CI, 1.78-60.6), there was no significant association according to the adjusted OR (6.58; 95% CI, 0.93-46.6; P = .059) (Table 7).
Table 6.
Logistic Regression Analysis for Predicting LDD at L1/L2 a
| Variable | Crude OR (95% CI) | Adjusted OR (95% CI) | P |
|---|---|---|---|
| Sex | 0.33 (0.40-3.06) | 0.06 (0.00-4.14) | .189 |
| Weight | 1.01 (0.91-1.11) | 0.95 (0.76-1.19) | .638 |
| Gymnastics experience | 1.22 (0.85-1.76) | 0.98 (0.69-1.40) | .930 |
| Competition level | 28.0 (3.56-220.2) | 47.8 (2.75-830.50) | .008 b |
a LDD, lumbar disk degeneration; OR, odds ratio.
b Significantly associated with presence of LDD at L1/L2 (P < .01).
Table 7.
Logistic Regression Analysis for Predicting LDD a
| Variable | Crude OR (95% CI) | Adjusted OR (95% CI) | P |
|---|---|---|---|
| Sex | 0.90 (0.20-4.13) | 0.42 (0.02-7.74) | .561 |
| Weight | 0.98 (0.90-1.07) | 0.96 (0.81-1.13) | .623 |
| Gymnastics experience | 1.33 (0.94-1.87) | 1.19 (0.84-1.67) | .322 |
| Competition level | 10.4 (1.78-60.6) | 6.58 (0.93-46.6) | .059 |
a LDD, lumbar disk degeneration; OR, odds ratio.
Discussion
These cross-sectional and prospective studies investigated the effects of competition level on the prevalence and incidence of LDD in Japanese collegiate gymnasts. In the cross-sectional study (study 1), the prevalence of 1 or more degenerated disks was not associated with the level of competition. However, the prevalence of LDD at L1/L2 in the international group was significantly higher than that in the other 2 groups. In the prospective study (study 2), the presence of LDD at L1/L2 was associated significantly with international-level competition.
Prevalence of LDD in International-Level Gymnasts
The main finding of this study was that the prevalence of LDD at L1/L2 was significantly higher in the international group. We also found that the international competition level for gymnasts was a risk factor for LDD at L1/L2. In general, LDD, particularly in the lower lumbar disks (L4/L5 and L5/S1), is commonly reported in the general population. 5,23 Similarly, the prevalence of LDD at each spinal level for 6 competitive sports was reported by Hangai et al, 8 who observed LDD predominantly in the lower lumbar disks. With regard to competition level, Kaneoka et al 9 found that the comparison of the prevalence of LDD between elite and recreational swimmers revealed that L5/S1 was degenerated significantly more frequently in elite swimmers. In gymnastics, a previous study found that LDD at the L1/L2 level was common among 24 male elite gymnasts. 21 Our study indicated that the prevalence of LDD in the lower lumbar disks was common among regional and national athletes. Therefore, we believe that gymnasts competing at the international level have a high frequency of L1/L2 LDD. In other words, we think that these morphological changes of the upper lumbar disk were sport-specific injuries of elite gymnasts.
Effects of Competition Level
In the present study, the presence of 1 or more degenerated disks was not associated with level of competition. These findings are somewhat in contrast to the results of Goldstein et al, 7 who found excessive LDD among Olympic-level gymnasts. One previous study on LDD in elite swimmers showed that lumbar disks in elite (high-load) swimmers were injured more frequently than were those in recreational (low-load) swimmers. 9 In general, there was an association between level of competition and the presence of 1 or more degenerated disks. On the contrary, in gymnastics, an epidemiology study found that subelite female gymnasts experienced more injuries to the lower back than did elite female gymnasts (19.4% and 9.2%, respectively). 12 In gymnastics, every 4 years, concurrently with the Olympic games, there are rule changes, and the skill level continues to evolve. As a result, even for regional group gymnasts, skills such as the Yurchenko vault, the Tkatchev, the uneven and horizontal bars, somersaults, and twists are difficult. Although there are no data on the loading of the lumbar disks during gymnastics skills, these skills require repetitive extension, flexion, and torsion motions of the spine. Therefore, we think that the level of competition has little effect on the prevalence of LDD in modern gymnasts.
GJL and the FFD
Several studies have reported that individuals with GJL are at an increased risk for musculoskeletal injury. 3,16,17,20 With regard to LDD, increased GJL has been associated closely with a lower prevalence of LDD in patients (age, 30-40 years), and the increased lumbar lordosis associated with GJL might explain the decreased risk of LDD demonstrated by Kim et al. 11 However, we could not obtain sagittal spinal alignment on lateral radiographs in this study. The reason why GJL was not a risk factor for LDD collegiate gymnasts is unknown. Thus, further investigation is needed to clarify the relationship between GJL and LDD. Similarly, FFD was not a risk factor for LDD in collegiate gymnasts. We considered that gymnasts perform specific actions such as hyperflexion and hyperextension of the spine, resulting in physical loading of the lumbar disks. Although a previous study indicated that a combination of repetitive flexion and extension increases the risk of injury to the spinal disks in animals, 24 LDD may occur during the growth spurt in gymnasts. Thus, we do not believe that FFD is a risk factor for LDD in collegiate gymnasts.
Limitations
Several limitations of this study should be acknowledged. First, it was not possible to consider other factors (ie, gene polymorphism, biomechanical factors, and muscle strength) to clarify the risk factors for LDD in Japanese collegiate gymnasts, although these are known to contribute to LDD. This limitation may have led to false-positive findings. We believe that additional studies to evaluate other factors are needed to establish the association between competition level and LDD progression. Second, the sample size was not large enough to reach a definitive conclusion in a prospective study. It was challenging to find 1 gymnastics team with many levels of competitive collegiate gymnasts with a relatively long history of gymnastics experience. Therefore, further studies with a larger sample population are required to confirm these findings. Finally, intraobserver agreement could not be assessed. MRI findings were evaluated by 2 experienced orthopaedic surgeons in our study. As the evaluators were medical doctors specializing in spinal disorders, we believe that their evaluation was highly reliable.
Conclusion
Although the prevalence of 1 or more degenerated disks was not associated with the level of competition, the prevalence and incidence of LDD was significantly higher at the L1/L2 disks in international Japanese gymnasts. The results of this study indicated that competition level is a risk factor for LDD at L1/L2 in Japanese collegiate gymnasts.
Acknowledgment
The authors thank Masataru Takahashi for providing technical assistance.
Footnotes
Final revision submitted March 14, 2022; accepted May 16, 2022.
One or more of the authors has declared the following potential conflict of interest or source of funding: This work was supported by a Japan Society for the Promotion of Science KAKENHI grant (16K01741). AOSSM checks author disclosures against the Open Payments Database (OPD). AOSSM has not conducted an independent investigation on the OPD and disclaims any liability or responsibility relating thereto.
Ethical approval for this study was obtained from Nippon Sport Science University (ref No. 009-G003).
References
- 1. Abdalkader M, Guermazi A, Engebretsen L, et al. MRI-detected spinal disc degenerative changes in athletes participating in the Rio de Janeiro 2016 Summer Olympics games. BMC Musculoskelet Disord. 2020;21(1):45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Beighton P, Solomon L, Soskolne CL. Articular mobility in an African population. Ann Rheum Dis. 1973;32(5):413–418. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Cameron KL, Duffey ML, DeBerardino TM, Stoneman PD, Jones CJ, Owens BD. Association of generalized joint hypermobility with a history of glenohumeral joint instability. J Athl Train. 2010;45(3):253–258. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4. Capel A, Medina FS, Medina D, Gómez S. Magnetic resonance study of lumbar disks in female dancers. Am J Sports Med. 2009;37(6):1208–1213. [DOI] [PubMed] [Google Scholar]
- 5. Cheung KM, Karppinen J, Chan D, et al. Prevalence and pattern of lumbar magnetic resonance imaging changes in a population study of one thousand forty-three individuals. Spine (Phila PA 1976). 2009;34(9):934–940. [DOI] [PubMed] [Google Scholar]
- 6. Folkvardsen S, Magnussen E, Karppinen J, et al. Does elite swimming accelerate lumbar intervertebral disc degeneration and increase low back pain? A cross-sectional comparison. Eur Spine J. 2016;25(9):2849–2855. [DOI] [PubMed] [Google Scholar]
- 7. Goldstein JD, Berger PE, Windler GE, Jackson DW. Spine injuries in gymnasts and swimmers: an epidemiologic investigation. Am J Sports Med. 1991;19(5):463–468. [DOI] [PubMed] [Google Scholar]
- 8. Hangai M, Kaneoka K, Hinotsu S, et al. Lumbar intervertebral disk degeneration in athletes. Am J Sports Med. 2009;37(5):149–155. [DOI] [PubMed] [Google Scholar]
- 9. Kaneoka K, Shimizu K, Hangai M, et al. Lumbar intervertebral disk degeneration in elite competitive swimmers: a case control study. Am J Sports Med. 2007;35(3):1341–1345. [DOI] [PubMed] [Google Scholar]
- 10. Kikuchi N, Min SK, Ueda D, Igawa S, Nakazato K. Higher frequency of the ACTN3 R allele + ACE DD genotype in Japanese elite wrestlers. J Strength Cond Res. 2012;26(12):3275–3280. [DOI] [PubMed] [Google Scholar]
- 11. Kim TH, Lee HM, Moon SH, et al. Joint laxity negatively correlates with lumbar disc degeneration in young adults. Spine (Phila Pa 1976). 2013;38(24):e1541–e1547. [DOI] [PubMed] [Google Scholar]
- 12. Kolt GS, Kirkby RJ. Epidemiology of injury in elite and subelite female gymnasts: a comparison of retrospective and prospective findings. Br J Sports Med. 1999;33(5):312–318. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Koyama K, Nakazato K, Min SK, et al. Anterior limbus vertebra and intervertebral disk degeneration in Japanese collegiate gymnasts. Orthop J Sports Med. 2013;1(3):2325967113500222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Koyama K, Nakazato K, Min S, et al. Radiological abnormalities and low back pain in gymnasts. Int J Sports Med. 2013;34(3):218–222. [DOI] [PubMed] [Google Scholar]
- 15. Kraft CN, Pennekamp PH, Becker U, et al. Magnetic resonance imaging findings of the lumbar spine in elite horseback riders: correlations with back pain, body mass index, trunk/leg-length coefficient, and riding discipline. Am J Sports Med. 2009;37(11):2205–2213. [DOI] [PubMed] [Google Scholar]
- 16. Lee SM, Oh SC, Yeom JS, et al. The impact of generalized joint laxity (GJL) on the posterior neck pain, cervical disc herniation, and cervical disc degeneration in the cervical spine. Spine J. 2016;16(12):1453–1458. [DOI] [PubMed] [Google Scholar]
- 17. Myer GD, Ford KR, Paterno MV, Nick TG, Hewett TE. The effects of generalized joint laxity on risk of anterior cruciate ligament injury in young female athletes. Am J Sports Med. 2008;36(6):1073–1080. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Nagashima M, Abe H, Amaya K, et al. Risk factors for lumbar disc degeneration in high school American football players: a prospective 2-year follow-up study. Am J Sports Med. 2013;41(9):2059–2064. [DOI] [PubMed] [Google Scholar]
- 19. Pfirrmann CW, Metzdorf A, Zanetti M, Hodler J, Boos N. Magnetic resonance classification of lumbar intervertebral disc degeneration. Spine (Phila PA 1976). 2001;26(17):1873–1878. [DOI] [PubMed] [Google Scholar]
- 20. Ramesh R, Von Arx O, Azzopardi T, Schranz PJ. The risk of anterior cruciate ligament rupture with generalised joint laxity. J Bone Joint Surg Br. 2005;87(6):800–803. [DOI] [PubMed] [Google Scholar]
- 21. Swärd L, Hellström M, Jacobsson B, Nyman R, Peterson L. Disc degeneration and associated abnormalities of the spine in elite gymnasts: a magnetic resonance imaging study. Spine (Phila Pa 1976). 1991;16(4):437–443. [DOI] [PubMed] [Google Scholar]
- 22. Takatalo J, Karppinen J, Näyhä S, et al. Association between adolescent sport activities and lumbar disk degeneration among young adults. Scand J Med Sci Sports. 2017;27(12):1993–2001. [DOI] [PubMed] [Google Scholar]
- 23. Teraguchi M, Yoshimura N, Hashizume H, et al. Prevalence and distribution of intervertebral disc degeneration over the entire spine in a population-based cohort: the Wakayama Spine Study. Osteoarthritis Cartilage. 2014;22(1):104–110. [DOI] [PubMed] [Google Scholar]
- 24. Thoreson O, Ekström L, Hansson HA, et al. The effect of repetitive flexion and extension fatigue loading on the young porcine lumbar spine, a feasibility study of MRI and histological analyses. J Exp Orthop. 2017;4(1):16. [DOI] [PMC free article] [PubMed] [Google Scholar]