The Sagittal Integral Morphotype in Male and Female Rowers

The goal of this study was to describe the integrated spinal assessment of the sagittal morphotype in rowers to determine whether the intense practice of rowing causes a modification of the sagittal curvatures of the spine, its relationship with the rowing technique, and training background. The second goal was to analyse how the dorsal and lumbar curves behave in the three phases of the rowing gesture, and to determine which phases can be detrimental to the correct development of the spine during growth. We analysed the spine curvatures in the sagittal plane of 29 females and 82 males, which were measured with an inclinometer in standing, slump sitting, maximal trunk flexion and during rowing performance. The average value of thoracic kyphosis in the rowers was 30° (mean, 30 + 8.27°). Thoracic hyperkyphosis was found in only two rowers (1.8%). Lumbar lordosis was within normal range in 84.1% of the males (mean, 27 + 9.57°) and 75.9% of female rowers (mean, 33°). Functional thoracic hyperkyphosis was observed in 57.4% of the males and 17.1% of the females. Functional lumbar hyperkyphosis was observed in 28 of the 69 males (40.5%) and five of 22 females (17.2%). Rowing seems to provide adequate spine alignment in the sagittal plane on standing. The integrated spinal assessment of the sagittal morphotype showed that half or our rowers presented with functional thoracic hyperkyphosis, and 43.2% presented with functional lumbar hyperkyphosis. Spine behaviour during the rowing technique shows that the thoracic kyphosis (98.2%) and lumbar spine (91%) perform within normative ranges and could explain the adequate positioning of the spine in the sagittal plane on standing. Years of rowing training tend to reduce thoracic kyphosis in males.


Participants
Participants were recruited from four different clubs associated with rowing federation in the southern region of Spain. Rowers, parents, and coaches were informed of the study procedures before the assessments were performed and all study participants provided written informed consents. Inclusion criteria were: belonging to a male or female rowers' club with membership in a rowing federation, participating in regional or national competitions, and having trained 18 h per week or more during the last six months [3]. Exclusion criteria were the presence of scoliosis (>20 • Cobb angle) or any spine deformity on the sagittal plane that required orthopedic treatment [3]. The final sample included 111 rowers; 29 females and 82 males. The mean age (±standard deviation) was 17.43 ± 3.25 years (men: minimum 14, maximum 35, average 17.2; women: minimum 14, maximum 26, average 17.8) and the mean years of training was 4.98 ± 3.77 (men: minimum 0.5, maximum 20, average 4.72; women: minimum 0.5, maximum 15, 5.73 average).

Measurements
Integrated spinal assessments of the sagittal morphotype were quantified in all participants [1,3] while wearing undergarments and barefoot. Thoracic and lumbar spine curvatures in the sagittal plane were measured in standing position, slump sitting (SS), and maximal trunk flexion (MTF), according to the assessment protocol defined by Santonja [34]. Measurements were performed by an orthopaedic consultant with 15 years of expertise, and athletes were assessed and data from every rower were obtained during the same session. Quantification of the sagittal curvatures of the spine was carried out with a Unilevel inclinometer (ISOMED, Inc., Portland, OR, USA). Upon standing, the inclinometer was placed at T1 to begin with, and then slid down to the end of the thoracic kyphosis, where the greatest value was observed. After resetting the inclinometer, the lumbar curve was quantified using the same procedure at this vertebral level. In order to quantify the thoracic and lumbar curves in SS and MTF, the inclinometer was placed at T1-T2, T12-L1 and L5-S1 [34][35][36]. Measurements were repeated twice to guarantee reliability ( Figure 1). by the Ethics and Scientific Committee of the University of Murcia (Spain) [ID: 1702/20

Participants
Participants were recruited from four different clubs associated with rowing fed tion in the southern region of Spain. Rowers, parents, and coaches were informed of study procedures before the assessments were performed and all study participants vided written informed consents. Inclusion criteria were: belonging to a male or fem rowers' club with membership in a rowing federation, participating in regional or nati competitions, and having trained 18 h per week or more during the last six months Exclusion criteria were the presence of scoliosis (>20° Cobb angle) or any spine deform on the sagittal plane that required orthopedic treatment [3]. The final sample included rowers; 29 females and 82 males. The mean age (±standard deviation) was 17.43 ± years (men: minimum 14, maximum 35, average 17.2; women: minimum 14, maxim 26, average 17.8) and the mean years of training was 4.98 ± 3.77 (men: minimum 0.5, m imum 20, average 4.72; women: minimum 0.5, maximum 15, 5.73 average).

Measurements
Integrated spinal assessments of the sagittal morphotype were quantified in all ticipants [1,3] while wearing undergarments and barefoot. Thoracic and lumbar spine vatures in the sagittal plane were measured in standing position, slump sitting (SS), maximal trunk flexion (MTF), according to the assessment protocol defined by Sant [34]. Measurements were performed by an orthopaedic consultant with 15 years of ex tise, and athletes were assessed and data from every rower were obtained during the s session. Quantification of the sagittal curvatures of the spine was carried out with a U level inclinometer (ISOMED, Inc., Portland, OR, USA). Upon standing, the inclinom was placed at T1 to begin with, and then slid down to the end of the thoracic kyph where the greatest value was observed. After resetting the inclinometer, the lumbar cu was quantified using the same procedure at this vertebral level. In order to quantify thoracic and lumbar curves in SS and MTF, the inclinometer was placed at T1-T2, T12 and L5-S1 [34][35][36]. Measurements were repeated twice to guarantee reliability (Figur Figure 1. Sagittal integral morphotype of the thoracic and lumbar spine (A) Standing assessm the inclinometer is placed at the beginning of the thoracic kyphosis before zeroing, and it is slid down to the greatest curve angle is observed. Once the inclinometer is zeroed, the lumbar c will be quantified with the same procedure. (B) Slump sitting quantification: cranial arrow po to the initial placement; the inclinometer was zeroed at T1-T2, before sliding it down to T12-L quantify the thoracic curve. The inclinometer was zeroed again at T12-L1 and slid down to L to quantify the lumbar curve. (C) Assessment in maximal trunk flexion: both arrows show the racic kyphosis limits. K = thoracic kyphosis; L= lumbar curve.
(A) (B) (C) Figure 1. Sagittal integral morphotype of the thoracic and lumbar spine (A) Standing assessment: the inclinometer is placed at the beginning of the thoracic kyphosis before zeroing, and it is then slid down to the greatest curve angle is observed. Once the inclinometer is zeroed, the lumbar curve will be quantified with the same procedure. (B) Slump sitting quantification: cranial arrow points to the initial placement; the inclinometer was zeroed at T1-T2, before sliding it down to T12-L1 to quantify the thoracic curve. The inclinometer was zeroed again at T12-L1 and slid down to L5-S1 to quantify the lumbar curve. (C) Assessment in maximal trunk flexion: both arrows show the thoracic kyphosis limits. K = thoracic kyphosis; L= lumbar curve.
The reliability of the researcher who carried out the measurements of the SIM was reflected as ICC: kyphosis in standing = 0.98; lordosis in standing = 0.94; kyphosis in sitting = 0.96; lumbar in sitting = 0.97; kyphosis in flexion = 0.87 and lumbar flexion = 0.97.
Normal values are considered when the measurements are within normative ranges in standing position, SS and MTF tests [34,35] and are summarised in Table 1. If the thoracic kyphosis was greater than 45 • , the measurements in self-correction of the kyphosis were also quantified. "Postural hyperkyphosis" was considered when the hyperkyphosis was reduced to ≤30 • during the self-correction tests [34,44]. The rowing stroke may be divided into drive and recovery phases. The drive phase includes the 'catch' when the oar enters the water, and the lumbar spine is fully flexed at this point of main work [20]. At the end of the drive phase, the oar is withdrawn, switching the lumbar spine to a relatively extended position. The 'finish' phase is a mid-way position during the drive and extension phases. Thoracic and lumbar spine measurements were also taken during the sport technique performance on the ergometer and these measurements were obtained during training against the usual resistance used with the ergometer. The measurements were at: (a) 'catch': maximal flexion of hip and trunk with the seat placed forward; (b) 'finish': participants sat upright on the seat, placed at full knee extension and elbows flexed towards the chest; (c) 'extension' position: maximal extension of the spine at the end of the stroke [20,27]. The inclinometer was placed and zeroed at T1-T2, before sliding it down to T12-L1 to quantify the thoracic curve. The inclinometer was zeroed again at T12-L1 and slid down to L5-S1 to quantify the lumbar curve. This procedure was carried out in the three positions in order to quantify both curves ( Figure 2) [1,3,5,10,12,30,35,44].
Age, gender, and year of training of each rower were also noted in order to correlate these factors to the sagittal plane spine measurements.

Statistical Analysis
All statistical analyses were carried out using MedCalc Statistical Software version 19.0.3 (MedCalc Software bvba, Ostend, Belgium). Initially, an exploratory analysis of the data was carried out, in which central tendency (median and mean), dispersion (95% confidence interval [CI] and standard deviation). Measures were calculated after performance of Shapiro-Wilk's test to verify normality. The percentages of rowers with spine curvatures outside the normative values were also calculated. An independent samples t-test or Mann-Whitney U test examined differences between genders. The correlations among the variables were examined using the Spearman's rank correlation coefficients (rho). The magnitude of the correlations was evaluated as trivial (r < 0.10), small (0.10 ≤ r < 0.30), moderate (0.30 ≤ r < 0.50), large (0.50 ≤ r < 0.70), very large (0.70 ≤ r < 0.90), and perfect (r ≥ 0.90) [16]. The acceptable type I error was set at p < 0.05 [45].

Statistical Analysis
All statistical analyses were carried out using MedCalc Statistical Software version 19.0.3 (MedCalc Software bvba, Ostend, Belgium). Initially, an exploratory analysis of the data was carried out, in which central tendency (median and mean), dispersion (95% confidence interval [CI] and standard deviation). Measures were calculated after performance of Shapiro-Wilk's test to verify normality. The percentages of rowers with spine curvatures outside the normative values were also calculated. An independent samples t-test or Mann-Whitney U test examined differences between genders. The correlations among the variables were examined using the Spearman's rank correlation coefficients (rho). The magnitude of the correlations was evaluated as trivial (r < 0.10), small (0.10 ≤ r < 0.30), moderate (0.30 ≤ r < 0.50), large (0.50 ≤ r < 0.70), very large (0.70 ≤ r < 0.90), and perfect (r ≥ 0.90) [16]. The acceptable type I error was set at p < 0.05 [45].

Results
The demographic features of the participants, significant differences between male and female rowers, and the average descriptive values of the sagittal curves can be found in Table 2. The independent t-test or Mann-Whitney U test showed no differences in age (p = 0.35) or years of training (p = 0.49) between the genders. The female participants showed greater lumbar lordotic angles than the males in standing position (p = 0.0008), but lower angles of lumbar kyphosis in SS (p = 0.028), and MTF (p = 0.0026) than the males. Thoracic kyphosis values were similar in standing position between the genders, but lower values in women were observed in SS (p = 0.003), and MTF (p = 0.045).

Results
The demographic features of the participants, significant differences between male and female rowers, and the average descriptive values of the sagittal curves can be found in Table 2. The independent t-test or Mann-Whitney U test showed no differences in age (p = 0.35) or years of training (p = 0.49) between the genders. The female participants showed greater lumbar lordotic angles than the males in standing position (p = 0.0008), but lower angles of lumbar kyphosis in SS (p = 0.028), and MTF (p = 0.0026) than the males. Thoracic kyphosis values were similar in standing position between the genders, but lower values in women were observed in SS (p = 0.003), and MTF (p = 0.045). The sport technique analysis showed that the values of thoracic kyphosis during the three phases of rowing (95% CI at 'catch', 'finish' and 'extension') were within the normal range (Table 2) in trunk flexion (≤65 • ), and were reduced in females during 'catch' (p = 0.0026) and 'finish' (p = 0.008). Thoracic extension values are similar in the male and female participants. Only one rower reached 74 • during the 'catch' phase and 66 • during the 'extension' phase. Another rower reached 68 • during the 'extension' phase, but the rest of the participants showed thoracic kyphosis curves within the normal values.
The 95% CI of the lumbar curve angles were within normal ranges during trunk flexion (10-30 • ) and were significantly lower in women than in men during the three phases of rowing (p = 0.0001). Ten rowers exceeded the normative 30 • during the 'catch' phase (9%), and a lordotic curve was observed in 25 rowers during the 'extension' phase. Table 3 summarises the number of cases according to the classical diagnosis in the standing position of the thoracic and lumbar spines, the sagittal morphotype of the spine integrating the three tests (in the last column of the table), and the percentage of rowers whose measurements were outside the normative values. In total, 91.5% of the males and 86.2% of the females possessed thoracic kyphosis in standing position within the normative values (20-45 • ). Thoracic hyperkyphosis (>45 • ) was observed in only one male (50 • ) and one female rower (55 • ), but both showed a curve reduction to <30 • during the self-correction test [34,44] (postural hyperkyphosis). Of the male participants, 84.1%, and 75.9% of the females showed lumbar lordosis within the normative ranges. Only two males and six female rowers had hyperlordosis (>40 • ) and all of them presented with postural hyperlordosis (lumbar curve in flexion with kyphosis of 10-30 • ) [34,35].
Regarding the integrative sagittal morphotype, 57.4% of the male rowers had "functional thoracic hyperkyphosis" (normal range kyphosis in standing position with adopted hyperkyphotic attitude during SS and/or MTF; Figure 3), and this finding was three times less frequent in females (17.1%). Twenty-eight of 69 male rowers (40.5%) and five of 22 female rowers (17.2%) with normal lordosis in standing were diagnosed with functional lumbar hyperkyphosis (lumbar kyphotic posture was quantified >30 • in the MTF and/or >20 • SS tests) ( Figure 4).

Discussion
This research is the first work describing the effect of rowing training on thoracic kyphosis and lumbar lordosis in standing, as well as the effect of rowing training on the SIM of the spine in this sport. Our main relevant findings showed how the kyphosis and lordosis adapt to the rowing technique training. A high percentage of functional thoracic hyperkyphosis was observed (57.4% in the male rowers; three times less in women [17.1%]). Functional lumbar hyperkyphosis was observed in 34.1% of the male rowers, while only half of the female rowers showed this lumbar spine adaptation (17.2%). The female gender seemed to play a protective role for the dynamic adaptation of the spine. Also, our research compared the behaviour of the thoracic and lumbar segments during the three phases of rowing, and our results showed that the thoracic and lumbar spine performed within normal ranges. This could be useful to understand the relationship between back pain and spine adaptations, as well as the need for preventive programmes in this sport.
Low frequencies of thoracic hyperkyphosis in male (1.2%) and female (3.4%) rowers were observed in our study and all cases of thoracic hyperkyphosis were flexible when assessed with self-correction tests [34,44]. This adequate positioning of the thoracic spine in the standing position suggests that rowing is a protective sport against thoracic hy-

Discussion
This research is the first work describing the effect of rowing training on thoracic kyphosis and lumbar lordosis in standing, as well as the effect of rowing training on the SIM of the spine in this sport. Our main relevant findings showed how the kyphosis and lordosis adapt to the rowing technique training. A high percentage of functional thoracic hyperkyphosis was observed (57.4% in the male rowers; three times less in women [17.1%]). Functional lumbar hyperkyphosis was observed in 34.1% of the male rowers, while only half of the female rowers showed this lumbar spine adaptation (17.2%). The female gender seemed to play a protective role for the dynamic adaptation of the spine. Also, our research compared the behaviour of the thoracic and lumbar segments during the three phases of rowing, and our results showed that the thoracic and lumbar spine performed within normal ranges. This could be useful to understand the relationship between back pain and spine adaptations, as well as the need for preventive programmes in this sport.
Low frequencies of thoracic hyperkyphosis in male (1.2%) and female (3.4%) rowers were observed in our study and all cases of thoracic hyperkyphosis were flexible when assessed with self-correction tests [34,44]. This adequate positioning of the thoracic spine in the standing position suggests that rowing is a protective sport against thoracic hyperkyphosis in men and in women. In contrast, 51.8% of hyperkyphosis has been reported in high-level swimmers younger than 15 years old [5,7]. A low frequency of lumbar hyperlordosis was also observed in the male participants (3.7%), indicating that rowing may be beneficial in men with lumbar hyperlordosis.

Thoracic Kyphosis
The average value of thoracic kyphosis in standing position was lower in rowers (30 • ) than in other sports ( Table 5). This value was lower than those of artistic [3] and trampoline gymnasts [4], climbers [8], swimmers [5], weightlifters [10], tennis players [31], and hockey players [1]. These values are even more favourable than those of scholars [35,[39][40][41] adolescents [42], and non-athletic adults (controls) [12,46]. Thoracic kyphosis of rowers in standing position showed similar values to rhythmic [46] and aesthetic group gymnasts [47]. Only dancers [12,48] showed lower values of thoracic kyphosis in standing, probably due to the posture work and body scheme required in this discipline. No significant differences between genders in this measurement was uncommon.

Sagittal Integral Morphotype
The SIM [34] included the quantification of the curves in at least three different positions (standing, SS and MTF), and implies the definition of new diagnostic concepts.
The diagnosis of functional thoracic hyperkyphosis is clinically relevant during pubertal growth spurs because curves could become structural, according to Bado [50]. In our rowers, the functional thoracic hyperkyphosis due only to hyperkyphosis in SS represented 84.6% of total functional thoracic hyperkyphosis in rowers, suggesting bad postural hygiene in sitting. In contrast, the functional thoracic hyperkyphosis due to hyperkyphosis in MTF (15.4%) could denote an adaptation to the sport performance. The wedging of immature vertebral bodies is another potential consequence in high-performance rowers, as observed in other young athletes [7,22,23], due to repetitive trunk flexion movements [24].
If the sagittal spinal assessment would have been carried out in standing position only, the majority of the rowers would have shown thoracic and lumbar curves within the normative values. This supports the integrated spinal assessment of the sagittal morphotype as a more specific screening tool.
4.6. Curve Adaptation According to Sport Technique, Age, and Years of Training 4.6.1. Age and Years of Training Thoracic kyphosis tends to reduce with years of training in male rowers (rho = −0.258), but not in female rowers. This positive effect could explain why the majority of the male rowers' thoracic kyphosis measurements (91.3%) fell within the normal range. This is an unusual finding because thoracic kyphosis tends to increase with age [57], and should make us think about the potential benefits of this sport. Lumbar lordosis was not correlated to years of training and tended to reduce with age, only in male rowers (rho = −0.302).

Sport Technique
Reduced thoracic kyphosis during the three rowing phases in males and during two phases in females ('finish' and 'extension') was observed. Technique performance seems to perfect with age, leading to less kyphotic positioning; thus, explaining our adaptative results.
Lumbar lordosis increased only in females during the 'extension' phase (rho = 0.503) (X = −5.55 ± 11.1; 95% CI = −8.0-0.0; p < 0.0001). Again, this finding supports the benefits of this sport on the spine position in the sagittal plane. Wilson et al. [27] have also shown higher maximal flexion values between L2-L4 during rowing stroke (mean maximum flexion angle, 54.38 ± 9.48 • (range, 35.88-75.98 • ). Differences in spine positioning during rowing between males and females have been observed in our sample in regards to lumbar spine performance, but no differences in age or years of training have been observed.
The SIM studies the baseline postural adaptation as a result of years of a specific training, not spinal movement during the sport performance. This methodology allows comparison between different sport disciplines, as well as plotting to normative [1,3] and developmental data [58].
The lumbar spine was kyphotic during the three phases of the rowing technique in the male rowers, and in the 'catch' and 'finish' phases in the females, but all average values were within the normative value range for flexion tests. The average convexity values were greater during 'catch', and progressively reduced during the 'finish' and 'extension' phases for both genders. The male rowers showed significantly more lumbar flexion during the whole performance, and females even showed some degrees of lumbar lordosis at the end of the stroke.
Our large sample size and no significant differences in terms of age and years of training between the genders allowed us to observe the specific distribution of the sagittal morphotype of the spine in rowers, which has been previously described in other sports (Table 5). Future studies understanding the development of this integrative spinal assessment in regards to years of training, as well as its relationship with back pain in rowers, are recommended. Lumbar curvatures in the slump sitting and trunk forward bending positions, together with height, have been recently found as predicting factors of sciatica history in female classical ballet dancers [32]. Recurrent lower back pain has been related to the lumbar curve during trunk flexion, as well as reduced hamstring extensibility [33,59]. Hamstring length and demands are factors to consider in future analyses of rowers.
Nugent et al. [60] found that rowers without lower back pain, or considered "healthy", have different kinematics (including flatter low back spinal position at the 'finish' phase) than those with lower back pain (larger lumbar kyphosis). McGregor et al. [61] found that rowers with lower back pain had significantly less range of motion at the L5/S1 level (in the 'catch' position: 7.5 ± 1.3 • in normal; 4.8 ± 1.2 • in previous history of lower back pain groups; and 2.8 ± 5.5 • in current lower back pain group). Recently, Cejudo et al. [59] found a relationship between lower back pain and static functional lumbar hyperkyphosis, and structured hyperlordosis in male and female team sports players.
Functional adaptations of the spinal sagittal curves seem to be the response to biomechanical stresses [62] and does not always depend on the years of training, but appear to be specific to each sport technique [1,3,8]. Future studies may also describe the effect of preventive intervention for the functional adaptations described.
The limitations of our study include the lack of radiographic assessment of the three positions, to establish the correlation with inclinometer quantification. Secondly, it has not been possible to measure the sagittal curves dynamically during the rowing performance, as there are no reliable measurement systems that would allow to quantify the curves of the back subjected to the workloads. On the other hand, the reliability of the inclinometer has already been studied against radiographs [7,37,38,63], and ethical limitations were found to irradiate healthy adults for non-clinical reasons.
The clinical relevancy of our research was to present that rowers are less hyperkyphotic than the general population and other sportsmen (Table 5). This was also observed in the lumbar spine, indicating that rowing may have a lumbar kyphosis-reductive effect in females, while this finding has been found to frequently increase in scholars and teenagers [35]. Regardless of this, spine alignment remained within normative ranges of lumbar kyphosis during the 'extension' and 'finish' phases of the rowing technique. A total of 9% showed lumbar kyphosis larger than 30 • that has been related to lower back pain [60].
Future research will require the determination of the relationship of back pain to the integrated spinal assessment of the SIM in rowers. Also, establishing a specific threshold for lumbar kyphosis during the 'catch' and 'extension' phases will guide the sport technique to prevent back pain due to functional lumbar hyperkyphosis.

Conclusions
Rowing seems to provide appropriate spine positioning in the sagittal plane in the standing position, since 90% of high competition rowers showed kyphosis and lordosis values within the normal range. The SIM indicated that half of the male rowers had thoracic functional hyperkyphosis, and almost half presented with functional lumbar hyperkyphosis. In contrast, lumbar hyperlordosis is the rowing adaptation more often observed in female rowers (20.7%), while functional thoracic hyperkyphosis and functional lumbar hyperkyphosis are less frequently observed in female rowers.
Spine behaviour during the rowing technique shows that thoracic kyphosis (98.2%) and the lumbar spine (91%) perform within normative ranges, which could explain the adequate positioning of the spine in the sagittal plane upon standing. Years of rowing training tend to reduce thoracic kyphosis in males.

Data Availability Statement:
The data used to support the findings of this study are available from the corresponding author upon request.