Menarche in Scoliotic and Non-Scoliotic Balkan Girls and the Relationship between Menarche and the Laterality of Scoliotic Curves

Abstract

Background:
Menarche, as an important parameter in the assessment of scoliosis progression in girls, is proven to be dependent on geographical latitude. The aim of this study was to determine whether the age of menarche differs in scoliotic and non-scoliotic Balkan girls and the relationship between menarche and the laterality of scoliotic curves.

Participants and methods:
This is a retrospective study with three groups: scoliotic, non-scoliotic, and control. Patient data collection and analysis were approved by the Ethical Committee of the Institute.

Statistical analysis:
The SPSS 24 program was used, and we employed One-way ANOVA, Fisher's, and Chi-squared tests to compare different groups. Statistical significance was defined as p < 0.05.

Results:
No statistically significant difference was found in the age of menarche between the three groups (p = 0.168). In the scoliotic postmenarchal group, the primary right curve was dominant in 54.80%, while in the scoliotic premenarchal group, the primary left curve was dominant in 60.09% (p < 0.01).

Conclusion:
In Balkan girls from Bosnia and Herzegovina and Serbia, there was no significant difference in the age of menarche between scoliotic and non-scoliotic girls. A significant difference was found in the laterality of the primary curve in premenarchal and postmenarchal scoliotic girls.

Full text

Citation: Pjanic, S.; Jevtic, N.; Grivas,
T.B. Menarche in Scoliotic and
Non-Scoliotic Balkan Girls and the
Relationship between Menarche and
the Laterality of Scoliotic Curves. J.
Clin. Med. 2024,13, 132. https://
doi.org/10.3390/jcm13010132
Academic Editors: Hideaki Nakajima
and Kanji Mori
Received: 24 October 2023
Revised: 19 December 2023
Accepted: 21 December 2023
Published: 26 December 2023
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
Journal of
Clinical Medicine
Article
Menarche in Scoliotic and Non-Scoliotic Balkan Girls and
the Relationship between Menarche and the Laterality of
Scoliotic Curves
Samra Pjanic 1, Nikola Jevtic 2and Theodoros B. Grivas 3, *
1Department of Pediatric Rehabilitation, Institute for Physical, Rehabilitation Medicine and Orthopedic
Surgery “Dr Miroslav Zotovic”, 78000 Banja Luka, Bosnia and Herzegovina; samra.pjanic@hotmail.com
2Scolio Centar, 403916 Novi Sad, Serbia; njevticns@gmail.com
3Former Head of Department of Traumatology and Orthopaedics, “Tzaneio” General Hospital of Piraeus,
18536 Piraeus, Greece
*Correspondence: tgri69@otenet.gr
Abstract: Background: Menarche, as an important parameter in the assessment of scoliosis pro-
gression in girls, is proven to be dependent on geographical latitude. The aim of this study was to
determine whether the age of menarche differs in scoliotic and non-scoliotic Balkan girls and the
relationship between menarche and the laterality of scoliotic curves. Participants and Methods: This
is a retrospective study with three groups: scoliotic, non-scoliotic, and control. Patient data collection
and analysis were approved by the Ethical Committee of the Institute. Statistical Analysis: The
SPSS 24 program was used, and we employed One-way ANOVA, Fisher’s, and Chi-squared tests to
compare different groups. Statistical significance was defined as p< 0.05. Results: No statistically
significant difference was found in the age of menarche between the three groups (p= 0.168). In
the scoliotic postmenarchal group, the primary right curve was dominant in 54.80%, while in the
scoliotic premenarchal group, the primary left curve was dominant in 60.09% (p< 0.01). Conclusion:
In Balkan girls from Bosnia and Herzegovina and Serbia, there was no significant difference in the
age of menarche between scoliotic and non-scoliotic girls. A significant difference was found in the
laterality of the primary curve in premenarchal and postmenarchal scoliotic girls.
Keywords: menarche; idiopathic scoliosis; Balkan
1. Introduction
Idiopathic scoliosis represents a three-dimensional deformity of the spine and thorax
that can occur at any age in growing children, and it especially progresses during the
pubertal rapid growth spurt. IS occurs in 80% of all scoliosis cases, while the remaining
20% represent secondary scoliosis due to other pathological conditions [
1
]. Depending on
the age of occurrence, it can be classified as infantile (0–3 years of age), juvenile (4–9 years
of age), and adolescent idiopathic scoliosis (10–18 years of age) [
2
]. The greatest risk of
progression is expected during puberty due to the peak height velocity. Progressive cases
of AIS are much more frequent in girls than in boys, with a ratio of 7:1 in favor of girls,
with Cobb angle values above 30◦[1].
Many studies have been conducted regarding the aetiopathogenesis of IS [
3
,
4
], sug-
gesting there is a multifactorial cause including genetic [
5
] and epigenetic factors [
6
]; the
central nervous system; skeletal spinal growth; bone metabolism; metabolic pathways;
biomechanics; and other factors, yet its etiology still remains unclear [7,8].
The risk of scoliosis progression is related to growth potential, which can be deter-
mined by the assessment of skeletal maturity. Bone age as an essential parameter for
evaluating the remaining growth during puberty can be determined based on pelvis and
upper limb radiographs (elbow, hand, wrist and humeral head ossification [
9
]). One of the
J. Clin. Med. 2024,13, 132. https://doi.org/10.3390/jcm13010132 https://www.mdpi.com/journal/jcm

J. Clin. Med. 2024,13, 132 2 of 12
most important and used indicators of skeletal maturity is the Risser sign [
10
], due to the
fact it can often be assessed on the same spine radiograph as the Cobb angle. The Risser
sign is assessed by the ossification of the iliac apophysis divided into five stages (0 to 5)
and is displayed on full AP or PA spine radiographs on the pelvic iliac crest. The most
growth potential is expected between Risser sign 0 and 2, whereas Risser sign 0 covers
about two-thirds of puberty and therefore can be misleading [
11
]. Therefore, the Risser
sign has been proven to have limited sensitivity during peak growth velocity, and there is
the possibility of high mismatch risk and mistreatment [
12
]. For this reason, there is a need
for additional parameters that can help in the assessment of growth potential and risk of
scoliosis progression.
There are also some other skeletal maturity indicators, such as Sanders [
13
] and elbow
triradiate cartilage classification [
14
], that are not widely utilized in clinical practice due to
additional radiation (the need to radiograph the wrist or elbow). There is a clear correlation
between growth velocity and skeletal maturation [15].
Among the clinical parameters, data about age at menarche are considered to be
important, along with biometric measurements and Tanner stages [
16
]. The most important
biometric measurements include standing height, sitting height, arm span, and weight,
which should be repeated and recorded at regular intervals. The sitting height is more
accurate than the standing height since the trunk and lower extremities grow at different
rates. When the sitting height is approximately 84 cm, 80% of girls experience menarche.
The Tanner stages signal the development of secondary sexual characteristics throughout
the course of puberty. Tanner stage 2 marks the beginning of puberty, with the first
appearance of pubic hair, the budding of the nipples, and the swelling of the testes as the
first physical signs of the onset of puberty [
11
]. The age at the menarche onset is also one of
the indicators of the remaining growth potential in girls [
17
]. Some authors state that it is
considered to be even more reliable than the Risser sign [18].
The first physical sign of puberty occurs about 2 years before menarche, and final
height is usually achieved 2.5–3 years after menarche. In girls, menarche occurs at age 13.5
years of bone age, usually at Risser grade I [
11
]. After girls experience menarche, there is a
gradual decrease in the scoliosis progression risk. This is due to the fact that at the time of
menarche, approximately two-thirds of the period of the pubescent growth spurt and the
peak of growth have passed. The potential for scoliosis progression is much lower after
spinal growth and skeletal maturation are complete [2].
The late onset of menarche correlates with delayed skeletal maturity and a higher
prevalence of AIS. For this reason, in girls who experience menarche later, there is a pro-
longed period of spine vulnerability and a greater possibility of scoliosis progression [19].
Taking everything above into consideration, data about menarche in girls can provide
clinicians with additional information about remaining growth, helping them to assess the
risk of progression and therefore guide them in treatment decisions.
For this reason, the age of menarche onset is a parameter that has been documented
during the clinical assessment and follow-up of scoliotic patients in many clinics around
the world and during school screening programs.
There are a few studies showing that melatonin may play a role in the pathogenesis
of scoliosis, supporting the neuroendocrine hypothesis [
20
]. Melatonin, as a hormone
produced mainly in the pineal gland but also in the retina, is called “the light of the night”
since its synthesis and release are stimulated by the darkness and inhibited by the light.
Among many other roles, melatonin influences the sexual maturation process by reducing
the secretion of gonadotropins, mainly LH. This is related to the occurrence of menarche,
which arises as the melatonin levels decrease during growth, influencing the onset of
puberty [21–23].
This can explain why different sunlight exposure, depending on geographical location
and equatorial distance, influences melatonin secretion and modifies age at menarche.
Therefore, the role of melatonin can be extended to the findings that menarche depends on
geographical latitude [24–28].

J. Clin. Med. 2024,13, 132 3 of 12
This might be a reason why reported AIS prevalence in the literature increases
in the northern geographic latitudes and decreases with latitudes approaching the
equator [29–45].
This claim is supported by the epidemiological data on AIS prevalence in different
countries, showing that Finland has the highest geographical latitude and an AIS prevalence
of 12% and Singapore has the lowest geographical latitude and an AIS prevalence of 0.93%.
When assessing the influence of geographic factors, it is important to distinguish them
from socioeconomic circumstances [46].
There is also a higher prevalence of scoliosis in a population of blind women (42.3%)
compared to the prevalence in the general population of the same region (2.9%) [47]. This
finding contributes to the possible role of melatonin in IS etiopathogenesis. In blind women,
there is an increased production of melatonin due to a lack of light, which leads to late
menarche and a prolonged period of spine vulnerability.
The only country in the Balkan region that has published data on AIS prevalence is
Greece [48].
When comparing scoliotic and non-scoliotic girls in the Mediterranean region, no
statistically significant difference has been found in the age of menarche. On the other hand,
there was a statistically significant difference between menarche-positive and menarche-
negative scoliotic girls in relation to the laterality of scoliotic curves [
17
]. The laterality of
the curve is defined as the deviation of the spine in the frontal plane and is represented
by the Cobb angle, measured on the full spine radiograph in PA projection. It is the most
documented measurement, frequently used in scoliotic patients for follow-up and treatment
outcomes, and it is also considered one of the main predictors of progression [49].
To our knowledge, there are no data about age of menarche in scoliotic and non-
scoliotic girls in the Balkan countries of Serbia and Bosnia and Herzegovina.
The aims of the study were to determine whether the age of menarche differs in
scoliotic and non-scoliotic Balkan girls; to compare the results to the findings from other
countries, and to assess the relationship between menarche and the laterality of
scoliotic curves.
2. Patients and Methods
2.1. Study Design
A retrospective study based on prospectively collected clinical data was conducted in
Bosnia and Herzegovina and Serbia.
2.2. Participants
Participants for the study were selected among 2000 patients of the Institute for
Physical, rehabilitation medicine and orthopedic surgery “Dr Miroslav Zotovic” in Banja
Luka (Bosnia and Herzegovina) and healthy girls randomly selected during screening in
sports clubs in Novi Sad (Serbia). Patient data collection and analysis were approved by
the Ethical Committee of the Institute.
2.3. Methods
Criteria for the inclusion in the study were gender and Cobb angle. Since our research
is based on menarche, boys were automatically excluded from the study. The girls enrolled
in the study were referred to our clinic due to clinical trunk asymmetry detected during
official school screening or by other health professionals or parents. The girls who showed
asymmetry in the Adam’s bending test and had scoliometer readings
≥
5
◦
were referred for
further diagnostics. The golden standard used to diagnose scoliosis consisted of a full spine
radiograph in PA projection performed in our clinic. Scoliosis was defined by the SRS defini-
tion as the curve with a Cobb angle
≥
10
◦
. Scoliosis was excluded if the Cobb angle was <10
◦
.
The Cobb angle was measured in the TraumaCad
®
(https://www.brainlab.com/surgery-
products/orthopedic-surgery-products/orthopedic-templating-software/ (accessed on 23
October 2023)) software program with a focus on the primary scoliotic curve, defined as the

J. Clin. Med. 2024,13, 132 4 of 12
curve with the most structural vertebral changes in terms of lateral deviation and rotation.
The girls in Serbia were examined as part of the regular screening program in amateur
sports clubs, where they were engaged in some type of sports training up to 4 times a
week. In the control group, we included the girls with no trunk asymmetry in the standing
position or Adam’s bending test or with any signs of scoliosis.
According to the above-described parameters, the participants were divided into three
groups: scoliotic group, non-scoliotic group, and control group.
The scoliotic group consisted of 494 patients, with a mean age of 12.57
±
2.4 years
(interval 7 to 18 years) and an average Cobb angle of 20.44
±
10.88
◦
. The non-scoliotic
group consisted of 523 patients, with a mean age of 11.51
±
2.71 years (interval 7 to 18 years)
and an average Cobb angle of 6.71
±
1.76
◦
. The control group consisted of 86 healthy girls,
with a mean age of 13.63 ±1.54 years (interval 10 to 17 years).
3. Statistical Analysis
Statistical analysis was performed using the program SPSS Inc. (Chicago, IL, USA),
released in 2016 (SPSS for Windows, Version 24.0. Chicago, IL, USA).
The results are presented as frequency and percentage (for all participants in three
main groups—scoliotics, non-scoliotics, and control and subgroups—according to the age
of menarche and BMI level), mean and standard deviation (SD) (for average age and body
height of the participants), and median and interquartile range—IQR (for Risser sign).
One-way ANOVA was used to compare the groups and determine if there were statistically
significant differences between them, measured on interval scale, with normal distribution.
Tukey’s HSD test was used as a post hoc test if there was significant difference between
groups. Fisher’s test was used to compare the groups measured on nominal or ordinal
scales (BMI level). A Chi-squared test was used when the frequency in the categories was
less than 5. Statistical significance was defined as p< 0.05.
4. Results
There were 1017 girls selected among patients for the first 2 groups and 86 healthy
girls in the control group.
Data on the height of all participants and according to the age of menarche, as well as
a comparison between the groups, are presented in Table 1.
Table 1. Comparison between scoliotic, non-scoliotic and control groups according to height.
Height (cm) Scoliotic Non-Scoliotic Control pValue
All patients 159.1 ±12.5 153.8 ±14.1 166.7 ±9.7 p< 0.001 a
Premenarchal 150.2 ±12.8 145.2 ±11.7 154.3 ±6.0 p< 0.001 a
Postmenarchal 165.9 ±6.7 165.7 ±6.3 169.8 ±7.3 p< 0.001 a
Results are presented as mean ±sd. aOne-way ANOVA, post hoc Tukey’s HSD.
There was a significant difference in height between the three groups (p< 0.001). The
girls in the control group were significantly taller than the participants in the other two
groups (scoliotics and non-scoliotics). With post hoc analysis and according to the age of
menarche, a significant difference was found in premenarchal girls between the control and
non-scoliotic groups (p< 0.001), as well as in postmenarchal girls between the control and
scoliotic groups (p= 0.020).
To form BMI categories for the participants, the CDC growth reference chart for
girls was used, with five categories according to percentiles: Underweight (<5 percentiles),
Healthy Weight (5 to 85 percentiles), Overweight (85 to 95 percentiles), Obesity
(>95 percentiles), Severe Obesity (>95 percentiles ×1.2), Table 2.
There was no statistically significant difference between the scoliotic, non-scoliotic
and control groups according to BMI for all girls (p= 0.073), premenarchal girls (p= 0.560)
and postmenarchal girls (p= 0.128). There was also no statistically significant difference

J. Clin. Med. 2024,13, 132 5 of 12
in the scoliotic group between premenarchal and postmenarchal girls (Chi-squared test,
p= 0.371).
Table 2. Comparison between scoliotic, non-scoliotic and control groups according to BMI.
Underweight Healthy
Weight Overweight Obesity Severe Obesity pValue
All patients
Scoliotic 52 (10.5%) 377 (76.3%) 42 (8.5%) 22 (4.5%) 1 (0.2%)
p= 0.073 a
Non-scoliotic 32 (6.1%) 404 (77.2%) 58 (11.1%) 26 (5.0%) 3 (0.6%)
Control 4 (4.7%) 75 (87.2%) 6 (7.0%) 1 (1.2%) 0 (0.0%)
Premenarchal
Scoliotic 25 (11.7%) 155 (72.8%) 23 (10.8%) 10 (4.7%) 0 (0.0%)
Non-scoliotic 24 (7.9%) 226 (74.1%) 36 (11.8%) 18 (5.9%) 1 (0.3%) p= 0.560 a
Control 2 (11.8%) 15 (88.2%) 0 (0.0%) 0 (0.0%) 0 (0.0%)
Postmenarchal
Scoliotic 27 (9.6%) 222 (79.0%) 19 (6.8%) 12 (4.3%) 1 (0.4%)
p= 0.128 a
Non-scoliotic 8 (3.7%) 178 (81.7%) 22 (10.1%) 8 (3.7%) 2 (0.9%)
Control 2 (2.9%) 60 (87.0%) 6 (8.7%) 1 (1.4%) 0 (0.0%)
aChi-squared test.
The Risser sign was homogenized and there was no significant difference between the
groups (Chi-square test, p= 0.461).
Data about the age of participants and age at menarche in all three groups are presented
in Table 3.
Table 3. Age and age at the onset of menarche in all three groups of girls: scoliotics, non-scoliotics
and healthy girls.
Menarche
TOTAL
Yes No
Scoliotics
N 281 213 494
% 56.88% 43.12% 100%
Age Age at menarche Age Age
Mean 14.04 12.38 10.63 12.57
SD 1.50 1.11 1.95 2.40
Min-max 10–18 9–15 7–16 7–18
Non-scoliotics
N 218 305 523
% 41.68% 58.32% 100%
Age Age at menarche Age Age
Mean 13.92 12.18 9.78 11.51
SD 1.69 1.22 1.85 2.71
Min-max 11–18 8–15 7–15 7–18
Control group
N 69 17 86
% 80.23% 19.77% 100%
Age Age at menarche Age Age
Mean 14.07 12.26 11.82 13.63
SD 1.28 1.22 1.19 1.54
Min-max 12–17 10–15 10–14 10–17

J. Clin. Med. 2024,13, 132 6 of 12
In the scoliotic group, 281 girls (56.88%) with a mean age of 14.04
±
1.50 (range 10–18)
were postmenarchal (mean age at menarche 12.38
±
1.11), while 213 girls (43.12%) with a
mean age of 10.63 ±1.95 (range 7–16) were premenarchal.
In the non-scoliotic group, 218 girls (41.68%) with a mean age 13.92
±
1.69 (range 11–18)
were postmenarchal (mean age at menarche 12.18
±
1.22), while 305 girls (58.32%) with a
mean age of 9.78 ±1.85 (range 7–15 years) were premenarchal.
In the control group, 69 girls (80.23%) with a mean age of 14.07
±
1.28 (interval 12–17)
were postmenarchal (mean age at menarche 12.26
±
1.22 (range 10–15), while 17 girls were
premenarchal (mean age at menarche: 11.82 ±1.19 (range 10–14).
No statistically significant difference was found in age of menarche between the three
groups (p= 0.168), presented in Table 4.
Table 4. Difference in age of menarche in scoliotic and non-scoliotic girls.
Scoliotic Non-Scoliotic Control Group pValue
N 281 218 69 0.168 a
Age (years) 12.38 ±1.11 12.18 ±1.22 12.26 ±1.22
at-test.
The mean Cobb angle of non-scoliotic girls was 6.71
±
1.76
◦
. In scoliotic girls, the
average Cobb angle was 20.44
±
10.88
◦
; in the postmenarchal scoliotic group, it was
21.89 ±11.04◦, while in the premenarchal scoliotic group, it was 18.43 ±9.98◦.
The mean Cobb angles in postmenarchal and premenarchal scoliotic girls, according
to the laterality and localization of the primary scoliotic curve, are presented in Table 5.
Table 5. The mean Cobb angle in postmenarchal and premenarchal scoliotic girls.
Postmenarchal Premenarchal
Right 21.36 ±10.96 19.94 ±12.29
Lumbar 16.09 ±5.76 15.00 ±9.45
Thoracic 23.38 ±12.16 23.46 ±13.96
Thoracolumbar 20.67 ±10.08 15.25 ±6.88
Left 22.46 ±11.13 17.39 ±7.89
Lumbar 25.25 ±11.92 18.29 ±9.33
Thoracic 17.59 ±9.06 16.77 ±5.46
Thoracolumbar 20.83 ±9.98 17.04 ±7.49
The Cobb angle, as a quantitive measure of curve magnitude, was analyzed in relation
to menarchial status and the laterality of the curve in scoliotic curves. There was no
statistically significant difference in Cobb angle between postmenarchal and premenarchal
girls with a right scoliotic curve (t = 0.930, p= 0.353). On the contrary, a statistically
significant difference was found between postmenarchal and premenarchal girls with a left
scoliotic curve (t = 4.297, p< 0.001). The results are presented in Table 6.
Table 6. Cobb angle in premenarchal and postmenarchal scoliotic girls according to the laterality of
the curve.
Scoliotic Postmenarchal Premenarchal t pValue
Right 21.36 ±10.96 19.94 ±12.29 0.930 0.353 a
Left 22.46 ±11.13 17.39 ±7.89 4.297 <0.001 a
at-test.
Furthermore, there was a statistically significant, but very weak, negative correlation
between the Cobb angle and menarchial status (r =
−
0.159, p< 0.001), while there was no
statistically significant correlation between the Cobb angle and the laterality of the primary
scoliotic curve (r = −0.061, p= 0.176).

J. Clin. Med. 2024,13, 132 7 of 12
In the scoliotic group of girls, a statistically significant relationship was found between
the age at menarche and the laterality of the primary scoliotic curve (
χ2
(1,n = 494) = 10.18,
p< 0.01, phi = 0.148).
In postmenarchal scoliotic girls, the primary right curve was dominant in 54.80%,
while in scoliotic premenarchal girls, the primary left curve was dominant in 60.09%
(p< 0.01). These results are shown below in Tables 7and 8.
Table 7. Distribution of the laterality of primary curves in the scoliotic postmenarchal group.
281 Scoliotic Girls with Menarche
Laterality of Primary Curve
Total
Left Right
Location of
Primary Curve
Lumbar
Count 61 23 84
% Within Location of Primary Curve 72.62% 27.38% 100%
% of Total 21.71% 8.18% 29.89%
Thoracic
Count 13 80 93
% Within Location of Primary Curve 13.98% 86.02% 100%
% of Total 4.63% 28.47% 33.10%
Thoraco
Lumbar
Count 53 51 104
% Within Location of Primary Curve 50.96% 49.04% 100%
% of Total 18.86% 18.15% 37.01%
Total
Count 127 154 281
% Within Location of Primary Curve 45.20% 54.80% 100%
% of Total 45.20% 54.80% 100%
Table 8. Distribution of the laterality of primary curves in the scoliotic premenarchal group.
213 Scoliotic Girls without Menarche
Laterality of Primary Curve
Total
Left Right
Location of
Primary Curve
Lumbar
Count 38 9 47
% Within Location of Primary Curve 80.85% 19.15% 100%
% of Total 17.84% 4.22% 22.06%
Thoracic
Count 14 48 62
% Within Location of Primary Curve 22.58% 77.42% 100%
% of Total 6.57% 22.54% 29.11%
Thoraco
Lumbar
Count 76 28 104
% Within Location of Primary Curve 73.08% 26.92% 100%
% of Total 35.68% 13.15% 48.83%
Total
Count 128 85 213
% Within Location of Primary Curve 60.09% 39.91% 100%
% of Total 60.09% 39.91% 100%
5. Discussion
Menarche in girls is widely considered to be one of the important parameters in the
assessment of the risk of scoliosis progression and one of the influencing factors in the
etiopathogenesis of IS. The age of menarche can indicate the remaining growth potential in
girls [12] and be even more reliable than a Risser sign [18].

J. Clin. Med. 2024,13, 132 8 of 12
However, the Risser sign as a skeletal maturity indicator has been widely used by
professionals in clinical settings. Nonetheless, its accuracy in the assessment of the risk
of scoliosis progression has been undermined lately due to reported limitations, espe-
cially during growth spurts. It has been shown that there is a high risk of mismatch in
patients assessed with Risser staging compared to the Sanders classification [
12
]. For this
reason, Risser staging cannot be used exclusively to assess the risk of progression and
remaining growth.
Regardless of its significance, there are only a few studies that highlight the importance
of menarche in girls.
In 2002, Grivas et al. [
17
] answered the pending question of whether there is a differ-
ence in the age of menarche between scoliotics and non-scoliotics among Mediterranean
girls. They found no statistically significant difference in the age at menarche between
scoliotic and non-scoliotic girls. Furthermore, Mediterranean girls were younger in age
compared to their counterparts in North Europe. These results are in accordance with the
results of our study, which can be explained by similar geographical latitude of the Balkan
countries (Greece 38
◦
16
′
29.82
′′
N, 22
◦
00
′
E, Bosnia and Herzegovina 43.9159
◦
N, 17.6791
◦
E,
Serbia 44.0165
◦
N, 21.0059
◦
E) and supports the findings that the distance from the equator
affects the age of menarche [
19
]. There is also an association between AIS prevalence and
age at menarche in different geographic latitudes [50–60].
The scoliotic girls in northern countries, with a greater distance from the equator,
experience menarche at a later age, which is connected to a higher prevalence of IS in these
countries. This concept seems to be true in southern-globe countries as well [
61
]. This
suggests the possible role of geography in the pathogenesis of IS. Unfortunately, since there
are no official data about scoliosis prevalence in Serbia and Bosnia and Herzegovina, we
were not able to contribute to these findings.
The growth parameters in terms of standing height and weight were also taken
into consideration.
Our results showed a significant difference in height between the groups in terms
of premenarchal girls in the control group being taller than non-scoliotic girls, as well as
postmenarchal girls in the control group being taller than scoliotic girls.
This finding is not in accordance with some previously published results [
62
–
66
] and
can possibly be explained by the sample size of our control group and the age difference
between the groups—that is, the girls in the control group are older (13.63 years of age)
compared to scoliotic (12.57 years of age) and non-scoliotic girls (11.51 years of age).
Goldberg et al. [
18
] found that scoliotic girls are taller when they are younger, but
not in adolescence, while Duval-Beaupère did not find any difference in height between
scoliotics and healthy children [67].
When analyzing weight according to BMI groups, the majority of participants in all
groups had a healthy weight (normal BMI). In the scoliotic group, there were more girls
with a low BMI compared to the non-scoliotic and control groups. However, no significant
difference in weight according to BMI groups was found (p= 0.073). Grivas et al. [
64
]
reported that scoliotic girls from the age of 8 to 12 years are heavier compared to their
non-scoliotic counterparts, but they are thinner after the age of 13, while results from
another study showed no difference in weight between scoliotics and non-scoliotics [
18
,
62
].
A significant difference in the laterality of scoliotic curves in premenarchal and post-
menarchal scoliotic girls was found and is in accordance with previously published re-
sults [
17
]. The menarche-positive scoliotic girls showed predominantly right-sided primary
curves, while the menarche-negative scoliotic girls had mainly left-sided primary curves.
They showed that the primary right curve was dominant in menarche-positive girls in 61%,
while the primary left curve was dominant in menarche-negative girls in 64.3%, which
is similar to our findings (54.80% in menarche-positive girls and 60.09% in menarche-
negative girls).
In menarche-positive girls, the primary right scoliotic curve was dominant in 54.80%,
while in menarche-negative girls, the primary left scoliotic curve was dominant in 60.09%

J. Clin. Med. 2024,13, 132 9 of 12
(p< 0.01), which represents the patterns reflecting developmental theory and scoliosis
produced by Goldberg et al. [
18
] in terms of three developmental gradients: dorso-ventral,
cranio-caudal, and left-right. According to the left-right asymmetry, girls who are preme-
narchal, younger, and less developed present left-sided primary curves, while girls who
are postmenarchal, older and more developed, present right-sided primary curves.
The reason for this finding could also be in the similar underlying mechanism of
progressive IIS since left curves are dominant both in IIS and premenarchal scoliotic girls.
The development of the thorax in progressive IIS is asymmetrical due to a developmental
delay of the upper ribs. leading to the funnel-shaped rib cage that seems to derange
the symmetric forces of ribs acting on the spine. For some reason, in these children, the
thorax does not undergo normal modeling during childhood development, but there is a
change in the upper ribs, which do not grow and elevate symmetrically. This can cause
spinal deformity due to the inability of the upper rib system to act as a spinal rotation-
defending system in the trunk compared to the pelvic rotation-inducing system during
gait, particularly when bipedal gait in infants has been established. This hypothesis may
also be relevant to the Nottingham concept of IS etiology [68].
The limitations of our study include a relatively small number of girls in the control
group (86 participants). In the future, we plan to include in the study more healthy
girls in the control group and also to conduct additional analysis according to the age of
participants in different groups.
6. Conclusions
In Balkan girls from Bosnia and Herzegovina and Serbia, there was no significant
difference in the age of menarche between scoliotic and non-scoliotic girls. However, a
significant difference was found in the laterality of the primary curve in premenarchal and
postmenarchal scoliotic girls. Furthermore, the results showed a significant difference in
height between scoliotic and non-scoliotic girls. Further research is needed to put these
results in the context of scoliogeny.
Author Contributions: Conceptualization: S.P. and T.B.G.; Data curation: S.P.; Statistical analysis,
Literature Investigation: S.P., T.B.G. and N.J.; Project administration: T.B.G., S.P. and N.J.; Writing—
original draft: S.P. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: The study was approved by the Ethical Committee of the
Institute for physical and rehabilitation medicine and orthopedic surgery “Dr Miroslav Zotovic”
(Protocol code: 135-01-4971-2/21, approved on 14 May 2021).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: Data are available on demand.
Acknowledgments: The authors are grateful to Philip Golic for his assistance in the statistical analysis
of the data of this study.
Conflicts of Interest: P.S. and T.B.G. declare no conflict of interest, N.J. is the owner of Scolio Centar
but he has no conflict of interest with this publication.
Abbreviations
AIS adolescent idiopathic scoliosis
AP anteroposterior
BMI body mass index
CDC center for control disease and prevention
IS idiopathic scoliosis
IIS infantile idiopathic scoliosis

J. Clin. Med. 2024,13, 132 10 of 12
LH luteinizing hormone
PA posteroanterior
SRS Scoliosis Research Society
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