European Spine Journal 2019 (Jul); 28 (7): 1565–1571 ~ FULL TEXT
Jeffrey J. Hebert, Charlotte Leboeuf-Yde, Claudia Franz, Arnaud Lardon, Lise Hestbæk, Neil Manson, Niels Wedderkopp
Faculty of Kinesiology,
University of New Brunswick,
NB, E3B 5A3, Canada.
PURPOSE: To examine the prospective associations of pubertal development and linear growth with spinal pain frequency and duration in children.
METHODS: We recruited students from 10 public primary schools. Over 42 months, pubertal development was assessed four times and categorized according to Tanner stages 1-5, and height was measured on seven occasions. Occurrences of spinal pain were reported weekly via text messaging. We constructed variables for spinal pain duration (total weeks with pain) and frequency (number of episodes). Potential associations between pubertal development and growth were examined with generalized estimating equations and reported with incident rate ratios (IRRs). All models were adjusted for potential confounders.
RESULTS: Data from 1021 children (53% female; mean [SD] age = 9.4 [1.4] years), with median participation duration of 39 months, were included. Advancing pubertal development was associated with increased spinal pain duration (IRR [95% CI] = 1.90 [1.45, 2.49] to 5.78 [4.03, 8.29]) and frequency of pain episodes (IRR [95% CI] = 1.32 [1.07, 1.65] to 2.99 [2.24, 3.98]). Similar associations were observed for each 1-cm change in height in 6 months with spinal pain duration (IRR [95% CI] = 1.19 [1.15, 1.23]) and frequency (IRR [95% CI] = 1.14 [1.11, 1.17]). The relations between pubertal development and spinal pain, as well as growth and spinal pain, were largely independent.
CONCLUSIONS: In young people, pubertal development and linear growth are likely to be independent risk factors for the development of spinal pain. Pubertal development demonstrates evidence of dose-response in its relationship with spinal pain. This knowledge may assist healthcare providers with clinical decision-making when caring for pediatric patients. These slides can be retrieved under Electronic Supplementary Material.
KEYWORDS: Back pain; Body height; Growth and development; Puberty; Risk factors
From the Full-Text Article:
Spinal pain is the largest cause of disability worldwide ,
yet its etiology is unknown in most cases. [2-4] Spinal pain
is common in young people [5, 6], often presenting in childhood
and increasing in prevalence with age; 1 in 3 9-year-old
children and half of 15-year-old adolescents experience spinal
pain in the previous month.  The occurrence of spinal
pain in youth is notable as it often tracks into adulthood. 
Little is known about risk factors for the development of
spinal pain in youth. [9, 10] Previous studies have reported
a relationship between spinal pain and pubertal development. [11-13] Puberty is characterized by the rapid developmental
physical and psychological changes occurring during
the transition from childhood and adulthood.  One of
the most striking changes during puberty is linear growth
(change in height), with mean growth during peak height
velocity of 9 cm and 10 cm per year occurring in girls and
boys, respectively.  Linear growth is a potential cause
of spinal pain owing to rapid mechanical loading changes
on the spine. [16-19]
Two recent systematic reviews reported conflicting evidence
for a causal association between pubertal development
and spinal pain. [20, 21] However, several important
limitations of the primary research were identified, including
the lack of longitudinal studies of children at various stages
of pubertal development, and tracking of children over sufficient
time periods to account for variations in growth and
development. Additionally, the measures of spinal pain were
prone to recall bias, and statistical analyses were often suboptimal
for the characteristics of the data. Consequently, the
authors called for additional longitudinal research to investigate
the role of pubertal development and its components.
Therefore, this study examined the prospective associations
of pubertal development and linear growth with spinal
pain frequency and duration in children. We hypothesized
that advancing pubertal development and greater changes
in height would be associated with increased spinal pain
frequency and duration in children.
This prospective cohort study was nested in the Childhood
Health, Activity, and Motor Performance School Study Denmark
(CHAMPS study-DK). The CHAMPS study-DK is
a quasi-experimental trial designed to identify the effects
of physical education on physical activity, cardiovascular
health, and motor performance of primary school students.  All 19 public primary schools in the Svendborg region
of Denmark were invited to participate in the study. Ten
schools elected to participate. Students from six schools
received an intensive physical education program comprising
270 min per week, while students from the remaining
four schools received the usual physical education program
(90 min per week).
In the current study, all participating students were
merged in a common cohort. Linear growth was measured
at baseline, 6, 12, 18, 30, and 42 months. Estimates
of pubertal development were obtained at baseline, 12, 30,
and 42 months. Spinal pain outcomes were measured on a
weekly basis for the duration of the study. Limitations in
human resources and equipment required that participating
children entered the study on a rolling basis, with participating
schools were progressively enrolled over the course
of a school year. Therefore, the median (IQR) participation
time of individual students was 39.0 (34.6–42.2) months.
Additional details about the study have been reported previously
The study sample included all primary school students
enrolled in the first through sixth grades in the participating
schools. Parents provided written consent for all participating
children and children gave verbal consent prior to enrollment.
Ethical approval was provided by the Regional Scientific
Committee of Southern Denmark (ID S20080047),
and the study was registered with the Danish Data Protection
Agency (J.nr. 2008-41-2240).
Anthropometric measures and pubertal development
Measures of height and weight were obtained with children
barefoot and wearing light clothes. Height was measured
to the nearest .5 cm using a portable stadiometer (SECA
214, Seca Corporation, Hanover, MD, USA), and weight was
measured to the nearest .1 kg with a calibrated Tanita BWB-
800S digital scale (Tanita Corporation, Tokyo, Japan). Linear
growth was reported as the change in height occurring
between each of the six time points. Body mass index was
classified as normal, overweight, or obese using age- and
sex-specific norms developed by the International Obesity
Task Force. 
We measured pubertal development with Tanner stages.  As part of a structured interview, Tanner stage was
self-assessed by children with the assistance of explanatory
text and visual representations of pubic hair development in
boys and breast development in girls.  Pubertal development
was reported on a scale from 1 to 5, with higher scores
indicating later pubertal stages. Stage 1 represents prepubertal
status, while stages 2–4 denote increasing levels of
adolescent development, and stage 5 indicates adult development.
Tanner scores 4 and 5 were collapsed into a common
category owing to the low prevalence of these scores early
in the study.
Spinal pain outcomes
Spinal (neck, mid-back, and/or lower back) pain was measured
using a Web-based SMS text messaging system (SMSTrack
ApS, Esbjerg, Denmark) each week for the duration
of the study, except during school holidays. Every Sunday,
parents were sent SMS messages inquiring about the presence
or absence of spinal pain experienced by their child
that week. Surrogate parental reporting was used to address
concerns over the validity of self-reporting by children. [27, 28] All responses were uploaded to an online database; nonsensical
responses resulted in a telephone call to parents
for clarification. This approach is reliable and valid when
compared to information about back pain obtained from
structured clinical interviews. 
From these data, we constructed two spinal pain outcomes:
spinal pain duration and frequency. Pain duration
was characterized by the total weeks of spinal pain reported
during each period (i.e., between each measure of growth
and pubertal development). We estimated spinal pain frequency
by measuring the number of pain episodes occurring
during each study period. Episodes were defined by the
occurrence of spinal pain that was preceded by one or more
pain-free weeks immediately prior to a pain report.
Data were analyzed using Stata v15 software (StataCorp,
College Station, TX, USA). We investigated the longitudinal
associations between (1) pubertal development and (2) linear
growth and each spinal pain outcome using generalized
estimating equation models. Each model included a negative
binomial family, a log link with an exchangeable correlation
matrix, and robust standard errors to account for the clustered
nature of the data.
Exposures for pubertal development comprised the Tanner
stage score at each of the four time points (baseline, 12,
30, and 42 months). Linear growth exposures were represented
by the change in height occurring between each of the
seven time points (baseline, 6, 12, 18, 30, and 42 months).
Spinal pain outcomes were the measures of duration
(weeks with pain) and frequency (episode count) occurring
between exposure measurements. Separate analyses were
conducted for each spinal pain outcome, and results were
reported with incidence rate ratios (IRR) and 95% confidence
intervals. Alpha was .05 for all analyses.
We explored for but identified no significant interactions
between sex and Tanner score or sex and height change and
therefore included no interaction terms in the final models.
Sex and school type (usual or intensive physical education)
were included as covariates in all models. We did not adjust
for age owing to its collinearity with linear growth and
We further explored the associations between linear
growth and spinal pain by modeling parameter estimates and
confidence intervals for 2, 3, 4, and 5 cm changes in height
during a 6-month period. To investigate the independent
associations between pubertal development and spinal pain,
independent of growth, we constructed additional models
controlling for change in height. Conversely, we controlled
for pubertal development to investigate the independent
associations between linear growth and spinal pain.
Descriptive statistics at baseline and follow-up for demographic
and anthropometric variables, as well as pubertal
development, are presented in Table 1. During the study, 885
(52.7%) children reported at least one episode of spinal pain.
Among children who experienced spinal pain, the median
(IQR) total symptom duration was 2 (1–5) weeks. Figures 1
and 2 report the associations between pubertal development
and linear growth, respectively, for each spinal pain outcome
Pubertal development and spinal pain
Advancing pubertal development was associated with spinal
pain duration (Fig. 1a). Relative to Tanner stage 1 development,
children at Tanner stage 2 (IRR [95% CI] = 1.90 [1.45
to 2.49]), stage 3 (IRR [95% CI] = 3.58 [2.55 to 5.03]), and
stage 4/5 (IRR [95% CI] = 5.78 [4.03 to 8.29]) experienced
greater durations of spinal pain.
Similarly, Tanner stages 2 (IRR [95% CI] = 1.32 [1.07
to 1.65]), 3 (IRR [95% CI] = 1.91 [1.50 to 2.44]), and 4/5
(IRR [95% CI] = 2.99 [2.24 to 3.98]) were associated with
a greater frequency of spinal pain episodes (Fig. 1a). Controlling
for linear growth resulted in modest reductions to
the magnitude of associations between pubertal development
and spinal pain duration and frequency, with nearly
all parameter estimates remaining significant (Fig. 1b).
Linear growth and spinal pain
Greater changes in height were associated with increased
spinal pain duration (IRR [95% CI] = 1.19 [1.15 to 1.23])
and frequency of episodes (IRR [95% CI] = 1.14 [1.11 to
1.17]) (Fig. 2a). This translates into a 19% increased risk for
an additional week in which spinal pain was reported and
14% greater risk for an additional pain episode per 1 cm of
linear growth in a 6-month period. Estimated risks associated
with 2-, 3-, 4-, and 5-cm height increases in 6 months
are displayed in Fig. 2a. After controlling for pubertal status,
all associations between growth and spinal pain duration and
frequency remained significant (Fig. 2b).
The current study advances the understanding of spinal
pain in young people. Both pubertal development and linear
growth were associated with spinal pain. Boys and girls with
more advanced pubertal development and those undergoing
greater growth experienced increased spinal pain frequency
and duration. Moreover, these relationships were largely
independent; controlling for growth had little impact on the
relations between pubertal development and spinal pain, and
controlling for pubertal development had little impact on the
relations between linear growth and spinal pain. We found
no evidence for a modifying role of sex in these relationships
but did identify evidence of dose–response between pubertal
development and spinal pain duration and frequency. This
means that pubertal development and linear growth are
potential risk factors for spinal pain in both girls and boys
that they may explain unique aspects of risk.
It should be noted that pubertal development and linear
growth are non-modifiable factors. Nevertheless, their
associations with spinal pain have clinical relevance.
Recognizing the role of puberty and growth may help clinicians
to manage young people with spinal pain. Traditionally,
the occurrence of spinal pain in youth was thought to
be a rare and concerning presentation, owing to its potential
for pathological etiology.  However, current evidence
suggests spinal pain in young people to be a relatively common
and usually benign condition , even in the case of
chronic pain.  Therefore, recognition of the relations
between pubertal development, growth, and spinal pain can
assist clinicians in setting appropriate expectations and provide
reassurance and advice to pediatric patients and parents—
recommendations common to all clinical guidelines
for the management of non-specific back pain. 
It is also important for clinicians to remain vigilant and
identify concerning features of spinal pain in young people
that should raise clinical suspicion for serious pathology.  Pediatric patients presenting with spinal pain and ‘red
flags’ such as recent trauma, fever, weight loss, previous
malignancy, or other findings such as pain during lumbar
extension that may indicate spondylolysis/spondylolisthesis,
warrant additional evaluation and/or referral. 
Information about sedentary and physical activity behavior,
as well as the recognition of psychosocial factors associated
with future disability and potential learned behaviors,
may inform the management of spinal pain in this population. [31, 35]
Our study results are consistent with the two previous
population-based longitudinal studies that identified relationships
between pubertal development and back pain
among Dutch and American adolescents (odds ratios [95%
CI] 1.34 [1.13 to 1.57] to 1.61 [1.30 to 1.99]).  However,
those studies found no significant relationships between
growth (‘growth spurt’) and back pain (odds ratios [95%
CI] 1.04 [.89 to 1.21] to 1.13 [.98 to 1.31]). Compared to
the current study, those participants were approximately
1.5 years older at baseline (mean age = 11.1–11.6 years).
The current investigation addressed several important
limitations of the prior longitudinal studies. While those
studies included only a single measure of pubertal development
and growth at baseline, we obtained serial measures of
pubertal development at four time points and linear growth
at seven time points over the 42-month study period. The
back pain outcomes in previous studies relied on participants’
ability to accurately self-report their frequency of pain
over the preceding 3 months. We limited potential for recall
bias by intensively measuring spinal pain each week and
constructed variables comprising two pain characteristics:
frequency and duration.
In addition, most adolescents in the previous studies
were already in a mid-pubertal developmental stage at
baseline, and therefore it is possible that some effects
of early pubertal development were missed. In contrast,
a large proportion of children in the current study were
prepubertal (51% Tanner stage 1), or in the early stage of
pubertal development (38% Tanner stage 2) at baseline.
Despite the differences in the samples and methodology,
the results with respect to the relationship between
pubertal development and spinal pain were consistent,
thus increasing the confidence in this finding.
The existence of an association between exposure and
outcome does not infer a cause and effect relationship. In
the context of the Bradford Hill criteria , however,
the current study results support several elements of causality
between pubertal development and spinal pain. As
discussed, our results are consistent with previous longitudinal
evidence and thus provide evidence of replication.
Additionally, we identified evidence of dose–response,
with more advanced pubertal development associated
with increased spinal pain duration and frequency.
Temporality is potentially the most challenging causal
criteria to establish in spinal pain research. Spinal pain
is classified as a chronic disease [37, 38], characterized
by recurrent episodes  that occur rarely or frequently.  It is, therefore, difficult to distinguish between the
onset of disease and a new episode of recurrent pain,
and challenging to assemble a true inception cohort of
disease-free individuals. Consequently, most studies of
spinal pain investigate the episodes or patterns of pain
and not the cause of the disease itself.  Most children
in the current study were younger than the expected
age of onset for spinal pain.  Therefore, the temporal
sequencing of exposure and outcome was likely intact for
many participants (i.e., the onset of puberty preceding the
occurrence of spinal pain).
The primary strengths of the current study were the prospective
design, intensive monitoring of spinal pain, long-term
follow-up, and multilevel analyses that accounted for the longitudinal
nature of the data and potential confounding. Study
limitations include measurement issues related to the exposure
and outcome variables. Compared to self-assessment, the
grading of pubertal stages is more accurate when performed
by physicians as part of a clinical examination. However, compared
to prior studies using self-assessment , our measures
of pubertal development were conducted as part of a structured
interview, and participants were provided with standardized
text and illustrations to assist with decision-making, which
may have improved the accuracy of these assessments. Nevertheless,
misclassification resulting from the assessment of
pubertal development represents a potential source of error
in our study.
Although our intensive measures of spinal pain frequency
and duration likely helped to limit recall bias, we did not capture
all aspects of pain. Knowledge of additional pain characteristics
and consequences such as pain intensity, functional
limitations, and the need for healthcare utilization will help
to further the understanding of pubertal development and linear
growth. Finally, there may be other factors that were not
considered in the current study that explain the relationships
between pubertal development, growth, and spinal pain. These
limitations are potential sources of residual confounding in
Future research is needed to investigate the role of other
features of pubertal development and their relations with spinal
pain. Specifically, the examination of psychological and
hormonal characteristics of development may advance the
understanding of the role of puberty in the development of
spinal pain in youth.
The authors gratefully acknowledge the valuable
work of numerous students who assisted with data collection in
the CHAMPS study-DK. We also thank the participating children,
their parents, and teachers in the schools involved in the project. We
are grateful for the cooperation with The Svendborg Project, Sport
Study Sydfyn, and the Municipality of Svendborg. Finally, we wish
to acknowledge members of the CHAMPS study-DK not listed as coauthors
in this paper: E. Jespersen, M. Heidemann, and C.T. Rexen.
The TRYG Foundation, University College Lillebaelt, University
of Southern Denmark, The Nordea Foundation, The IMK foundation,
The Region of Southern Denmark, The Egmont Foundation,
The A.J. Andersen Foundation, The Danish Rheumatism Association,
Østifternes Foundation, Brd. Hartmann’s Foundation, TEAM Denmark,
The Danish Chiropractor Foundation, and The Nordic Institute
of Chiropractic and Clinical Biomechanics. The funding sources played
no role in the design, conduct, or reporting of this study.
Conlict of interest
Prof. Hebert receives salary support from the Canadian
Chiropractic Research Foundation and the New Brunswick Health
Research Foundation. The authors declare no additional conflicts of
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