INTRODUCTION
Coronavirus disease 2019 (COVID-19), caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has imposed a significant socio-economic burden worldwide [1]. As SARS-CoV-2 disseminated globally, healthcare systems faced unprecedented challenges in terms of capacity, resource allocation, and patient care during the COVID-19 pandemic [2]. Prior to the development of vaccines, fundamental preventive measures such as social distancing and the use of face masks served as the primary strategies to curb the spread of SARS-CoV-2 infection [3]. These measures significantly hampered the execution of essential public health activities, including the assessment of prevalence in communities and the provision of primary healthcare services [2].
The school-based scoliosis screening programs were initially conducted by the US Preventive Service Task Force in the early 1960s [4]. The primary objective of these programs was to generate epidemiological data concerning adolescent idiopathic scoliosis (AIS) on a national scale, thereby decreasing the likelihood of delayed diagnosis among affected individuals [4]. Given that it is a progressive condition during the growth period, a delayed diagnosis of AIS is linked to a poor prognosis in management, which may heighten the necessity for surgical intervention [5].
During the COVID-19 pandemic, lockdowns restricted access to healthcare, including the temporary suspension of elective surgeries [6]. Similarly, school-based scoliosis screening programs in South Korea were also disrupted. However, to date, the impact of these school-based scoliosis screening programs in South Korea, particularly in comparing prepandemic and postpandemic conditions, remains undescribed. Therefore, this study aims to evaluate the trends in school-based scoliosis screening programs, with a focus on assessing the impact of the COVID-19 pandemic, including its effects on referral numbers and radiological profiles in patients with AIS.
MATERIALS AND METHODS
1. Study Design and Subject Selection
This study was performed according to the Helsinki Declaration and approved by the Institutional Review Board (IRB) of Korea University Anam Hospital (IRB No. 2024AN0502) where the experiment was performed. A written informed consent was waived because data analyses were performed retrospectively using anonymized data. The study was also conducted in accordance with the current guidelines of STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) [7].
A routine cross-sectional epidemiology study was conducted to collect scoliosis data on schoolchildren residing in Seoul and its metropolitan regions of the Republic of Korea. Schoolchildren aged 10 to 14 years were randomly selected each year with no specific consideration for geographic or economic levels. Taking the COVID-19 pandemic year of 2020 into account, we categorized 3 periods: the prepandemic period (between 2017 and 2019), and the postpandemic period (between 2021 and 2023). A total of 298,666 volunteer individuals residing in Seoul and the metropolitan area participated in the school-based scoliosis screening program, which was divided into the COVID-19 pandemic era: prepandemic group (between 2017 and 2019, n=201,160) and postpandemic group (between 2021 and 2023, n=97,506) (Table 1).
2. School-Based Scoliosis Screening Program
School-based scoliosis screening program was administrated by the scoliosis center of tertiary hospital using a standardized protocol [8]. This program was supervised by a senior orthopedic surgeon with extensive experience in AIS. Trained nurses affiliated with our scoliosis center primarily assessed all volunteered schoolchildren between 10–14 years for AIS screening using visual inspection, the Adam’s forward bending test, and measurement of the angle of axial trunk rotation (ATR) using a scoliometer. Individuals exhibiting an ATR greater than 5° were classified as part of the screened population. Subsequently, these individuals were referred to the scoliosis center for further evaluation, which included capturing standing anteroposterior and lateral radiographs of the entire spine to assess the scoliotic curve. A final diagnosis of AIS was confirmed when the curve magnitude using Cobb angle was more than 10° and further management for the patients with AIS was advised.
3. Data Collection
We included the data on referral volumes, the prevalence rate of AIS, and its trend between the pre- and postpandemic periods. During the screening procedures, we collected data each year on the total number of schoolchildren, the number of males, and the number of females. Regarding the screened schoolchildren (an ATR of 5° or more), we recorded the baseline characteristics including age, sex, height, weight, body mass index (BMI), and menarche age in females. Using the data gathered by standing anteroposterior and lateral radiographs of the whole spine, we included the curve magnitude measured by Cobb angle. Meanwhile, we also analyzed the referral pattern, which is divided into inappropriate referral (Individuals with a Cobb angle<10°), appropriate referral (AIS patients in the screened population, but not required any treatment), and late referral (AIS patients in the screened population and need to treatment such as bracing or surgery). Bracing was applied for patients with a Cobb angle of 25°–40° and a Risser stage of 0–2. Surgery was recommended for those with a Cobb angle exceeding 40° and a Risser stage of 0–2 or for those with a Cobb angle greater than 50° and a Risser stage of >3 [9].
4. Statistical Analysis
Statistical analysis was performed using Python (ver. 3.11.5, Python Software Foundation, USA) with matplotlib (ver. 3.7.2). A normal distribution was confirmed by the Kolmogorov-Smirnov test. After confirming data homogeneity or heteroscedasticity, the Student t-test was used for continuous variables (as presented mean and standard deviation [SD]), and the chi-square test or Fisher exact test (as presented number) was used for categorical variables to compare between the 2 groups, as appropriate. The prevalence rate of AIS is measured as the annual prevalence rate from January to December and presented as the values (percentage, %) and 95% confidence intervals (CIs). To investigate the factors of the screened population according to the change in the COVID-19 pandemic, we used multivariate logistic regression analysis, presenting the odd ratios (ORs) and 95% CIs. Statistical significance was set at p<0.05.
RESULTS
1. Prevalence of AIS Between the Pre- and Postpandemic Era
The prevalence rate of AIS among the total examined population was 3.29% (95% CI, 3.21–3.37) in the prepandemic group, comparing to 3.17% in postpandemic group (95% CI, 3.06–3.28) with no statistical difference (p=0.093) (Fig. 1A). However, the prevalence rate of AIS among the screened population was higher in the postpandemic group (49.35%; 95% CI, 48.12–50.59) than in the prepandemic group (41.47%; 95% CI, 40.71–42.24) (p< 0.001) (Fig. 1B). The proportion of screened schoolchildren was significantly lower in the postpandemic group (6,267 of 97,506 [6.43%]; 95% CI, 6.28%–6.58%) compared to the prepandemic group (15,951 of 201,160; 7.93%; 95% CI, 7.81%–8.05%). For the trend over time, the prevalence of the screened population (screened individuals per total examined population) and AIS population (AIS individuals per total examined population) gradually decreased (Fig. 1C).
2. Baseline Characteristics for Screened Population Between the Pre- and Postpandemic Era
Individuals screened through the school-based scoliosis screening program were referred to our hospital and subsequently evaluated for AIS using radiological examinations. The screened and AIS individuals were then compared by grouping them into pre- and postpandemic categories, respectively. For 2 groups between prepandemic (n=15,951) and postpandemic (n=6,267) era, there was no statistical difference in sex (p=0.101) and height (p=0.607). The age of the screened population was significantly younger in the postpandemic group (11.19 years) than in the prepandemic group (11.45 years) (p<0.001). The BMI (p<0.001) and weight (p<0.001) were significantly lower in the postpandemic group (BMI, 17.96 kg/m2; weight, 42.28 kg) than in the prepandemic group (BMI, 18.44 kg/m2; weight, 43.55 kg). There was same trend in AIS individuals between the 2 groups (Table 2).
3. The Factors of the Screened Population According to the Change in the Pandemic Era
Using the multivariate logistic regression analysis, the scoliosis diagnosis was influenced by the change in the pandemic era: OR=3.66 (95% CI, 3.23–4.12) in total screened population, OR=3.82 (95% CI, 3.30–4.43) in screened female, and OR=2.80 (95% CI, 2.24–3.49) in screened male. Further factors such as age, menarche age BMI, degree of main Cobb angle, also influenced according to the change in the pandemic era (Table 3).
4. Referral Patterns and Self-Perception Between the Pre-and Postpandemic Era
For the screened population, the proportion of appropriate referral was significantly higher in the postpandemic (46.86%) than in the prepandemic group (38.59%) (p<0.001). However, there was no statistical difference in the late referral (2.88%) in the prepandemic and 2.49% in the postpandemic (p=0.112). In self-perception, the proportion of not recognizing AIS was significantly higher in the postpandemic (99.64%), compared to the prepandemic group (91.46%) (p <0.001). For the screened female population, the appropriate referral rate was 43.94% in the prepandemic group and 51.99% in the postpandemic group with statistical differences (p<0.001), respectively. Furthermore, the late referral rate was significantly lower in the postpandemic group (3.49%) than in the prepandemic group (4.11%) (p<0.001). In self-perception, the proportion of not recognizing AIS was significantly higher in the postpandemic (99.74%), compared to the prepandemic group (88.87%) (p<0.001). For the screened male population, there was no statistical difference in the late referral rate (p=0.758) and selfperception (p=0.658) between the 2 groups (Table 4).
5. Menarche Between the Pre- and Postpandemic Era
We investigated the difference in the proportion of females who had experienced menarche and their menarche age before and after the COVID-19 pandemic in the screened female population. Among the screened female population, the proportion of females who had experienced menarche was 44.67% (4,610 of 10,321) in the prepandemic group and 57.87% (2,389 of 4,128) in the postpandemic group, respectively. There was a statistical difference in the menarche for the screened female population between the 2 groups (p<0.001) (Fig. 2A). Among the screened female population who had experienced menarche, the age of menarche was younger in the postpandemic group (mean±SD, 10.75±0.91) than in the prepandemic group (11.06±0.98) (p< 0.001) (Fig. 2B). In females with AIS, the mean menarche age at prepandemic was 11.09±0.95 years (95% CI, 11.02–11.15) in 2017, 11.12±0.96 years (95% CI, 11.04–11.19) in 2018, and 11.18±1.10 (95% CI, 11.09–11.27) in 2019. However, the menarche age was significantly decreased following the onset of pandemic, measuring 10.45±0.65 years (95% CI, 10.32–10.57) in 2021, 10.83±0.91 (95% CI, 10.75–10.91) years in 2022, and 10.76±0.95 years (95% CI, 10.69–10.84) in 2023 (Fig. 2C).
6. Cobb Angle for AIS Population Between the Pre- and Postpandemic Era
For the patients who were diagnosed with AIS after a schoolbased screening program, there was no statistical difference in Cobb angle between the prepandemic (mean±SD, 14.46±5.02) and the postpandemic (14.66±5.81) groups (p=0.078) (Fig. 3A). For the female AIS population, Cobb angle was significantly higher in the postpandemic group (15.33±6.22) than in the prepandemic group (15.03±5.35) (p=0.036) (Fig. 3B). However, no statistical difference in Cobb angle of male AIS population were observed between the prepandemic (12.66±3.70) and postpandemic group (12.82±3.46) (p=0.293) (Fig. 3C).
DISCUSSION
The COVID-19 lockdown, instituted to mitigate the transmission of SARS-CoV-2, has profoundly affected various aspects of the healthcare system [10]. In particular, the screening of asymptomatic idiopathic scoliosis has been delayed, leading to potential negative consequences [11,12]. Delays in primary consultations may hinder the achievement of the main objectives of school-based screening programs, which aim for early detection and appropriate intervention [4]. Despite acknowledging these issues, there is a scarcity of studies that comprehensively investigated the impact of the COVID-19 pandemic on schoolbased screening programs. Data from our school-based screening program in South Korea indicated that the prevalence of AIS remained relatively stable between the prepandemic and postpandemic periods. However, the detection rate of AIS among the screened population (with ATR ≥5°) showed a significant increase with a 1.19 (1.09–1.17) of RR. Furthermore, the mean Cobb angle in the screened population with AIS significantly increased after the COVID-19 pandemic, particularly among females. Our findings suggested that delayed screening during 3 years of the postpandemic period, caused by the COVID-19 pandemic, resulted in the observation of larger curvatures in females at the time of detection. Therefore, following the pandemic of infectious diseases such as COVID-19, the screening strategy of AIS should be restructured during the postpandemic period.
Dermott et al. [11] investigated the impact of COVID-19 on AIS referrals, which showed decreased referral volumes between 2019 and 2020 in the single institution retrospective cohort study. Like this study, our study shares common findings in a marked decrease in referral volume in 2020. However, this trend has gradually returned to prepandemic levels as our screening program progressed into 2021 and 2022. Meanwhile, the study by Dermott et al. [11] observed no statistical difference in Cobb angle between 2019 and 2020. In contrast, our study demonstrated a significant difference in Cobb angle in females, which is believed to be attributable to the difference in the rate of menarche experience [11]. Postpandemic, not only the COVID-19 infection itself but also the effects of the pandemic and vaccination influenced menarche, leading to accelerated growth and larger measurements of the scoliosis curve [13,14]. Pereira-Duarte et al. [12] in Canada reported that patients with AIS, after the first COVID-19 wave (September 2020), had a significantly larger Cobb angle, and the delay in consultation contributed to missing the potential window for bracing or vertebral body tethering. However, in our large population-based comparative study between 2017 and 2023, no significant difference in the late referral rate was observed. This result is not solely attributable to the effects of COVID-19 on changes in baseline characteristics. Rather, the prevalence of AIS itself did not change due to the pandemic, and the increase in the rate of AIS detected in the screened population contributed to these findings. Importantly, the proportion of screened schoolchildren was significantly lower in the postpandemic group compared to the prepandemic group in our cohort. Fong et al. [15] emphasized that the effectiveness of a school-based screening program relies heavily on the clinical expertise of healthcare professionals and their consistent involvement, as well as the establishment of a well-integrated system. The differences observed in our study may be attributed to these factors. Specifically, there was a 1-year hiatus in 2020 due to the COVID-19 pandemic, during which the integrated screening system was temporarily suspended as a result of nationwide lockdowns. The program was gradually reinstated as pandemicrelated restrictions eased. Therefore, understanding the various effects of COVID-19 and developing future screening strategies accordingly is crucial to achieving the objectives of the existing school-based scoliosis screening programs.
Interestingly, the mean weight, and BMI of the screened population significantly decreased in the postpandemic period compared to the prepandemic period. Recent evidence suggested that the COVID-19 pandemic increased weight in adolescent due to limited physical activities and worsened dietary habits [16,17]. However, these trends were reversed after the main COVID-19 pandemic and returned to the prepandemic period [16]. In the midst of the pre- and post-COVID-19 pandemic, the screened population of this study were significantly decreased in 2023. According to the 2-year cross-sectional study by Jeon and Kim [18], they found that being underweight closely related with the incidence of idiopathic scoliosis. Furthermore, studies also emphasized that AIS patients who are underweight are relatively welldetected in school-based scoliosis screening programs [19,20]. It is possible that this underweight population was better screened in the school-based program, which resumed in the early post-COVID-19 pandemic period in our study. Alongside this, there may be cases in the early postpandemic phase that were missed during screening. Thus, it will be important to employ a variety of screening tools in the future to enhance detection rates in the school-based scoliosis program.
After the COVID-19 pandemic, the most notable characteristics of the screened population are a younger chronological age, a higher percentage of females who had experienced menarche, and a younger age at menarche. Consequently, the Cobb angle in females showed a significant increase as a result of our study. In the post-COVID-19 pandemic, suspected precocious puberty was increasingly referred to the department of pediatric endocrinology [14,21]. The trend for early experience of menarche and rapid progression of puberty has been focused on the postpandemic period, which were published in various observational studies [14,21-23]. Puberty is influenced by a complex interplay of hormonal, physical, and psychological changes [14]. Several studies have indicated changes in gonadotropin-releasing hormone by SARS-CoV-2 infection, although no definitive pathophysiological mechanisms have been established [24]. Furthermore, the COVID-19 lockdown and vaccination have been associated with increased stress, anxiety, and depression, all of which negatively impacted adolescent mental health [25,26]. These physical and psychological factors may have also contributed to the earlier onset of menarche [14]. Since scoliotic curve progression is closely related to the degree of maturity, our study observed that the screened population was younger in chronological age and that AIS was detected with a higher magnitude of the Cobb angle curve in females.
For the assessment on the self-perception of scoliosis, the percentage of patients, or their parents, who independently perceived themselves as having scoliosis has significantly decreased in the post-COVID-19 pandemic period. Although the screened population in the postpandemic period showed a younger chronological age, earlier onset of menarche, and larger scoliotic curves in females, the rate of self-perception of scoliosis significantly decreased, especially in females. We thought the change in selfperception was due to the impact of the COVID-19 pandemic, which imposed restrictions on various activities and led to a reduction in scoliosis screening volumes [11,12,27]. Ultimately, the COVID-19 pandemic negatively impacted the school-based scoliosis screening program in South Korea. Given the importance of providing timely and appropriate treatment for patients with asymptomatic scoliosis, our findings highlight the need for an expansion and reorganization of the school-based scoliosis screening program in the postpandemic period.
The COVID-19 pandemic did not affect the overall prevalence of AIS; however, the increased rate of AIS in the screened population suggests that it influenced referral patterns and diagnostic timing. This highlights the need to clinically restructure the school-based scoliosis screening program, incorporating various methods, such as telemedicine, and improving awareness of self-perception in the postpandemic era [28]. Telemedicine, proven useful during the pandemic for education and consultation, has the potential to aid in visual inspections to identify shoulder asymmetry and rotation in forward bending, which can prompt referrals to scoliosis centers [29-31]. Additionally, advancements in artificial intelligence have introduced tools capable of estimating scoliosis through upright back image [32]. Although these tools are not yet highly accurate, further development could significantly enhance the school-based scoliosis screening program in the future [32-35].
There are several limitations to this study. First, as a retrospective analysis with prospective data collection, there is potential for bias due to the nature of the study design. However, we collected a relatively large sample size both before and after the COVID-19 pandemic, which strengthens our findings. Second, our study was based on a school-based screening program, which did not capture incidence rates and the prior history of COVID-19 infection. Future studies utilizing the International Classification of Diseases 10th Revision codes will be necessary to clarify the association between the COVID-19 pandemic and the incidence of AIS. Meanwhile, comparing referral patterns based on treatment type (bracing or surgery) may provide valuable insights. However, in our study, the proportion of AIS patients requiring surgical intervention was very low, ranging from 0.08% to 0.52%. Therefore, further study needs to be required to further explore the insight of school-based screening program with respect to referral patterns. Third, as an observational study, our research does not establish a causal relationship between the COVID-19 pandemic and school-based screening programs. Additionally, various factors such as behavioral and psychological influences interacted with the baseline characteristics of our study population but were not accounted for in this study. Lastly, our study did not include a longitudinal analysis to assess the prognosis of AIS patients after screening. Therefore, future longitudinal studies that control for covariates will be required to further strengthen our results.
CONCLUSION
Our large-scale population-based study demonstrates that the COVID-19 pandemic negatively impacted the school-based scoliosis screening program. While the prevalence of AIS remained consistent before and after the pandemic, the detection rate in the screened population significantly increased, with younger chronological age, earlier onset of menarche, and a higher Cobb angle curve observed. Given the critical importance of timely and appropriate treatment for asymptomatic scoliosis, these findings emphasize the need for expanding and reorganizing the school-based scoliosis screening program in the postpandemic period.
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