SPINE Volume 38, Number 19, pp 1690-1694 ©2013, Lippincott Williams & Wilkins
DIAGNOSTICS
Scheuermann Disease Evaluation of Radiological Criteria and Population Prevalence Ater A. Makurthou, MSc,*t+ Ling Oei, MD, MSc, MA,**§ Salih El Saddy, MSc,*t+ Stephan j . Breda, MSc,*t+ Martha C. Castaño-Betancourt, MSc,*t§ Albert Hofman, MD, PhD,+ Joyce B. j . van Meurs, PhD,*t§ André C. Uitterlinden, PhD,*+§ Fernando Rivadeneira, MD, PhD,**§ and Edwin H. G. Oei, MD, PhDt
Study Design. Observational population-based study. Objective. To determine the prevalence of radiographical Scheuermann disease in a Dutch population and evaluate the consistency of diagnostic criteria.
from 45° to 40° or 35° increased the number of cases marginally, corresponding to prevalence estimates not significantly different
Summary of Background Data. Scheuermann disease is a form of osteochondrosis characterized by increased posterior rounding of the thoracic spine with structural vertebral deformity. Different expert opinion-based radiological criteria exist, yet these have not been validated. The prevalence in the general population reported ranged from 1 % to 10%.
Conclusion. Our results revealed a prevalence of 4.0% of radiographical Scheuermann disease in Dutch individuals aged 45 years and older. Although there is no current "gold standard" for the radiographical definition, standardized scoring of independent features resulted in substantial interobserver agreement, and different applications of diagnostic criteria did not significantly alter the classification.
Methods. Lateral spine radiographs of 2753 Rotterdam Study participants (aged 45-89 yr) were assessed for Scheuermann disease using S0rensen and Sachs' radiographical criteria in 2 phases. Cohen K statistics were calculated for interrater agreement. Prevalence estimates were calculated and sex differences were tested with Pearson x^ test. We evaluated whether varying the kyphosis angle criterion would change the prevalence estimate. Results. A total of 677 (24.6%) individuals had endplate irregularities and 140 (5.1%) individuals had vertebral wedging. Abnormalities were significantly more prevalent among males (P < 0.05). The interrater agreement K statistics were 78.8% for vertebral wedging and 79.4% for endplate irregularity. A total of 127 individuals had both criteria, of which 111 had a kyphosis angle greater than 45°, resulting in a prevalence of 4.0% (95% confidence interval [CI]: 3.3%-4.7%). The disease prevalence was 4.5% ¡n males versus 3.6% in females, yet this difference was not statistically significant (P = 0.23). Adjustment of the kyphosis angle criterion
From the Departments of *lnternal Medicine; tRadiology, and ^Epidemiology, Erasmus Medical Center, Rotterdam, the Netherlands; and §Netherlands Cenomics Initiative-sponsored Netherlands Consortium for Healthy Aging, The Hague, the Netherlands. Acknowledgment date: March 29, 2013. First revision date: April 25, 2013. Acceptance date: May 25, 2013. The manuscript submitted does not contain information ahout medical device(s)/drug(s). This unfunded project is embedded within the Rotterdam Study, which is funded by the Dutch government. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Edwin H. G. Oei, MD, PhD, Department of Radiology, Erasmus Medical Center, 's Gravendijkwal 230, 3015 CE Rotterdam, the Netherlands; E-mail: [email protected] DOI: 10.1097/BRS.0b013e31829ee8b7 1690
www.spinejournal.com
from the estimates using original criteria (4.2% [95% CI: 3.3%4.7%[ and 4.4% [95% CI: 3.6%-5.2%]).
Key words: Scheuermann disease, kyphosis, epidemiology, diagnosis, radiographical criteria, prevalence, thoracic spine, endplate irregularities, vertebral wedging, Rotterdam Study, osteochondrosis, Dutch, the Netherlands, lateral spine radiographs, population-based.
Level of Evidence: 3 Spine 2013;38:1690-1694
S
cheuermann disease is a form of osteochondrosis of the spine and is characterized by increased posterior rounding of the thoracic spine in association with structural deformity of the vertebral elements.^ Previous prevalence estimates of Scheuermann disease vary widely, ranging between 0.4% and 10%.'"'^ Scheuermann disease is diagnosed on the basis of radiographical criteria, yet, there is no diagnostic "gold standard." The criteria by Sorensen and Sachs are the most commonly applied^-* but different radiographical diagnostic criteria exist.' These different radiographical criteria include endplate irregularity, thoracic kyphosis greater than 35°'-' or 45°,'" and at least 1^'' or 3'" adjacent wedged vertebral bodies each of 5° or more in magnitude'" (Figure 1). Also, Schmorl nodes are thought to be a common but not obligate manifestation of Scheuermann disease.'^ When different criteria are used inconsistently, the estimates of disease prevalence may differ widely and seem unreliable. Therefore, the purpose of our study was to determine the prevalence of Scheuermann disease and its radiographical criteria in the Dutch population across sexes and to evaluate the consistency of the diagnostic criteria. September 2013
Spine
DIAGNOSTICS
MATERIALS AND METHODS The Rotterdam Study is a prospective population-based cohort study that started in 1990 in Ommoord, a suburb of Rotterdam, the Netherlands. The main objective of the Rotterdam Study is to investigate the prevalence, incidence, and risk factors for chronic disease and disability in elderly individuals aged 55 years and older. After approximately 1 decade, the Rotterdam Study was expanded with a younger cohort (RS-III), including participants aged 45 years and older living in the same suburb. A detailed description of the Rotterdam Study has been reported previously." The Medical Ethics Committee of the Frasmus University Medical Center has approved the Rotterdam Study. A trained research technician obtained standing lateral radiographs of the thoracolumbar spine of individuals visiting the research center. All radiographs were acquired digitally according to a standardized protocol, with a focus to detector distance of 120 cm (Fujifilm Medical Systems, Stamford, CT). A DICOM viewer was used for radiographical assessment. To diagnose Scheuermann disease, the radiographical criteria of Sorensen" and Sachs et aP were applied in 2 phases (Table 1). A.A.M. and S.S., research assistants trained by a musculoskeletal radiologist (E.H.G.O.), scored the radiographs. To determine the level of agreement, a randomly selected subset (N = 154) was assessed by both readers. The musculoskeletal radiologist (E.H.CO.) acted as a third reader
Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
TABLE I^^Bíographícal
Assessment of
^^H
Phases
Data Type
1
Qualitative
Vertebral body endplate irregularities
One or more vertebral levels
Qualitative
Vertebral wedging
At least 3 adjacent vertebral levels 5° or more per vertebra
Kyphosis angle
Between thoracic levels Th5 and Thl2 45°ormore in total
2
Quantitative
Criteria
Specifications
by assessing inconclusive radiographs to resolve discrepancies. In the first phase, we triaged potential cases from normal radiographs on the basis of 2 criteria: vertebral wedging at a minimum of 3 levels and presence of vertebral body endplate irregularities. Because Schmorl nodes are actually focal indentations of the vertebral endplate,'^ we scored these as endplate irregularities. We defined potential cases as those with consecutive vertebral wedging in combination with endplate irregularity. In the second phase, we reevaluated all these potential cases by measuring the thoracic kyphosis angle between thoracic vertebral levels Th5 and Thl2. We defined a kyphosis angle of 45° or more to diagnose the Scheuermann disease cases.'" In addition, we evaluated the impact of varying the kyphosis angle criterion on prevalence estimation of Scheuermann disease by adjusting from 45° to 40° or 35°. Finally, we reassessed the levels of vertebral wedging and endplate irregularities in more detail. All radiographs fulfilling these criteria were reassessed by the other reader (A.A.M. or S.S.) to verify the diagnosis of Scheuermann disease. Statistical Methods Frequencies of each of the independent radiological diagnostic criteria were assessed per vertebral and per patient levels, and the prevalence of Scheuermann disease was determined in the study population. A random subset of radiographs was scored by both readers (A.A.M. and S.S.), and Cohen K statistics for interrater agreement were calculated for this sample and graded according to Landis and Koch.''' Sex-specific and sex-combined prevalence estimates were calculated and sex differences were tested with Pearson x^ test. Analyses were performed with SPSS statistics software version 20 (IBM, Armonk, NY).
Figure 1. Lateral radiograph showing Scheuermann disease with marked endplate irregularities and mild anterior wedging of multiple midthoracic vertebrae, resulting in increased thoracic kyphosis. Spine
RESULTS Lateral spine radiographs were available and assessed for 2753 participants (mean age, 57 yr; range, 45-89 yr). After triage, we identified 677 (24.6%) cases with endplate irregularities and 140 (5.1%) cases with vertebral wedging (Table 2). The Cohen K statistics were 78.8% for vertebral wedging and 79.4% for endplate irregularity. We investigated whether the www.spinejournal.com
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DIAGNOSTICS
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Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
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occurrence of endplate irregularities and vertebral wedging differed between sexes. We found a higher prevalence of endplate irregularities among males than in females, but this difference was borderline statistically significant (P = 0.06). Also, we observed a significantly higher prevalence of vertebral wedging among males than among females (P = 0.02). In addition, most endplate irregularities occurred at thoracic and vertebral level 8 (Figure 2), and vertebral wedging was most common at the midthoracic region (Figure 3). Subsequently, 127 participants were classified as having both endplate irregularities and vertebral wedging (Table 2). The frequency of having both endplate irregularity and vertebral wedging was significantly higher in males than in females (5.6% vs. 3.9%; ? = 0.04).
Figure 2. Number of endplate irregu-
'-larities observed per thoracic (Th) and lumbar (L) vertebral level.
Next, we measured the kyphosis angle in the 127 potential cases of Scheuermann diseases (Table 3). A kyphosis angle of 45° or more was found in 111 cases (87% of the participants prioritized by the triage procedure), resulting in a definitive diagnosis of Scheuermann disease. The prevalence of Scheuermann disease was estimated to be 4.0% (95% confidence interval [CI]: 3.3%-4.7%), with no significant difference across sexes (? = 0.23) (Table 2). In addition, we evaluated whether a modification of the diagnostic criteria would infiuence the prevalence estimate of Scheuermann disease. By adjusting the kyphosis angle criterion from 45° to 40°, we found that this would increase the total number of Scheuermann disease cases to 115, resulting in no essential change in prevalence of 4.2% (95% CI: 3 . 3 % 4.7%). Similarly, no major difference was observed by using a kyphosis angle cutoff of 35°, in which the prevalence was 4.4% (95% CI: 3.6%-5.2%) after just adding 6 additional cases.
DISCUSSION
10
Upper thoracic Th4-Th6
Midthoracic Th7-Th9
Lovt/er thoracic ThlO-Thl2
Vertebral level interval Figure 3. Distribution of vertebral wedging of 3 adjacent vertebrae of 5° or more per thoracic (Th) region. 1692
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In this first epidemiological study in the Dutch population, we found a prevalence for radiographical Scheuermann disease of 4.0%, applying the criteria defined by S0rensen and Sachs. Although no "gold standard" for the radiographical definition exists, standardized scoring of independent features resulted in substantial interobserver agreement, and different definitions of diagnostic criteria did not alter disease classification. The population-based study design with radiographs of the full thoracolumbar spine and a meticulous scoring system enabled us to identify radiographical Scheuermann disease cases without clinical complaints, which would have been missed by a clinical-based study. We assessed a large number of radiographs specifically for Scheuermann disease and recorded each of the diagnostic criteria separately and in detail with high interobserver agreement. Usually, Scheuermann kyphosis becomes clinically overt during growth spurt and ceases to progress once axial skeletal maturity is reached.""^ Therefore, aU participants with Scheuermann disease should have displayed radiographical features at the time of our examination. Nevertheless, our September 2013
Spine
DIAGNOSTICS
Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
TABLE 2 HEquencies
of the Radiological " ^ H i ^^agnostic Criteria of Scheuermann 1 Females (N = 1566)
Total (N = 2753)
Endplate irregularity
313 (26.4%)
364 (23.2%)
677 (24.6%)
0.06
Vertebral wedging
74 (6.2%)
66 (4.2%)
140 (5.1%)
0.02
Endplate irregularity -Ivertebral wedging
66 (5.6%)
61 (3.9%)
127 (4.6%)
0.04
Scheuermann disease
54 (4.5%)
57 (3.6%)
m (4.0%)
1quencies Per Kyphotic
Angle ^ 1 for P o t e n M ^ ^ ^ ^ H
Kyphotic Angle Interval
Males (N = 1187)
Variable
TABLE 3.
P*
0.23
•P value X' males versus females.
study in older individuals could have included some falsepositive cases because of the coexistence of degenerative disease. However, the most typical features of spine degeneration are disc disease, osteophytosis, and facet joint osteoarthritis,'^ which are not diagnostic criteria for Scheuermann disease. Furthermore, these degenerative changes occur much less commonly in the thoracic spine than in the cervical and lumbar regions.'* As mortality rate is unchanged in Scheuermann disease,*" our prevalence estimates may also be extrapolated to younger populations. Different expert opinion-based criteria have been used for diagnosing Scheuermann disease and these criteria remain controversial.** Therefore, we evaluated the effect of modifying the kyphosis angle criterion and found that only few more would be classified as Scheuermann cases without affecting the prevalence. Composite standardized assessment of independent criteria seems to result in sufficient diagnostic consistency. Our prevalence of 4.0% is within the previously reported range (0.4%-10%)'^'^ and highlights that radiographical Scheuermann disease is not infrequent in the general population. Each of the diagnostic criteria, that is, endplate irregularities and vertebral wedging, occurred most commonly at the midthoracic region. The frequency of both endplate irregularities and vertebral wedging was higher in males than in females; however, the sex difference in the prevalence was not statistically significant, which could be due to the limited study power with a relatively low number of cases. Some publications have reported prevalences of Scheuermann disease to be closely similar between the sexes,""^' whereas others have observed Scheuermann disease to be more prevalent among males than in females.'^'-^ An accurate and precise diagnosis of Scheuermann disease is important to provide proper treatment and hopefully to avert disability. Although coexistence with osteoporotic vertebral fractures can occur, the disorders should be distinguished as disease treatment is very different.*-"•'''•-' Radiographical findings should be correlated with clinical symptoms that typically started at adolescent age,^* nonetheless, taking into Spine
Frequency
%
20-25
2
1.6
25-30
1
0.8
30-35
3
2.4
35-40
6
4.7
40-45
4
3.1
45-50
27
21.3
50-55
30
23.6
55-60
31
24.4
60-65
12
9.4
65-70
3
2.4
70-75
4
3.1
75-80
2
1.6
80-85
2
1.6
127
100.0
Total
account recall bias. Some patients with adult Scheuermann kyphosis are only moderately affected by the disease'^"'-^''; future research might elucidate why some individuals have more complaints than others. In addition, the condition is generally not well known among clinical practitioners, which may cause diagnosis of Scheuermann disease to be missed or delayed. The fairly high disease prevalence underscores that Scheuermann disease should not be overlooked.
CONCLUSION In sum, our study revealed a prevalence of 4.0% of Scheuermann disease in the Dutch population. Standardized scoring of independent features resulted in substantial interobserver agreement, and different applications of diagnostic criteria did not alter disease classification.
>^ Key Points Q The prevalence of radiographical Scheuermann disease was 4.0% in a Dutch population sample aged 45 years and older. •
Vertebral wedging and endplate irregularities are significantly more prevalent among males.
•
Standardized scoring of independent Scheuermann disease radiographical features shows substantial interobserver agreement.
•
Current diagnostic criteria for Scheuermann disease seem sufficient, as different applications on a population level did not significantly alter disease classification. www.spinejournal.com
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DiAGNOSTICS
Acknowledgments The authors are grateful to the study participants, the staff from the Rotterdam Study (particularly Lydia Buist and Hannie van den Boogert for acquisition of the radiographs), and the participating general practitioners and pharmacists. The authors thank René Vermeren, Nano Suwarno, and Mart Rentmeester for their technical support. The Medical Ethics Committee of the Erasmus University Medical Center has approved the Rotterdam Study. The Rotterdam Study is funded by Erasmus Medical Center and Erasmus University, Rotterdam, Netherlands Organization for the Health Research and Development (ZonMw), the Research Institute for Diseases in the Elderly (RIDE), the Ministry of Education, Culture and Science, the Ministry for Health, Welfare and Sports, the European Commission (DG XII), The Netherlands Genomics Initiative (NGI), Netherlands Consortium of Healthy Ageing (NCHA), and the Municipality of Rotterdam. References 1. Hart ES, Merlin C, Harisiades J, et al. Scheuermann's thoracic kyphosis in the adolescent patient. Orthop Nurs 2010;29:365-71; quiz 72-3. 2. Damborg E, Engell V, Andersen M, et al. Prevalence, concordance, and heritability of Scheuermann kyphosis based on a study of twins. / Bone ]oint Surg Am 2006;88:2133-6. 3. Heithoff KB, Gundry CR, Burton CV, et al. Juvenile discogenic disease. Spine (Phila Pa 1976) 1994;19:335-40. 4. Nissinen M. Spinal posture during pubertal growth. Acta Paediatr 1995;84:308-12. 5. Papagelopoulos PJ, Mavrogenis AE, Savvidou OD, et al. Current concepts in Scheuermann's kyphosis. Orthopedics 2008;31:52-8; quiz 9-60. 6. Puisto V, Rissanen H, Heliovaara M, et al. Mortality in the presence of a vertebral fracture, scoliosis, or Scheuermann's disease in the thoracic spine. Ann Epidemiol 2008;18:595-601. 7. Serensen KH. Seheuermann's ]uvenile Kyphosis: Clinical Appearanees. Radiography, Aetiology and Prognosised. Copenhagen, Denmark: Munksgaard; 1964. 8. Sachs B, Bradford D, Winter R, et al. Scheuermann kyphosis. Eollow-up of Milwaukee-brace treatment. / Bone ]oint Surg Am ' 1987;69:50-7. 9. Wenger DR, Frick SL. Scheuermann kyphosis. Spine (Phila Pa 1976) 1999;24:2630-9. 10. Bradford DS, Moe JH, Montalvo EJ, et al. Scheuermann's kyphosis and roundback deformity. Results of Milwaukee brace treatment. / Bone]oint Surg Am 1974;56:740-58.
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Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
11. Masharawi Y, Rothschild B, Peled N, et al. A simple radiological method for recognizing osteoporotic thoracic vertebral compression fractures and distinguishing them from Scheuermann disease. Spine (Phila Pa 1976) 2009;34:1995-9. 12. Pfirrmann CW, Resnick D. Schmorl nodes of the thoracic and lumbar spine: radiographie-pathologie study of prevalence, characterization, and correlation with degenerative changes of 1,650 spinal levels in 100 cadavers. Radiology 2001;219:368-74. 13. Hofman A, van Duijn CM, Eranco OH, et al. The Rotterdam Study: 2012 objectives and design update. Eur ] Epidemiol 2011;26: 657-86. 14. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics ]977;33:159-74. 15. Eotiadis E, Kenanidis E, Samoladas E, et al. Scheuermann's disease: focus on weight and height role. Eur Spine ] 2008;17: 673-8. 16. Lemire JJ, Mierau DR, Crawford CM, et al. Scheuermann's juvenile jcyphosis. / Manipulative Physiol Ther 1996;19: 195-201. 17. Peterson CK, Bolton JE, Wood AR. A cross-sectional study correlating lumbar spine degeneration with disability and pain. Spine (Phila Pa 1976) 2000;25:218-23. 18. Niemelainen R, Battie MC, Gill K, et al. The prevalence and characteristics of thoracic magnetic resonance imaging findings in men. Spine (Phila Pa 1976) 2008;33:2552-9. 19. Lowe TG, Line BG. Evidence based medicine: analysis of Scheuermann kyphosis. Spine (Phila Pa 1976) 2007;32:S115-9. 20. Murray PM, Weinstein SL, Spratt KE. The natural history and longterm follow-up of Scheuermann kyphosis. / Bone ]oint Surg Am 1993;75:236-48. 21. Rachbauer E, Sterzinger W, Eibl G. Radiographic abnormalities in the thoracolumbar spine of young elite skiers. Am ] Sports Med 2001;29:446-9. 22. Eisk JW, Baigent ML, Hill PD. Scheuermann's disease. Clinical and radiological survey of 17 and 18 year olds. Am ] Phys Med 1984;63:18-30. 23. Ristolainen L, Kettunen JA, Heliovaara M, et al. Untreated Scheuermann's disease: a 37-year follow-up study. Eur Spine ] 2012;21:819-24. 24. Jiang G, Eastell R, Barrington NA, et al. Comparison of methods for the visual identification of prevalent vertebral fracture in osteoporosis. Osteoporos lnt 2004;15:887-96. 25. Oei L, Rivadeneira E, Ly E, et al. Review of radiological scoring methods of osteoporotic vertebral fractures for clinical and research settings. Eur Radiol 2013;23:476-86. 26. Summers BN, Singh JP, Manns RA. The radiological reporting of lumbar Scheuermann's disease: an unnecessary source of confusion amongst clinicians and patients. Br] Radiol 2008;81:383-5. 27. Wood KB, Melikian R, Villamil E Adult Scheuermann kyphosis: evaluation, management, and new developments. / Am Acad Orthop Surg20\2;20:lU-2\.
September 2013
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DIAGNOSTICS
Scheuermann Disease Evaluation of Radiological Criteria and Population Prevalence Ater A. Makurthou, MSc,*t+ Ling Oei, MD, MSc, MA,**§ Salih El Saddy, MSc,*t+ Stephan j . Breda, MSc,*t+ Martha C. Castaño-Betancourt, MSc,*t§ Albert Hofman, MD, PhD,+ Joyce B. j . van Meurs, PhD,*t§ André C. Uitterlinden, PhD,*+§ Fernando Rivadeneira, MD, PhD,**§ and Edwin H. G. Oei, MD, PhDt
Study Design. Observational population-based study. Objective. To determine the prevalence of radiographical Scheuermann disease in a Dutch population and evaluate the consistency of diagnostic criteria.
from 45° to 40° or 35° increased the number of cases marginally, corresponding to prevalence estimates not significantly different
Summary of Background Data. Scheuermann disease is a form of osteochondrosis characterized by increased posterior rounding of the thoracic spine with structural vertebral deformity. Different expert opinion-based radiological criteria exist, yet these have not been validated. The prevalence in the general population reported ranged from 1 % to 10%.
Conclusion. Our results revealed a prevalence of 4.0% of radiographical Scheuermann disease in Dutch individuals aged 45 years and older. Although there is no current "gold standard" for the radiographical definition, standardized scoring of independent features resulted in substantial interobserver agreement, and different applications of diagnostic criteria did not significantly alter the classification.
Methods. Lateral spine radiographs of 2753 Rotterdam Study participants (aged 45-89 yr) were assessed for Scheuermann disease using S0rensen and Sachs' radiographical criteria in 2 phases. Cohen K statistics were calculated for interrater agreement. Prevalence estimates were calculated and sex differences were tested with Pearson x^ test. We evaluated whether varying the kyphosis angle criterion would change the prevalence estimate. Results. A total of 677 (24.6%) individuals had endplate irregularities and 140 (5.1%) individuals had vertebral wedging. Abnormalities were significantly more prevalent among males (P < 0.05). The interrater agreement K statistics were 78.8% for vertebral wedging and 79.4% for endplate irregularity. A total of 127 individuals had both criteria, of which 111 had a kyphosis angle greater than 45°, resulting in a prevalence of 4.0% (95% confidence interval [CI]: 3.3%-4.7%). The disease prevalence was 4.5% ¡n males versus 3.6% in females, yet this difference was not statistically significant (P = 0.23). Adjustment of the kyphosis angle criterion
From the Departments of *lnternal Medicine; tRadiology, and ^Epidemiology, Erasmus Medical Center, Rotterdam, the Netherlands; and §Netherlands Cenomics Initiative-sponsored Netherlands Consortium for Healthy Aging, The Hague, the Netherlands. Acknowledgment date: March 29, 2013. First revision date: April 25, 2013. Acceptance date: May 25, 2013. The manuscript submitted does not contain information ahout medical device(s)/drug(s). This unfunded project is embedded within the Rotterdam Study, which is funded by the Dutch government. No relevant financial activities outside the submitted work. Address correspondence and reprint requests to Edwin H. G. Oei, MD, PhD, Department of Radiology, Erasmus Medical Center, 's Gravendijkwal 230, 3015 CE Rotterdam, the Netherlands; E-mail: [email protected] DOI: 10.1097/BRS.0b013e31829ee8b7 1690
www.spinejournal.com
from the estimates using original criteria (4.2% [95% CI: 3.3%4.7%[ and 4.4% [95% CI: 3.6%-5.2%]).
Key words: Scheuermann disease, kyphosis, epidemiology, diagnosis, radiographical criteria, prevalence, thoracic spine, endplate irregularities, vertebral wedging, Rotterdam Study, osteochondrosis, Dutch, the Netherlands, lateral spine radiographs, population-based.
Level of Evidence: 3 Spine 2013;38:1690-1694
S
cheuermann disease is a form of osteochondrosis of the spine and is characterized by increased posterior rounding of the thoracic spine in association with structural deformity of the vertebral elements.^ Previous prevalence estimates of Scheuermann disease vary widely, ranging between 0.4% and 10%.'"'^ Scheuermann disease is diagnosed on the basis of radiographical criteria, yet, there is no diagnostic "gold standard." The criteria by Sorensen and Sachs are the most commonly applied^-* but different radiographical diagnostic criteria exist.' These different radiographical criteria include endplate irregularity, thoracic kyphosis greater than 35°'-' or 45°,'" and at least 1^'' or 3'" adjacent wedged vertebral bodies each of 5° or more in magnitude'" (Figure 1). Also, Schmorl nodes are thought to be a common but not obligate manifestation of Scheuermann disease.'^ When different criteria are used inconsistently, the estimates of disease prevalence may differ widely and seem unreliable. Therefore, the purpose of our study was to determine the prevalence of Scheuermann disease and its radiographical criteria in the Dutch population across sexes and to evaluate the consistency of the diagnostic criteria. September 2013
Spine
DIAGNOSTICS
MATERIALS AND METHODS The Rotterdam Study is a prospective population-based cohort study that started in 1990 in Ommoord, a suburb of Rotterdam, the Netherlands. The main objective of the Rotterdam Study is to investigate the prevalence, incidence, and risk factors for chronic disease and disability in elderly individuals aged 55 years and older. After approximately 1 decade, the Rotterdam Study was expanded with a younger cohort (RS-III), including participants aged 45 years and older living in the same suburb. A detailed description of the Rotterdam Study has been reported previously." The Medical Ethics Committee of the Frasmus University Medical Center has approved the Rotterdam Study. A trained research technician obtained standing lateral radiographs of the thoracolumbar spine of individuals visiting the research center. All radiographs were acquired digitally according to a standardized protocol, with a focus to detector distance of 120 cm (Fujifilm Medical Systems, Stamford, CT). A DICOM viewer was used for radiographical assessment. To diagnose Scheuermann disease, the radiographical criteria of Sorensen" and Sachs et aP were applied in 2 phases (Table 1). A.A.M. and S.S., research assistants trained by a musculoskeletal radiologist (E.H.G.O.), scored the radiographs. To determine the level of agreement, a randomly selected subset (N = 154) was assessed by both readers. The musculoskeletal radiologist (E.H.CO.) acted as a third reader
Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
TABLE I^^Bíographícal
Assessment of
^^H
Phases
Data Type
1
Qualitative
Vertebral body endplate irregularities
One or more vertebral levels
Qualitative
Vertebral wedging
At least 3 adjacent vertebral levels 5° or more per vertebra
Kyphosis angle
Between thoracic levels Th5 and Thl2 45°ormore in total
2
Quantitative
Criteria
Specifications
by assessing inconclusive radiographs to resolve discrepancies. In the first phase, we triaged potential cases from normal radiographs on the basis of 2 criteria: vertebral wedging at a minimum of 3 levels and presence of vertebral body endplate irregularities. Because Schmorl nodes are actually focal indentations of the vertebral endplate,'^ we scored these as endplate irregularities. We defined potential cases as those with consecutive vertebral wedging in combination with endplate irregularity. In the second phase, we reevaluated all these potential cases by measuring the thoracic kyphosis angle between thoracic vertebral levels Th5 and Thl2. We defined a kyphosis angle of 45° or more to diagnose the Scheuermann disease cases.'" In addition, we evaluated the impact of varying the kyphosis angle criterion on prevalence estimation of Scheuermann disease by adjusting from 45° to 40° or 35°. Finally, we reassessed the levels of vertebral wedging and endplate irregularities in more detail. All radiographs fulfilling these criteria were reassessed by the other reader (A.A.M. or S.S.) to verify the diagnosis of Scheuermann disease. Statistical Methods Frequencies of each of the independent radiological diagnostic criteria were assessed per vertebral and per patient levels, and the prevalence of Scheuermann disease was determined in the study population. A random subset of radiographs was scored by both readers (A.A.M. and S.S.), and Cohen K statistics for interrater agreement were calculated for this sample and graded according to Landis and Koch.''' Sex-specific and sex-combined prevalence estimates were calculated and sex differences were tested with Pearson x^ test. Analyses were performed with SPSS statistics software version 20 (IBM, Armonk, NY).
Figure 1. Lateral radiograph showing Scheuermann disease with marked endplate irregularities and mild anterior wedging of multiple midthoracic vertebrae, resulting in increased thoracic kyphosis. Spine
RESULTS Lateral spine radiographs were available and assessed for 2753 participants (mean age, 57 yr; range, 45-89 yr). After triage, we identified 677 (24.6%) cases with endplate irregularities and 140 (5.1%) cases with vertebral wedging (Table 2). The Cohen K statistics were 78.8% for vertebral wedging and 79.4% for endplate irregularity. We investigated whether the www.spinejournal.com
1691
Spine
DIAGNOSTICS
442
450
299
Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
1
,.
• 1
11 1
1
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250 200 •
ISO •
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'' ''
ThlO Thil Vertebrallevet
occurrence of endplate irregularities and vertebral wedging differed between sexes. We found a higher prevalence of endplate irregularities among males than in females, but this difference was borderline statistically significant (P = 0.06). Also, we observed a significantly higher prevalence of vertebral wedging among males than among females (P = 0.02). In addition, most endplate irregularities occurred at thoracic and vertebral level 8 (Figure 2), and vertebral wedging was most common at the midthoracic region (Figure 3). Subsequently, 127 participants were classified as having both endplate irregularities and vertebral wedging (Table 2). The frequency of having both endplate irregularity and vertebral wedging was significantly higher in males than in females (5.6% vs. 3.9%; ? = 0.04).
Figure 2. Number of endplate irregu-
'-larities observed per thoracic (Th) and lumbar (L) vertebral level.
Next, we measured the kyphosis angle in the 127 potential cases of Scheuermann diseases (Table 3). A kyphosis angle of 45° or more was found in 111 cases (87% of the participants prioritized by the triage procedure), resulting in a definitive diagnosis of Scheuermann disease. The prevalence of Scheuermann disease was estimated to be 4.0% (95% confidence interval [CI]: 3.3%-4.7%), with no significant difference across sexes (? = 0.23) (Table 2). In addition, we evaluated whether a modification of the diagnostic criteria would infiuence the prevalence estimate of Scheuermann disease. By adjusting the kyphosis angle criterion from 45° to 40°, we found that this would increase the total number of Scheuermann disease cases to 115, resulting in no essential change in prevalence of 4.2% (95% CI: 3 . 3 % 4.7%). Similarly, no major difference was observed by using a kyphosis angle cutoff of 35°, in which the prevalence was 4.4% (95% CI: 3.6%-5.2%) after just adding 6 additional cases.
DISCUSSION
10
Upper thoracic Th4-Th6
Midthoracic Th7-Th9
Lovt/er thoracic ThlO-Thl2
Vertebral level interval Figure 3. Distribution of vertebral wedging of 3 adjacent vertebrae of 5° or more per thoracic (Th) region. 1692
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In this first epidemiological study in the Dutch population, we found a prevalence for radiographical Scheuermann disease of 4.0%, applying the criteria defined by S0rensen and Sachs. Although no "gold standard" for the radiographical definition exists, standardized scoring of independent features resulted in substantial interobserver agreement, and different definitions of diagnostic criteria did not alter disease classification. The population-based study design with radiographs of the full thoracolumbar spine and a meticulous scoring system enabled us to identify radiographical Scheuermann disease cases without clinical complaints, which would have been missed by a clinical-based study. We assessed a large number of radiographs specifically for Scheuermann disease and recorded each of the diagnostic criteria separately and in detail with high interobserver agreement. Usually, Scheuermann kyphosis becomes clinically overt during growth spurt and ceases to progress once axial skeletal maturity is reached.""^ Therefore, aU participants with Scheuermann disease should have displayed radiographical features at the time of our examination. Nevertheless, our September 2013
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DIAGNOSTICS
Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
TABLE 2 HEquencies
of the Radiological " ^ H i ^^agnostic Criteria of Scheuermann 1 Females (N = 1566)
Total (N = 2753)
Endplate irregularity
313 (26.4%)
364 (23.2%)
677 (24.6%)
0.06
Vertebral wedging
74 (6.2%)
66 (4.2%)
140 (5.1%)
0.02
Endplate irregularity -Ivertebral wedging
66 (5.6%)
61 (3.9%)
127 (4.6%)
0.04
Scheuermann disease
54 (4.5%)
57 (3.6%)
m (4.0%)
1quencies Per Kyphotic
Angle ^ 1 for P o t e n M ^ ^ ^ ^ H
Kyphotic Angle Interval
Males (N = 1187)
Variable
TABLE 3.
P*
0.23
•P value X' males versus females.
study in older individuals could have included some falsepositive cases because of the coexistence of degenerative disease. However, the most typical features of spine degeneration are disc disease, osteophytosis, and facet joint osteoarthritis,'^ which are not diagnostic criteria for Scheuermann disease. Furthermore, these degenerative changes occur much less commonly in the thoracic spine than in the cervical and lumbar regions.'* As mortality rate is unchanged in Scheuermann disease,*" our prevalence estimates may also be extrapolated to younger populations. Different expert opinion-based criteria have been used for diagnosing Scheuermann disease and these criteria remain controversial.** Therefore, we evaluated the effect of modifying the kyphosis angle criterion and found that only few more would be classified as Scheuermann cases without affecting the prevalence. Composite standardized assessment of independent criteria seems to result in sufficient diagnostic consistency. Our prevalence of 4.0% is within the previously reported range (0.4%-10%)'^'^ and highlights that radiographical Scheuermann disease is not infrequent in the general population. Each of the diagnostic criteria, that is, endplate irregularities and vertebral wedging, occurred most commonly at the midthoracic region. The frequency of both endplate irregularities and vertebral wedging was higher in males than in females; however, the sex difference in the prevalence was not statistically significant, which could be due to the limited study power with a relatively low number of cases. Some publications have reported prevalences of Scheuermann disease to be closely similar between the sexes,""^' whereas others have observed Scheuermann disease to be more prevalent among males than in females.'^'-^ An accurate and precise diagnosis of Scheuermann disease is important to provide proper treatment and hopefully to avert disability. Although coexistence with osteoporotic vertebral fractures can occur, the disorders should be distinguished as disease treatment is very different.*-"•'''•-' Radiographical findings should be correlated with clinical symptoms that typically started at adolescent age,^* nonetheless, taking into Spine
Frequency
%
20-25
2
1.6
25-30
1
0.8
30-35
3
2.4
35-40
6
4.7
40-45
4
3.1
45-50
27
21.3
50-55
30
23.6
55-60
31
24.4
60-65
12
9.4
65-70
3
2.4
70-75
4
3.1
75-80
2
1.6
80-85
2
1.6
127
100.0
Total
account recall bias. Some patients with adult Scheuermann kyphosis are only moderately affected by the disease'^"'-^''; future research might elucidate why some individuals have more complaints than others. In addition, the condition is generally not well known among clinical practitioners, which may cause diagnosis of Scheuermann disease to be missed or delayed. The fairly high disease prevalence underscores that Scheuermann disease should not be overlooked.
CONCLUSION In sum, our study revealed a prevalence of 4.0% of Scheuermann disease in the Dutch population. Standardized scoring of independent features resulted in substantial interobserver agreement, and different applications of diagnostic criteria did not alter disease classification.
>^ Key Points Q The prevalence of radiographical Scheuermann disease was 4.0% in a Dutch population sample aged 45 years and older. •
Vertebral wedging and endplate irregularities are significantly more prevalent among males.
•
Standardized scoring of independent Scheuermann disease radiographical features shows substantial interobserver agreement.
•
Current diagnostic criteria for Scheuermann disease seem sufficient, as different applications on a population level did not significantly alter disease classification. www.spinejournal.com
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Acknowledgments The authors are grateful to the study participants, the staff from the Rotterdam Study (particularly Lydia Buist and Hannie van den Boogert for acquisition of the radiographs), and the participating general practitioners and pharmacists. The authors thank René Vermeren, Nano Suwarno, and Mart Rentmeester for their technical support. The Medical Ethics Committee of the Erasmus University Medical Center has approved the Rotterdam Study. The Rotterdam Study is funded by Erasmus Medical Center and Erasmus University, Rotterdam, Netherlands Organization for the Health Research and Development (ZonMw), the Research Institute for Diseases in the Elderly (RIDE), the Ministry of Education, Culture and Science, the Ministry for Health, Welfare and Sports, the European Commission (DG XII), The Netherlands Genomics Initiative (NGI), Netherlands Consortium of Healthy Ageing (NCHA), and the Municipality of Rotterdam. References 1. Hart ES, Merlin C, Harisiades J, et al. Scheuermann's thoracic kyphosis in the adolescent patient. Orthop Nurs 2010;29:365-71; quiz 72-3. 2. Damborg E, Engell V, Andersen M, et al. Prevalence, concordance, and heritability of Scheuermann kyphosis based on a study of twins. / Bone ]oint Surg Am 2006;88:2133-6. 3. Heithoff KB, Gundry CR, Burton CV, et al. Juvenile discogenic disease. Spine (Phila Pa 1976) 1994;19:335-40. 4. Nissinen M. Spinal posture during pubertal growth. Acta Paediatr 1995;84:308-12. 5. Papagelopoulos PJ, Mavrogenis AE, Savvidou OD, et al. Current concepts in Scheuermann's kyphosis. Orthopedics 2008;31:52-8; quiz 9-60. 6. Puisto V, Rissanen H, Heliovaara M, et al. Mortality in the presence of a vertebral fracture, scoliosis, or Scheuermann's disease in the thoracic spine. Ann Epidemiol 2008;18:595-601. 7. Serensen KH. Seheuermann's ]uvenile Kyphosis: Clinical Appearanees. Radiography, Aetiology and Prognosised. Copenhagen, Denmark: Munksgaard; 1964. 8. Sachs B, Bradford D, Winter R, et al. Scheuermann kyphosis. Eollow-up of Milwaukee-brace treatment. / Bone ]oint Surg Am ' 1987;69:50-7. 9. Wenger DR, Frick SL. Scheuermann kyphosis. Spine (Phila Pa 1976) 1999;24:2630-9. 10. Bradford DS, Moe JH, Montalvo EJ, et al. Scheuermann's kyphosis and roundback deformity. Results of Milwaukee brace treatment. / Bone]oint Surg Am 1974;56:740-58.
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Scheuermann Disease Radiological Criteria Evaluation • Makurthou et al
11. Masharawi Y, Rothschild B, Peled N, et al. A simple radiological method for recognizing osteoporotic thoracic vertebral compression fractures and distinguishing them from Scheuermann disease. Spine (Phila Pa 1976) 2009;34:1995-9. 12. Pfirrmann CW, Resnick D. Schmorl nodes of the thoracic and lumbar spine: radiographie-pathologie study of prevalence, characterization, and correlation with degenerative changes of 1,650 spinal levels in 100 cadavers. Radiology 2001;219:368-74. 13. Hofman A, van Duijn CM, Eranco OH, et al. The Rotterdam Study: 2012 objectives and design update. Eur ] Epidemiol 2011;26: 657-86. 14. Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics ]977;33:159-74. 15. Eotiadis E, Kenanidis E, Samoladas E, et al. Scheuermann's disease: focus on weight and height role. Eur Spine ] 2008;17: 673-8. 16. Lemire JJ, Mierau DR, Crawford CM, et al. Scheuermann's juvenile jcyphosis. / Manipulative Physiol Ther 1996;19: 195-201. 17. Peterson CK, Bolton JE, Wood AR. A cross-sectional study correlating lumbar spine degeneration with disability and pain. Spine (Phila Pa 1976) 2000;25:218-23. 18. Niemelainen R, Battie MC, Gill K, et al. The prevalence and characteristics of thoracic magnetic resonance imaging findings in men. Spine (Phila Pa 1976) 2008;33:2552-9. 19. Lowe TG, Line BG. Evidence based medicine: analysis of Scheuermann kyphosis. Spine (Phila Pa 1976) 2007;32:S115-9. 20. Murray PM, Weinstein SL, Spratt KE. The natural history and longterm follow-up of Scheuermann kyphosis. / Bone ]oint Surg Am 1993;75:236-48. 21. Rachbauer E, Sterzinger W, Eibl G. Radiographic abnormalities in the thoracolumbar spine of young elite skiers. Am ] Sports Med 2001;29:446-9. 22. Eisk JW, Baigent ML, Hill PD. Scheuermann's disease. Clinical and radiological survey of 17 and 18 year olds. Am ] Phys Med 1984;63:18-30. 23. Ristolainen L, Kettunen JA, Heliovaara M, et al. Untreated Scheuermann's disease: a 37-year follow-up study. Eur Spine ] 2012;21:819-24. 24. Jiang G, Eastell R, Barrington NA, et al. Comparison of methods for the visual identification of prevalent vertebral fracture in osteoporosis. Osteoporos lnt 2004;15:887-96. 25. Oei L, Rivadeneira E, Ly E, et al. Review of radiological scoring methods of osteoporotic vertebral fractures for clinical and research settings. Eur Radiol 2013;23:476-86. 26. Summers BN, Singh JP, Manns RA. The radiological reporting of lumbar Scheuermann's disease: an unnecessary source of confusion amongst clinicians and patients. Br] Radiol 2008;81:383-5. 27. Wood KB, Melikian R, Villamil E Adult Scheuermann kyphosis: evaluation, management, and new developments. / Am Acad Orthop Surg20\2;20:lU-2\.
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