Abstract
Background
The diagnosis of slipped capital femoral epiphysis (SCFE) often is delayed. Although lack of clinical suspicion is the main cause of delayed diagnosis, typical radiographic changes may not be present during the initial phases of SCFE. The peritubercle lucency sign for follow-up of the contralateral hip in patients with unilateral SCFE may be beneficial in assisting the early diagnosis. However, the accuracy and reliability of this sign in patients with SCFE is unknown.
Questions/purposes
(1) What is the accuracy, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of the peritubercle lucency sign on radiographs for the early diagnosis of SCFE compared with MRI as the gold standard? (2) What are the interobserver and intraobserver reliabilities of the peritubercle lucency sign on radiographs?
Methods
Between 2000 and 2017, 71 patients underwent MRI for an evaluation of pre-slip or a minimally displaced SCFE. Sixty percent of hips (43 of 71) had confirmed SCFE or pre-slip based on the presence of hip pain and MRI changes, and these patients underwent in situ pinning. Three independent experienced observers reviewed MR images of the 71 hips and agreed on the presence of a juxtaphyseal bright-fluid signal suggesting bone marrow edema in these 43 hips with SCFE, and absence MRI changes in the remaining 28 hips. The same three experienced observers and two inexperienced observers, including a general radiologist and an orthopaedic surgery resident, blindly assessed the radiographs for the presence or absence of the peritubercle lucency sign, without information about the diagnosis. Diagnostic accuracy measures including sensitivity, specificity, PPV, and NPV were evaluated. Intraobserver and interobserver agreements were calculated using kappa statistics.
Results
The overall accuracy of the peritubercle lucency sign on radiographs was 94% (95% CI 91 to 96), sensitivity was 97% (95% CI 95 to 99), specificity was 89% (95% CI 90 to 96), PPV was 93% (95% CI 90 to 96), and NPV was 95% (95% CI 92 to 99). All accuracy parameters were greater than 85% for the five observers, regardless of experience level. Intraobserver agreement was perfect (kappa 1.0), and interobserver agreement was excellent for the peritubercle lucency sign on radiographs across the five observers (kappa 0.81 [95% CI 0.73 to 0.88]). The reliability was excellent for experienced observers (kappa 0.88 [95% CI 0.74 to 1.00]) and substantial for inexperienced observers (kappa 0.70 [95% CI 0.46 to 0.93]), although no difference was found with the numbers available (p = 0.18).
Conclusions
The peritubercle lucency sign on radiographs is accurate and reliable for the early diagnosis of SCFE compared with MRI as the gold standard. Improving the early diagnosis of SCFE may be possible with increased awareness, high clinical suspicion, and a scrutinized evaluation of radiographs including an assessment of the peritubercle lucency sign.
Level of Evidence
Level III, diagnostic study.
Introduction
The diagnosis of a slipped capital femoral epiphysis (SCFE) usually is made with an AP pelvic radiograph and a lateral radiograph of the proximal femur [2, 9, 13]. Identifying the pre-slip stage and mild slip is more difficult than identifying moderate and severe SCFE because of the lack of displacement [11, 18, 38]. Early diagnosis is essential to allow for timely surgical intervention before the development of severe deformities and associated complications [4, 21, 31]. Nevertheless, delay in the diagnosis of SCFE has repeatedly been reported [11, 17, 29, 33, 34]. Although a lack of clinical suspicion is the main cause of delayed diagnosis, classic radiographic changes may not be present during the initial phases of SCFE. MRI findings help identify SCFE early in the pre-slip stage, with no displacement [8, 18, 26, 38, 39]. However, access to and the cost of MRI may limit its application.
The epiphyseal tubercle is an osseous prominence, eccentrically located at the posterior aspect of the physeal surface of the epiphysis, protruding into the metaphyseal fossa [19, 27, 28, 32, 35, 36]. Recent studies suggested there was a rotational mechanism of SCFE in which the epiphysis rotates with the fulcrum at the epiphyseal tubercle [20, 22, 35, 36]. If the epiphyseal tubercle acts as a stabilizer of the epiphysis [14, 15], then the abnormal mechanical environment associated with SCFE could lead to concentration of stress in the tubercle and its metaphyseal fossa. High-stress concentration could lead to early structural changes around the tubercle that could be identified on radiographs and MR images [22, 24]. The peritubercle lucency sign [24] recently has been described as a potential early radiographic sign in SCFE, but its accuracy to detect early SCFE is not known.
In this study we asked: (1) What is the accuracy, sensitivity, specificity, positive predictive value (PPV), and negative predictive value (NPV) of the peritubercle lucency sign on radiographs for the early diagnosis of SCFE compared with MRI as the gold standard? (2) What are the interobserver and intraobserver reliabilities of the peritubercle lucency sign on radiographs?
Patients and Methods
The institutional review board of our institution approved this retrospective study. We searched our institution’s database for patients with a possible diagnosis of SCFE who underwent a hip MRI between 2000 and 2017. During this period, 754 patients had a diagnosis of SCFE, of whom 181 underwent MRI. Eighty patients had MRI after surgical treatment of SCFE and were excluded. Seventeen patients with moderate or severe SCFE were excluded because the focus of the study was on SCFE with no or minimal displacement. Eight patients were excluded because of an incomplete set of images. Finally, three patients with a closed growth plate and two patients who underwent prophylactic treatment of contralateral SCFE were excluded. The final cohort included 71 patients who underwent hip MRI because of suspected SCFE or pre-slip. Fifty-one percent (36 of 71 patients) were female and 49% (35 of 71) were male, with a mean age ± SD at the time of MRI of 12.6 years ± 1.8 years. The median BMI-for-age percentile was 97.1 and the interquartile range (25th to 75th percentiles) was 94.1 to 99.2. The clinical indication for MRI was hip pain in 96% (68 of 71) of hips. Three hips were asymptomatic, and MRI was performed for surveillance of the contralateral hip in patients with unilateral SCFE (one hip) or to rule out subclinical pre-slip (two hips). Before MR images were acquired, the treating physician and radiologist reported that 62% (44 of 71 hips) had no radiographic evidence of SCFE and 25% (18 of 71 hips) had slight widening of the capital growth plate, indicating a pre-slip condition (Table 1). The study endpoints were (1) confirmation of the diagnosis of SCFE or pre-slip based on the presence on MRI of previously described features of SCFE [8, 18, 37-39], including widening of the capital growth plate or juxtaphyseal bone marrow edema; and (2) exclusion of a pre-slip or SCFE diagnosis based on negative findings on MRI and complete resolution of clinical symptoms at a minimum follow-up interval of 6 weeks after MR images were acquired. Of the 71 hips included in the study, 60% (43 hips) had a diagnosis of SCFE based on hip pain and MRI changes, and these patients underwent surgical treatment with in situ pinning (Fig. 1).
Table 1.
Demographic characteristics (n = 71)
Fig. 1.
This flowchart shows the study population of patients with a confirmed diagnosis of minimally displaced SCFE and a pre-slip condition or no SCFE diagnosis.
During the study period, MR images were obtained using a variety of scanners. Seventy-five percent of the studies (53 of 71) were performed at the authors’ institution, and the remaining 25% (18 of 71) of studies were performed an outside facility with images uploaded into the Picture Archiving and Communication System (PACS) for review. Seventy percent of the studies (50 of 71) were acquired with a 1.5 Tesla MRI system (GE Healthcare, Milwaukee WI, USA, and Siemens Healthcare, Erlangen Germany), and 30% (21 of 71) were acquired on a 3.0 Tesla MRI system (GE Healthcare and Siemens Healthcare). Although the imaging protocols varied across institutions and magnets, all scans included dedicated sequences of the affected hip with vendor-specific modifications. The 71 scans had at least one fluid-sensitive MRI sequence (T2-weighted, proton-density weighted, or inversion recovery) in the coronal plane and a fluid-sensitive sequence either in the axial, sagittal, or oblique sagittal plane through the femoral neck’s axis. Nineteen scans had sequences acquired after infusion of intravenous contrast. Coronal, axial, and sagittal fluid-sensitive MRI sequences were anonymized and exported separately for an independent evaluation by two experienced pediatric orthopaedic surgeons (DAM and ENN, who have 10 and 15 years of practice, respectively) and one experienced pediatric musculoskeletal radiologist (SB, 15 years of practice). The observers evaluated the MR images during a review session for training, followed by an independent blinded evaluation by each observer.
AP pelvic radiographs were acquired with the patient supine on the table and the radiography beam centered just above the pubic symphysis. Lateral radiographs were obtained in the bilateral frog-leg lateral position, with hips in 45° of flexion and abduction and externally rotated so the soles of the feet were facing each other [5]. The epiphyseal tubercle was identified as the most prominent protuberance located at the posterosuperior region of the physeal surface of the epiphysis (Fig. 2) [19, 35, 36]. For this study, we assessed Klein’s line sign [10] and the posterior epiphyseal tilt angle, measured in the lateral view [1, 23]. Tilt angles less than 12° [16, 25] and a symmetric Klein’s line transecting the epiphysis [10] indicated normal capital epiphysis alignment. For the 43 patients who had SCFE, we identified 21 hips in the pre-slip stage, defined as the presence of pain, normal radiographic tilt, Klein’s line intersecting the epiphysis, and the presence of juxtaphyseal edema on MRI. Twenty-two hips had evidence of minimally displaced slip, and in addition to edema as seen on MRI, there was an abnormal tilt angle (greater than 12°) and/or a positive Klein’s line sign (Table 2).
Fig. 2 A-D.
This figure shows the normal aspect of the epiphyseal tubercle (asterisks) and its metaphyseal fossa (arrowheads). We performed an imaging investigation in a 12-year-old boy with 1 day of left hip pain who previously had a right SCFE. After radiographs were taken, MR images were acquired to rule out a contralateral pre-slip condition. (A) AP and (B) lateral radiographs of the left hip show no epiphyseal displacement and a normal Klein’s line, tilt angle, and physeal width. No radiolucency is observed around the epiphyseal tubercle (asterisk). Fluid-sensitive MR images acquired in the (C) coronal (inversion recovery) and (D) axial oblique planes (proton-density) show no abnormalities around the epiphyseal tubercle (asterisk) and its metaphyseal fossa (arrowheads). The suspicion of a pre-slip condition was not confirmed.
Table 2.
Radiographic findings of the 71 hips stratified as normal, pre-slip, and minimally displaced SCFE
Accuracy of the Peritubercle Lucency Sign on Radiographs
The gold standard criteria for the diagnosis of SCFE in this study was the presence of a bright-fluid signal suggesting bone marrow edema adjacent to the capital femoral growth plate and widening of the growth plate (Fig. 3) [8, 18, 26, 37-39], leading to surgical treatment with in situ pinning. Intra-epiphyseal changes including a bright signal on fluid-sensitive sequences restricted to the epiphyseal tubercle were defined as the peritubercle edema sign and were also considered to indicate a positive diagnosis of SCFE on MRI (Fig. 4). The current gold-standard diagnosis of SCFE was based on the ability of MRI to detect the condition at the pre-slip stage or when there was minimal displacement [8, 18, 26, 37-39], associated with the in situ fixation decision-making. The MRI diagnosis was defined by the consistency of agreement among the three experienced observers (DAM, ENN, SB).
Fig. 3 A-D.
An imaging investigation of the left hip was performed to rule out contralateral pre-slip in a 15-year-old boy with 2 weeks of hip pain with a prior right SCFE. (A) AP and (B) lateral radiographs of the left hip show no epiphyseal displacement, a normal Klein’s line, and physeal widening. The peritubercle lucency sign is observed as subtle radiolucency (black arrowheads) surrounding the epiphyseal tubercle (asterisks) on a lateral view. Along with diffuse metaphyseal bone marrow edema, the peritubercle edema sign (white arrowhead) is observed on fluid-sensitive T2-weighted MR images acquired in the (C) coronal and (D) axial oblique planes, and is characterized by a focal intra-epiphyseal high-intensity signal at the epiphyseal tubercle.
Fig. 4 A-E.
An imaging investigation was performed in an 11-year-old girl with 3 weeks of left hip pain with a prior right SCFE. After radiographs were taken, MR images were acquired to rule out a pre-slip condition. (A) AP and (B) lateral radiographs of the left hip show no epiphyseal displacement, a normal Klein’s line, and physeal widening. (B) On a lateral view, there is evident lytic enlargement of the metaphyseal fossa (black arrowheads) around the epiphyseal tubercle (asterisks), characterizing the peritubercle lucency sign. Fluid-sensitive MR images acquired in the (C) coronal (T2-weighted), (D) axial oblique (proton density), and (E) sagittal (T2-weighted) planes show diffuse metaphyseal bone marrow edema and a focal intra-epiphyseal high-intensity signal at the epiphyseal tubercle, characterizing the peritubercle edema sign (white arrowheads).
For the analysis of the peritubercle lucency sign, the identification of the anatomic positioning of the epiphyseal was essential. On AP radiographs, the epiphyseal tubercle is usually found in the central 1/3 of the growth plate because of physiologic femoral anteversion. On lateral radiographs, the tubercle is usually located at the third posterior quadrant of the growth plate [24]. Focal changes around the tubercle including widening or enlargement of the corresponding metaphyseal fossa, with or without adjacent osteolysis or sclerosis, were recorded as a positive peritubercle lucency sign (Fig. 3). Lucency at the metaphyseal bone adjacent to the epiphyseal tubercle involved blurring of the trabecular bone and focal enlargement of the growth plate’s width that was restricted to the epiphyseal tubercle area (Fig. 5). The presence of chronic, abnormal stress may generate a sclerotic process, usually at the posterior metaphyseal bone adjacent to the epiphyseal tubercle. Global, diffuse physeal widening without metaphyseal lucency around the epiphyseal tubercle was considered a negative or absent peritubercle lucency sign [24].
Fig. 5 A-D.
An imaging investigation was performed in a 16-year-old girl with an 8-week history of right hip pain. After radiographs were taken, MR images were acquired to confirm minimally displaced SCFE. (A) AP and (B) lateral radiographs of the right hip show mild epiphyseal displacement, an abnormal Klein’s line, and physeal widening. The peritubercle lucency sign (black arrowheads) is observed at the metaphyseal fossa surrounding the epiphyseal tubercle (asterisks), which is in contact with the posterior wall of the fossa. Fluid-sensitive MRI sequences acquired in the (C) coronal (T2-weighted) and (D) sagittal (proton density) planes show a diffuse, high-intensity signal adjacent to the growth plate at the epiphyseal tubercle (white arrowhead, peritubercle edema sign).
AP and lateral radiographs at the onset of hip pain were anonymized and exported, and were independently evaluated by the three experienced observers (DAM, ENN, SB) and by two less experienced observers (SH, second-year orthopaedic surgery resident; and MPG, general pediatric radiologist with 1 year of practice, with no sub-specialization in musculoskeletal radiology). Radiographs were evaluated in an independent session by all observers, without information about the MRI results. For imaging interpretation, all five observers were blinded as to whether the hips underwent subsequent SCFE treatment and whether symptoms resolved.
We assessed the accuracy of the peritubercle lucency sign on radiographs by comparing the presence of this sign with the definitive diagnosis of SCFE based the on MRI gold-standard diagnosis. The sensitivity, specificity, PPV, and NPV were calculated. Values are reported for each observer and for all observers. Additional summary values for AP and lateral radiographs are reported based on measurements by the three experienced observers (DAM, ENN, SB). All imaging studies were assessed using the software Osirix Lite 8.5.2 (Pixmeo Sarl, Berne, Switzerland).
Reliability of the Peritubercle Lucency Sign on Radiographs
For interobserver agreement, we estimated kappa statistics and 95% confidence intervals (CIs). Overall interobserver agreement was calculated for the five observers (DAM, ENN, SB, SH, MPG), and separately for three observers (DAM, ENN, SB) who had more experience with the tubercle radiographic signs, and the other two observers (SH, MPG) who had little to no experience.
For intraobserver agreement, one observer (DAM) performed a blinded second reading of all radiographs after 2 months to evaluate intraobserver agreement as estimated by kappa values and 95% CIs. Only one observer performed intraobserver agreement, given the regular reading outcomes among the experienced observers.
Statistical Analysis
A power analysis indicated that to detect a kappa value of at least 0.8 with a 10% margin of error, we would require a minimum of 58 readings across observers based on a one-sided test, assuming an SCFE diagnosis rate of 60% in the sample. Intraobserver and interobserver agreement across the five observers were assessed by estimating Fleiss’s kappa [7] along with 95% CIs for the peritubercle lucency sign on radiographs. A concordance statistic [6] was also estimated to identify any paradoxical bias in our kappa estimates. For all instances in which concordance and kappa agreed, only kappa was reported. A subgroup analysis of interobserver agreement was conducted, separating agreement statistics by the observer’s experience level. Comparisons of agreement statistics were based on reviewing CIs. Non-overlapping CIs indicated a difference in reliability across experience level subgroups. Kappa values between 0 and 0.20 were considered poor reliability, values between 0.21 and 0.40 were considered fair, values between 0.41 and 0.60 were considered moderate, values between 0.61 and 0.80 were considered substantial, and values between 0.81 and 1.00 were considered excellent [7].
All tests were two-sided, and p values less than 0.05 were considered significant.
Results
The overall accuracy of radiographs for determining the peritubercle lucency sign was 94% (95% CI 91 to 96) among the five readers (Table 3). The accuracy by radiograph incidence was slightly higher for frog-leg lateral radiographs (95% [95% CI 92 to 98]) than for AP radiographs (87% [95% CI 83 to 92]; p = 0.04). The accuracy of the peritubercle lucency sign was above 90% for all observers, and the sensitivity, specificity, PPV, and NPV were all above 85%, regardless of experience level (Table 4).
Table 3.
Accuracy of the peritubercle radiolucency sign, positive Klein’s line, and physeal widening
Table 4.
Accuracy of the peritubercle radiolucency sign by observer and experience level and for all raters
For the 43 hips with an MRI-based diagnosis of SCFE, the radiographic peritubercle lucency sign on either the AP or lateral view was considered present in 100% of the hips (43 of 43) by Observer 1, in 95% (41 of 43) by Observer 2, in 100% (43 of 43) by Observer 3, in 98% (42 of 43) by Observer 4, and in 93% (40 of 43) by Observer 5. Overall, the five observers agreed about the presence or absence of the peritubercle lucency sign on 80% of the radiographs, whereas agreement was 92% among the three experienced observers and 86% between the two inexperienced observers. Concordance and kappa values were nearly identical, indicating a lack of paradox in our data and kappa estimates. Interobserver agreement was excellent across all five observers (kappa 0.81 [95% CI 0.73 to 0.88]). Reliability was considered excellent for experienced observers (kappa 0.88 [95% CI 0.74 to 1.00]) and substantial for inexperienced observers (kappa 0.70 [95% CI 0.46 to 0.93]), although no difference was observed with the numbers available (p = 0.18). Intraobserver agreement was perfect (kappa 1.00 [95% CI 0.77 to 1.00]) (Table 5).
Table 5.
Interobserver and intraobserver agreement for the peritubercle lucency sign
Discussion
An early diagnosis of SCFE is essential for timely treatment before the development of severe deformities. A recent study described the peritubercle lucency sign as a common and early radiographic finding in patients with SCFE [24]. However, the accuracy and reliability of radiographic imaging abnormalities around the epiphyseal tubercle are unknown. Compared with the current gold-standard for SCFE diagnosis, which is juxtaphyseal bone marrow edema on the MRI [8, 18, 26, 37-39], we found that the presence of the peritubercle lucency sign on radiographs is accurate, with high sensitivity, specificity, PPV, and NPV for the diagnosis of a pre-slip condition or minimally displaced SCFE. Intraobserver and interobserver reliability were substantial to excellent, suggesting that the peritubercle lucency sign is a reliable finding for the early diagnosis of SCFE, even for less experienced radiologists and orthopaedic surgeons in the beginning of the learning curve.
Our study has several limitations. First, MRI was performed on different imaging systems in and outside our institution, with variations between acquisition protocols. Second, there is a concern for observer bias because of the previously known clinical suspicion of SCFE. Nevertheless, all five observers were blinded to the research endpoints (SCFE versus non-SCFE). Third, 40% of the hips (28 of 71) had normal findings on MRI and complete resolution of symptoms at a minimum of 6 weeks after MR images were acquired, and they were not considered to have SCFE. Although we cannot entirely exclude the possibility that a slip developed later in some of these patients, the purpose of this study was to test radiographic and MRI findings for the diagnosis of SCFE at the time the images were obtained. Fourth, the BMI percentile in the general population of patients with SCFE is frequently elevated, potentially having a negative effect on the clarity of radiographs and identification of peritubercle lucency. Fifth, we did not compare these findings with those of a control population of asymptomatic patients. Focal periphyseal edema of the distal femur and proximal tibia have been seen on MRI in adolescents as a sign of early stages of physiologic physeal fusion rather than an abnormality [41]. Although the peritubercle edema sign could be an equivalent form of focal periphyseal edema of the proximal femur, we believe a further investigation is needed to clarify whether focal periphyseal edema zones exist around the hip.
We found the peritubercle lucency sign has high accuracy, sensitivity, and specificity for the early diagnosis of SCFE, even for less experienced observers. The peritubercle lucency sign was described for surveillance of the contralateral hip in patients with unilateral SCFE. The reported accuracy of the signal was 95%, sensitivity was 84%, and specificity was 99% [24]. However, the reference for accuracy testing in this previous study was in situ pinning surgery. Considering surgical treatment as the gold standard to test accuracy may be problematic because of selection bias. Surgeons may have been biased to perform early treatment to avoid development of a subsequent deformity without clear imaging evidence of SCFE. Here, we established MRI criteria as the gold standard for testing the accuracy of measurements of the peritubercle lucency sign, independent of surgical treatment [8, 18, 26, 37, 38]. The peritubercle lucency sign may improve the early diagnosis of SCFE, requiring a further longitudinal study to reinforce our hypothesis. However, the current radiographic criteria may not identify early SCFE with minimal or no displacement [10, 11, 17, 30]. Two previous studies showed that Klein’s line as a single criterion had poor sensitivity [11, 30]. Previous studies described blurring of the metaphyseal margin with loss of the typical mammillary processes and widening of the growth plate as early radiographic findings of imminent or incipient SCFE [3, 9, 12]. However, in our study only 20 of the 43 hips with SCFE had diffuse physeal widening on radiographs, yielding an accuracy of 66% and sensitivity of 44%, while the overall accuracy of the peritubercle sign was 94% and sensitivity was 97%, for both experienced and less experienced observers. We believe the peritubercle lucency sign may be valuable when there is no clear anatomic displacement but a potential mechanical insufficiency on the growth plate [40], allowing for peritubercle resorption and lucency on radiographs. The initial deformity may be rotational, in which the metaphysis rotates around the epiphyseal tubercle as a fulcrum [19, 35, 36]. Smaller degrees of rotation would not be noticeable using traditional methods such as Klein’s line, Southwick angle, or percentage of displacement [22, 24]. Instead, the abnormal relationship between the tubercle and its metaphyseal fossa, without its docking characteristics, would suggest the onset of SCFE, and this phenomenon was supported by our data. According to a recently described staging system, the deformity would progress with the tubercle pressing against the posterior wall of the socket, and the peritubercle lucency advancing toward the posterior cortex of the femoral neck [22].
We found that the peritubercle lucency sign is reproducible among three experienced observers and two less-experienced observers, who agreed about the presence or absence of the peritubercle lucency sign on 80% of the radiographs, allowing for excellent overall interobserver kappa agreement. The reliability among observers tended to be excellent for the experienced radiologist and trained orthopaedic surgeons, and substantial for the initial learning curve of the general radiologist and orthopaedic resident, with no differences between the kappa coefficients available. In a previous study [24], agreement between two observers was also excellent. Conversely, classic radiographic parameters for the early diagnosis of SCFE have been reported, with varying reproducibility [10, 30, 34, 39]. A report on a modified Klein’s method considering asymmetry of 2 mm in the epiphyseal width crossed by the Klein line found there was substantial agreement among observers [10]. However, weak-to-moderate interobserver agreement about widening of the growth plate (intraclass correlation coefficient range 0.53-0.73) was reported in 22 patients with unilateral SCFE who underwent MRI at the initial diagnosis [39].
In conclusion, we validated the radiographic peritubercle lucency sign as an accurate and reliable imaging sign for the early diagnosis of SCFE. We believe that application of this novel sign in clinical practice may improve the ability to identify SCFE during its early phases, especially in the pre-slip stage, when no displacement is present. However, further longitudinal studies are necessary to confirm this hypothesis. In adolescents with clinically suspected SCFE, we currently prefer AP pelvic and bilateral frog-lateral radiographs with attention to the peritubercle lucency sign in addition to the classic slip signs. We recommend MRI in adolescents with clinically suspected SCFE and negative findings on radiographs.
Acknowledgments
None.
Footnotes
Each author certifies that neither he or she, nor any member of his or her immediate family, has funding or commercial associations (consultancies, stock ownership, equity interest, patent/licensing arrangements, etc.) that might pose a conflict of interest in connection with the submitted article.
All ICMJE Conflict of Interest Forms for authors and Clinical Orthopaedics and Related Research® editors and board members are on file with the publication and can be viewed on request.
Each author certifies that his or her institution approved the human protocol for this investigation and that all investigations were conducted in conformity with ethical principles of research.
This work was performed at Boston’s Children’s Hospital, Boston, MA, USA.
References
- 1.Albers CE, Steppacher SD, Haefeli PC, Werlen S, Hanke MS, Siebenrock KA, Tannast M. Twelve percent of hips with a primary cam deformity exhibit a slip-like morphology resembling sequelae of slipped capital femoral epiphysis. Clin Orthop Relat Res. 2015;473:1212-1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Aronsson DD, Karol LA. Stable slipped capital femoral epiphysis: evaluation and management. J Am Acad Orthop Surg. 1996;4:173-181. [DOI] [PubMed] [Google Scholar]
- 3.Bloomberg TJ, Nuttall J, Stoker DJ. Radiology in early slipped femoral capital epiphysis. Clin Radiol. 1978;29:657-667. [DOI] [PubMed] [Google Scholar]
- 4.Carney BT, Weinstein SL. Natural history of untreated chronic slipped capital femoral epiphysis. Clin Orthop Relat Res. 1996:43-47. [PubMed] [Google Scholar]
- 5.Clohisy JC, Carlisle JC, Beaule PE, Kim YJ, Trousdale RT, Sierra RJ, Leunig M, Schoenecker PL, Millis MB. A systematic approach to the plain radiographic evaluation of the young adult hip. J Bone Joint Surg Am. 2008;90 Suppl 4:47-66. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Falotico R, Quatto P. On avoiding paradoxes in assessing inter-rater agreement. Italian Journal of Applied Statistics. 2010;22:151-160. [Google Scholar]
- 7.Fleiss JL. Measuring nominal scale agreement among many raters. Psychological Bulletin. 1971;76:378-382. [Google Scholar]
- 8.Futami T, Suzuki S, Seto Y, Kashiwagi N. Sequential magnetic resonance imaging in slipped capital femoral epiphysis: assessment of preslip in the contralateral hip. J Pediatr Orthop B. 2001;10:298-303. [PubMed] [Google Scholar]
- 9.Gekeler J. Radiology of adolescent slipped capital femoral epiphysis: measurement of epiphyseal angles and diagnosis. Oper Orthop Traumatol. 2007;19:329-344. [DOI] [PubMed] [Google Scholar]
- 10.Green DW, Mogekwu N, Scher DM, Handler S, Chalmers P, Widmann RF. A modification of Klein's Line to improve sensitivity of the anterior-posterior radiograph in slipped capital femoral epiphysis. J Pediatr Orthop. 2009;29:449-453. [DOI] [PubMed] [Google Scholar]
- 11.Green DW, Reynolds RA, Khan SN, Tolo V. The delay in diagnosis of slipped capital femoral epiphysis: a review of 102 patients. HSS J. 2005;1:103-106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Hesper T, Zilkens C, Bittersohl B, Krauspe R. Imaging modalities in patients with slipped capital femoral epiphysis. J Child Orthop. 2017;11:99-106. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Jarrett DY, Matheney T, Kleinman PK. Imaging SCFE: diagnosis, treatment and complications. Pediatr Radiol. 2013;43 Suppl 1:S71-82. [DOI] [PubMed] [Google Scholar]
- 14.Jonasson PS, Ekstrom L, Sward A, Sansone M, Ahlden M, Karlsson J, Baranto A. Strength of the porcine proximal femoral epiphyseal plate: the effect of different loading directions and the role of the perichondrial fibrocartilaginous complex and epiphyseal tubercle - an experimental biomechanical study. J Exp Orthop. 2014;1:4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Kiapour AM, Kiapour A, Maranho DA, Kim YJ, Novais EN. Relative contribution of epiphyseal tubercle and peripheral cupping to capital femoral epiphysis stability during daily activities. J Orthop Res. 2019;37:1571-1579. [DOI] [PubMed] [Google Scholar]
- 16.Kienle KP, Keck J, Werlen S, Kim YJ, Siebenrock KA, Mamisch TC. Femoral morphology and epiphyseal growth plate changes of the hip during maturation: MR assessments in a 1-year follow-up on a cross-sectional asymptomatic cohort in the age range of 9-17 years. Skeletal Radiol. 2012;41:1381-1390. [DOI] [PubMed] [Google Scholar]
- 17.Kocher MS, Bishop JA, Weed B, Hresko MT, Millis MB, Kim YJ, Kasser JR. Delay in diagnosis of slipped capital femoral epiphysis. Pediatrics. 2004;113:e322-325. [DOI] [PubMed] [Google Scholar]
- 18.Lalaji A, Umans H, Schneider R, Mintz D, Liebling MS, Haramati N. MRI features of confirmed "pre-slip" capital femoral epiphysis: a report of two cases. Skeletal Radiol. 2002;31:362-365. [DOI] [PubMed] [Google Scholar]
- 19.Liu RW, Armstrong DG, Levine AD, Gilmore A, Thompson GH, Cooperman DR. An anatomic study of the epiphyseal tubercle and its importance in the pathogenesis of slipped capital femoral epiphysis. J Bone Joint Surg Am. 2013;95:e341-348. [DOI] [PubMed] [Google Scholar]
- 20.Liu RW, Fraley SM, Morris WZ, Cooperman DR. Validity and Clinical Consequences of a Rotational Mechanism for Slipped Capital Femoral Epiphysis. J Pediatr Orthop. 2016;36:239-246. [DOI] [PubMed] [Google Scholar]
- 21.Loder RT, Starnes T, Dikos G, Aronsson DD. Demographic predictors of severity of stable slipped capital femoral epiphyses. J Bone Joint Surg Am. 2006;88:97-105. [DOI] [PubMed] [Google Scholar]
- 22.Maranho DA, Bixby S, Miller PE, Novais EN. A novel classification system for slipped capital femoral epiphysis based on the radiographic relationship of the epiphyseal tubercle and the metaphyseal socket. J Bone Joint Surg Open Access. 2019;4:e0033. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Maranho DA, Ferrer MG, Kim YJ, Miller PE, Novais EN. Predicting risk of contralateral slip in unilateral slipped capital femoral epiphysis: posterior epiphyseal tilt increases and superior epiphyseal extension reduces risk. J Bone Joint Surg Am. 2019;101:209-217. [DOI] [PubMed] [Google Scholar]
- 24.Maranho DA, Miller PE, Novais EN. The peritubercle lucency sign is a common and early radiographic finding in slipped capital femoral epiphysis. J Pediatr Orthop. 2018;38:e371-e376. [DOI] [PubMed] [Google Scholar]
- 25.Monazzam S, Bomar JD, Pennock AT. Idiopathic cam morphology is not caused by subclinical slipped capital femoral epiphysis: an MRI and CT study. Orthop J Sports Med. 2013;1:2325967113512467. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Montenegro NB, Junior VF, Grinfeld R, Rodrigues MB, Santos Pereira ED, Gorios C. Magnetic resonance imaging for diagnosing the pre-slip stage of the contralateral proximal femoral epiphysis in patients with unilateral epiphysiolysis. Rev Bras Ortop. 2011;46:439-443. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Novais EN, Maranho DA, Kim YJ, Kiapour A. Age- and sex-specific morphologic variations of capital femoral epiphysis growth in children and adolescents without hip disorders. Orthop J Sports Med. 2018;6:2325967118781579. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Novais EN, Maranho DA, Vairagade A, Kim YJ, Kiapour A. Smaller epiphyseal tubercle and larger peripheral cupping in slipped capital femoral epiphysis compared with Healthy hips: a 3-dimensional computed tomography study. J Bone Joint Surg [Am]. 2019. [DOI] [PubMed] [Google Scholar]
- 29.Pihl M, Sonne-Holm S, Christoffersen JK, Wong C. Doctor's delay in diagnosis of slipped capital femoral epiphysis. Dan Med J. 2014;61:A4905. [PubMed] [Google Scholar]
- 30.Pinkowsky GJ, Hennrikus WL. Klein line on the anteroposterior radiograph is not a sensitive diagnostic radiologic test for slipped capital femoral epiphysis. J Pediatr. 2013;162:804-807. [DOI] [PubMed] [Google Scholar]
- 31.Rahme D, Comley A, Foster B, Cundy P. Consequences of diagnostic delays in slipped capital femoral epiphysis. J Pediatr Orthop B. 2006;15:93-97. [DOI] [PubMed] [Google Scholar]
- 32.Scheuer L, Black S, Christie A. The lower limb. In: Scheuer L, Black S, Christie A, ed. Developmental Juvenile Osteology. San Diego, California: Elvesier Academic Press; 2000:374-467. [Google Scholar]
- 33.Schur MD, Andras LM, Broom AM, Barrett KK, Bowman CA, Luther H, Goldstein RY, Fletcher ND, Millis MB, Runner R, Skaggs DL. Continuing delay in the diagnosis of slipped capital femoral epiphysis. J Pediatr. 2016;177:250-254. [DOI] [PubMed] [Google Scholar]
- 34.Skaggs DL, Roy AK, Vitale MG, Pfiefer C, Baird G, Femino D, Kay RM. Quality of evaluation and management of children requiring timely orthopaedic surgery before admission to a tertiary pediatric facility. J Pediatr Orthop. 2002;22:265-267. [PubMed] [Google Scholar]
- 35.Tayton K. Does the upper femoral epiphysis slip or rotate? J Bone Joint Surg Br. 2007;89:1402-1406. [DOI] [PubMed] [Google Scholar]
- 36.Tayton K. The epiphyseal tubercle in adolescent hips. Acta Orthop. 2009;80:416-419. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Tins B, Cassar-Pullicino V, McCall I. The role of pre-treatment MRI in established cases of slipped capital femoral epiphysis. Eur J Radiol. 2009;70:570-578. [DOI] [PubMed] [Google Scholar]
- 38.Umans H, Liebling MS, Moy L, Haramati N, Macy NJ, Pritzker HA. Slipped capital femoral epiphysis: a physeal lesion diagnosed by MRI, with radiographic and CT correlation. Skeletal Radiol. 1998;27:139-144. [DOI] [PubMed] [Google Scholar]
- 39.Wensaas A, Wiig O, Hellund JC, Khoshnewiszadeh B, Terjesen T. Magnetic resonance imaging at primary diagnosis cannot predict subsequent contralateral slip in slipped capital femoral epiphysis. Skeletal Radiol. 2017;46:1687-1694. [DOI] [PubMed] [Google Scholar]
- 40.Witbreuk M, van Kemenade FJ, van der Sluijs JA, Jansma EP, Rotteveel J, van Royen BJ. Slipped capital femoral epiphysis and its association with endocrine, metabolic and chronic diseases: a systematic review of the literature. J Child Orthop. 2013;7:213-223. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Zbojniewicz AM, Laor T. Focal Periphyseal Edema (FOPE) zone on MRI of the adolescent knee: a potentially painful manifestation of physiologic physeal fusion? AJR Am J Roentgenol. 2011;197:998-1004. [DOI] [PubMed] [Google Scholar]