Forensic Sci Med Pathol DOI 10.1007/s12024-014-9559-2
ORIGINAL ARTICLE
The use of magnetic resonance imaging to examine ossification of the proximal tibial epiphysis for forensic age estimation in living individuals Jan Alexander Kra¨mer • Sven Schmidt Kai-Uwe Ju¨rgens • Markus Lentschig • Andreas Schmeling • Volker Vieth
•
Accepted: 12 March 2014 Ó Springer Science+Business Media New York 2014
Abstract The establishment of radiation-free examination procedures in the field of forensic age diagnostics in living persons is to be considered of special scientific interest so as to minimize necessary exposure to X-rays while facilitating additional assessment of skeletal development in all cases. To this end, the advantages offered by magnetic resonance imaging in securing a practical application which is as unrestricted and complication-free as possible should be among the methods exploited in investigating such indicators of skeletal maturity. Within the framework of a retrospective study, we investigated the ossification status of the proximal tibial epiphysis on the MRI scans of 124 females and 166 males aged between 10 and 30 years. All the images had been generated on a 3.0 T scanner using a T1-weighted turbo spin-echo sequence. When evaluating the ossification stage, a combination of modified classifications proposed by Schmeling et al. and by Kellinghaus et al. was used. The statistical evaluation included calculation of a variety of measures to describe specific ossification stages as well as kappa coefficients to assess intra- and inter-observer agreement on diagnoses of
individual stages. In forensic contexts, completion of the 14th year of life can be adequately evidenced in females with an ossification stage IV according to Schmeling et al. and in males with an ossification stage III c according to Kellinghaus et al. or an ossification stage IV according to Schmeling et al. In forensic contexts, the presence of an ossification stage IV according to Schmeling et al. can prove that the age of 16 years has been exceeded only in the male sex, whereby for age estimation purposes the diagnosis should be in line with other skeletal maturity indicators. The results available displayed a high degree of intra- and inter-observer agreement. Examination of the ossification status of the proximal tibial epiphysis using magnetic resonance imaging represents an effective additional tool for use in radiation-free forensic age diagnostics in living persons. Keywords Forensic age diagnostics Skeletal age Tibia MRI
Introduction J. A. Kra¨mer and S. Schmidt contributed equally to this work. J. A. Kra¨mer V. Vieth Department of Clinical Radiology, University Hospital Mu¨nster, Albert-Schweitzer-Campus 1, 48149 Mu¨nster, Germany S. Schmidt (&) A. Schmeling Institute of Legal Medicine, University Hospital Mu¨nster, Ro¨ntgenstraße 23, 48149 Mu¨nster, Germany e-mail: [email protected] K.-U. Ju¨rgens M. Lentschig Center of Modern Diagnostics, ZEMODI, Schwachhauser Heerstraße 63 a, 28211 Bremen, Germany
Especially high demands are made on the dependability of age diagnoses made for legal purposes. To improve accuracy and enhance reliability, the Study Group on Forensic Age Diagnostics (AGFAD) recommends using a combination of results relating to a variety of maturation systems [1, 2]. In particular, to provide evidence that a certain age has been reached for use in court, it is indispensable to include indicators of skeletal maturation in addition to a variety of characteristics of sexual and dental development. According to the current state of scientific knowledge, the use of computed tomography to monitor the ossification status of the medial clavicular epiphyses is particularly
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suited to providing sufficiently reliable evidence that age limits beyond the 17th year of life have been exceeded [3, 4]. Unlike age estimations with clinical indications, however, such examinations often face a lack of legal support in many areas of the law for X-ray diagnostic procedures to be performed [5]. This conflict, which is crucial to advisory age estimation practice, has provided considerable impetus to scientific efforts to establish radiation-free methods of evaluating skeletal age. In recent years, the use of ultrasound diagnostics to assess skeletal changes caused by maturation for the purpose of forming expert opinions has been studied as a cheap and generally accessible procedure [6–14]. However, any practical applicability of skeletal sonography in a forensic context faces the major obstacle that the interpretation of findings is highly dependent upon the experience of the examiner in question as well as its inadequate potential for objective documentation. For this reason, among others, a number of authors have directed most of their attention toward investigating the applicability of magnetic resonance imaging in determining skeletal maturity. The basic suitability of this imaging procedure in providing evidence of the indicators of maturity of the hand skeleton [15–17] and the clavicle [18–20] recommended by AGFAD have meanwhile been demonstrated. Currently, however, it is also hoped that it will be possible to expand the diagnostic spectrum by integrating maturity-dependent changes to other parts of the skeleton for which an unrestricted and complication-free examination based on magnetic resonance imaging can be secured. Due to its large dimensions and its distance from the trunk, the proximal tibial epiphysis is particularly well suited for this purpose. However, the potential of MRI scans for evaluating epiphyseal ossification of the proximal tibia has scarcely been studied [21–24]. The authors of the two publications available in relation to the forensic area of application differed significantly in some of the results which they achieved [22, 23]. The present study aims to check these discrepant results.
Materials and methods The present study is based on the retrospective analysis of sequences of MRI scans of the knee joint made between July 2010 and December 2012 at the Center of Modern Diagnostics (ZEMODI) in Bremen, Germany. The project was supported by a positive vote of the ethics commission ¨ rztekammer Bremen). of the Bremen Medical Council (A The initial group of patients selected comprised a total of 304 persons aged from 10 to 30 years in whose cases imaging diagnostics became necessary due to traumatic and/or degenerative changes to the joint or to investigate
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Table 1 Case group figures (n = 290) Chronological age (in years)
Female study participants
Male study participants
10
2
3
11
4
0
12
5
6
13
6
5
14
5
6
15
2
9
16 17
9 6
8 7
18
5
7
19
6
7
20
4
9
21
9
13
22
6
8
23
11
9
24
7
10
25
6
12
26
5
9
27
4
12
28
6
8
29
8
8
30
8
10
124
166
R
pain in the knee joint. Due to inadequate clinical information on the one hand, and in view of existing anamnestic indications of the presence of a systemic or a neoplastic disorder (juvenile idiopathic arthritis, rheumatoid arthritis, acute myeloid leukemia) as well as steroid treatment or chemotherapy on the other, the imaging material in 14 of these cases had to be excluded from further evaluation. Table 1 displays the case group data of the remaining 124 females and 166 males organized by chronological age and divided by sex. The MRI diagnostics on which the study is based were performed on two 3.0 T scanners (MAGNETOM Verio, Siemens, Germany; Biograph mMR, Siemens, Germany) with comparable imaging properties using a 15-channel knee coil (high-resolution 15ch Tx/Rx knee coil, QED, USA). For analysis of the scans, a T1-weighted turbo spinecho (T1-TSE) sequence in sagittal orientation was used (TR: 783 ms; TE: 13 ms; matrix: 512 (90 %); FoV: 180 mm; slice thickness: 3.0 mm; FA: 160°; voxel size: 0.4 9 0.4 9 3.0 mm; scan time: 1 min 57 s). A workstation (Multi Modality Work Place, Siemens, Germany) with a high-resolution diagnostic monitor was available for evaluation of the MRI scans. In the course of blinded examinations, all the scans were reviewed by a radiologist who undertook repeated
Forensic Sci Med Pathol Table 2 Projectional radiography stage classification of ossification of the medial clavicular epiphysis according to Schmeling et al. [25] Stage
Description
I
The ossification center has not yet ossified
II
The ossification center has ossified, the epiphyseal cartilage has not ossified
III IV
The epiphyseal cartilage is partially ossified The epiphyseal cartilage is fully ossified
V
The epiphyseal cartilage has fused completely and the epiphyseal scar is no longer visible
Table 3 Computed tomographic differentiation of ossification stages II and III of the medial clavicular epiphysis according to Kellinghaus et al. [3] Stage
Description
II a
The lengthwise epiphyseal measurement is one-third or less compared to the widthwise measurement of the metaphyseal ending The lengthwise epiphyseal measurement is between one-third and two-thirds compared to the widthwise measurement of the metaphyseal ending
II b
II c
The lengthwise epiphyseal measurement is over two-thirds compared to the widthwise measurement of the metaphyseal ending
III a
The epiphyseal–metaphyseal fusion completes one-third or less of the former gap between epiphysis and metaphysis
III b
The epiphyseal–metaphyseal fusion completes between onethird and two-thirds of the former gap between epiphysis and metaphysis
III c
The epiphyseal–metaphyseal fusion completes over twothirds of the former gap between epiphysis and metaphysis
assessment of a randomly selected subset of 10 % of the study population after an interval of 3 months. Moreover, a further independent assessment of this subset was performed by a second radiologist. Assessment of the ossification stage of the proximal tibial epiphysis was performed based on the classification system for the main stages of ossification of the medial clavicular epiphysis proposed by Schmeling et al. (Table 2 [25] ) as well as the classification system for the substages of ossification of the medial clavicular epiphysis put forward by
Kellinghaus et al. (Table 3 [3] ). Figure 1 shows a diagrammatic representation of the ossification stages. To determine the ossification stage, all the MRI slices were evaluated at all times. For stages 1, 2 (including substages 2a, 2b, 2c) and 3 (including substages 3a, 3b, 3c) the slice with the most developed femoral epiphysis was decisive in each case. The requirement for assignment to ossification stage 4 was full ossification of the epiphyseal plate in all slices and an identifiable epiphyseal scar in at least one slice. An ossification stage 5 is present when the epiphyseal plate is fully ossified in all the slices and no epiphyseal scar is definable in any of the slices. Statistical analysis of the data was performed using SPSS 16.0.1 (IBM SPSS Statistics) software. Calculation of a variety of statistical measures of location and dispersion (minimum, maximum, mean value with standard deviation, median with lower and upper quartile) served as the basis for describing the ossification stages ascertained in the material studied. For the statistical interpretation of intra- and inter-observer agreement in relation to the stage diagnoses, we calculated the relevant kappa coefficients.
Results Figures 2, 3, 4, 5, and 6 depict the characteristic MRI findings in relation to ossification stages IIc, IIIa, IIIb, IIIc and IV of the proximal tibial epiphysis which were detected in the study population. Ossification stages I, IIa, IIb and V were not detected among our test persons. In all the cases included in the investigation it was possible to determine the ossification stage of the proximal tibial epiphysis using magnetic resonance imaging. Tables 6 and 7 display the measures of location and dispersion calculated for the statistical characterization of the determined ossification stages, divided by sex. With increasing ossification stages of the proximal tibial epiphysis, the measures for both the female and the male sex display a rise in the mean values and medians of the chronological age of the individual, whereby a tendency toward a maturity advantage of female test persons as compared to males can be ascertained within the age interval seen as a whole.
Fig. 1 Diagrammatic representation of the ossification stages
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1
2 1
2
Fig. 2 Sagittal MRI sectional image of an ossification stage IIc of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. Patellae
Fig. 4 Sagittal MRI sectional image of an ossification stage IIIb of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked areas ossified parts of the epiphyseal cartilage
1
1 2
2
Fig. 5 Sagittal MRI sectional image of an ossification stage IIIc of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked areas ossified parts of the epiphyseal cartilage
Fig. 3 Sagittal MRI sectional image of an ossification stage IIIa of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked area ossified part of the epiphyseal cartilage
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Ossification stage IIc was detected in females before the age of 12, and in males before the age of 13, in all the age categories we considered. Ossification stage IIIa was found in females from the age of 11 until the age of 14, and in males from the age of 12 until the age of 15. Ossification stage IIIb was diagnosed in the females studied in only one
Forensic Sci Med Pathol
1
2
Fig. 6 Sagittal MRI sectional image of an ossification stage IV of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. Patellae
case: the individual concerned had reached the age of 14. The corresponding findings were ascertained among the males between the ages of 13 and 16. Ossification stage IIIc existed among female individuals from the age of 14 to the age of 18, and among male individuals from the age of 15 to the age of 19. In our study population, ossification stage IV was reached in females from the age of 15, and in males from the age of 16. Statistical analysis of the ossification stages determined twice in part of the study population yielded a kappa coefficient of 0.88 in relation to intra-observer agreement and a kappa coefficient of 0.85 in relation to inter-observer agreement.
Discussion Maturity-dependent morphological changes to the proximal tibia have been the focus of various clinical and anthropological studies for many years [26–32]. As a result, the information available today on the relevant individual developmental processes cover a comparatively broad age spectrum. Thus, the Pyle and Hoerr projectional radiography atlas indicates that fusion of the proximal epiphyseal plate of the tibia commences at the age of 13 years in females and 15.5 in males; the fusion process is completed
some 1.5 years later [30]. According to the results of various anatomical studies, complete epiphyseal fusion at the proximal tibia can be observed in females at the age of 18–19 years, and in males between the ages of 17 and 19 [26, 31, 33]. McKern and Steward confirm that complete entry of the entire population into this final ossification stage is not complete until the 23rd year of life [28]. When considering a possible cause for the more or less discrepant results of these studies, it is important to consider the different conceptual definitions used in connection with epiphyseal ossification, as some of these are reflected in diverse stage classifications [29]. Furthermore, as no comparative studies on age-dependent maturation of the proximal tibial epiphysis in one study population exist, evidence gained by scientific studies using a radiological and anatomical approach cannot be directly compared. This is a significant cause of the difficulty of utilizing currently accessible research results in dealing with future issues. This particularly applies to the very specific problems arising in the field of forensic age estimation. In recent years, forensic scientific interest has increasingly focused on establishing maturity indicators that are observable using magnetic resonance imaging, with the intention of facilitating diagnostic procedures to determine skeletal age in all relevant areas of the law. One of the research objectives is to combine the methodological advantages of MRI technology with the investigation of those skeletal elements which ensure that the process of practical application is as complication-free and unrestricted as possible. In this area, the long bones of the extremities play a special role. At present, only two systematic studies can be drawn upon in relation to the changes observable using magnetic resonance imaging during the epiphyseal maturation process at the proximal tibia [22, 23]. In a recently published retrospective study, Dedouit et al. [22] studied ossification of the proximal tibial epiphysis in 152 female and 138 male patients aged between 10 and 30 years who had to undergo an MRI examination of the knee joint due to existing pains. Patients with pathological changes to the knee or hormonal and/or systemic disorders were not included in the study. The sectional images were generated on a 1.5 T scanner (Intera, Philips, Netherlands) using a proton density-weighted fast spin echo (FSE) sequence. The findings, which were based in most cases on coronal image sequences, were used to calculate the intra- and inter-observer agreement of a radiologist and a forensic medical expert. They followed a five-stage classification of tibial epiphyseal ossification (Table 4 [22] ). Due to the MRI sequence used by Dedouit et al. [22], the results of this study are not comparable to our findings. Compared with other imaging methods, magnetic resonance imaging offers a range of potential for targeted contrast optimization. Thus, by selecting the
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Forensic Sci Med Pathol Table 4 Magnetic resonance imaging stage classification of ossification of the proximal tibial epiphysis according to Dedouit et al. [22]
Table 5 Magnetic resonance imaging categorization of ossification of the proximal tibial epiphysis according to Jopp et al. [23]
Stage
Description
Category
Description
I
Continuous horizontal cartilage signal intensity present between the metaphysis and the epiphysis, stripe-like, with a thickness greater than 1.5 mm and a multilaminar appearance (decreased signal intensity in the upper layer, increased signal intensity in the middle layer, and decreased signal intensity in the lower layer)
I
The epiphysis and diaphysis lie exactly over each other. The plate (cartilage strip/‘‘epiphyseal plate’’) shows up over the entire width of the growth plate (physis as a hypointense strip between the metaphysis and the epiphysis [open plate])
II
II
Continuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness greater than 1.5 mm, with increased signal intensity but without a multilaminar appearance
III
Continuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness less than 1.5 mm, with increased signal intensity
The cartilage strip is partially replaced by bone. Maturation begins in the central area of the plate and progresses toward the peripheries. At the medial and lateral periphery the cartilaginous plate can still be seen. The cartilage strip becomes narrower and more hyperintense (centrally closed plate)
III
The epiphysis and diaphysis are joined by bone. The growth plate is partially visible as a thin, dark strip (epiphyseal scar; closed plate)
IV
Discontinuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness less than 1.5 mm, with discontinuous increased signal intensity
V
No increased signal intensity between the metaphysis and the epiphysis
weighting of a measuring sequence a characteristic distribution of the signal intensities of different tissues can be achieved. However, as no standard values for specific tissues exist and details of the tissue composition of the maturing epiphyseal plate which provides the contrast are not reliably known, the findings of different studies gained using different MRI weightings cannot be easily compared. The T1-weighted sequences on which our investigations were based frequently display good indirect imaging of bone. For this reason, they are potentially particularly suited to providing very early evidence of initial epiphyseal ossification. With the aid of proton-weighted images on which the study by Dedouit et al. [22] is based, soft-tissue structures such as the epiphyseal cartilage can be represented. Based on the studies existing to date, it appears possible that the ossification stages defined by Dedouit et al. [22] display different chronological processes from the stages used by ourselves. As early as 2010, Jopp et al. [23] analyzed the age dependence of epiphyseal ossification at the proximal tibia using a prospective approach. The study was based on scans of 41 healthy males aged from 15 to 19 years. The Table 6 Ossification stages in relation to age for female test persons (expressed in years)
Stage
Minimum
Maximum
Mean value; standard deviation
Lower quartile; median; upper quartile
II c
3
10.1
12.8
11.2 ± 1.4
–; 10.7; –
III a
15
11.4
14.2
12.8 ± 0.9
12.0; 12.7; 13.5
III b
1
–
–
14.2; –
–; 14.2; –
III c
9
14.3
18.4
16.0 ± 1.4
14.7; 16.1; 17.3
96
15.6
30.8
23.7 ± 4.3
20.4; 23.6; 27.7
IV
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Number of cases
images were generated on a 1.5 T scanner and a 3.0 T scanner (Gyroscan Intera, Philips, Netherlands). A T1weighted turbo spin-echo (T1-TSE) sequence in coronal and sagittal section was available for evaluation. Two radiologists, independently of each other, undertook categorization of the status of epiphyseal ossification based on a three-tier model (Table 5 [23] ). As significant points of criticism relative to the study published by Jopp et al., the authors themselves named the absence of female test persons as well as the small number of cases on which the study was based. The partial congruence of the stage classifications of epiphyseal ossification of the proximal tibia as well as the use of the same MRI weightings explain the similar age intervals of corresponding ossification stages in our study as compared with the results of the investigation by Jopp et al. [23]. In summary, on the basis of the available data, it is possible to confirm the insights gained from numerous other studies according to which the overall maturation process of the proximal tibial epiphysis is completed earlier in females than in males [22]. To provide adequate proof that an individual has reached the age of 14, which is legally significant in many countries [34], only the diagnosis of ossification stage IV is applicable in females, as the results of our study show that this cannot be ascertained before a chronological age of 15.6 years. In relation to ossification stages IIIb and
Forensic Sci Med Pathol Table 7 Ossification stages in relation to age for male test persons (expressed in years)
Stage
Number of cases
Minimum
Mean value; standard deviation
Lower quartile; median; upper quartile
II c
7
10.1
13.6
11.9 ± 1.3
10.8; 12.2; 12.9
III a
16
12.2
15.8
14.4 ± 1.2
13.5; 14.7; 15.4
III b
3
13.9
16.2
15.1 ± 1.2
–; 15.1; –
16
15.0
19.5
16.7 ± 1.3
15.7; 16.6; 17.1
124
16.3
30.8
24.5 ± 3.8
21.4; 24.7; 27.5
III c IV
IIIc, the minimum ages of 14.2 and 14.3 years respectively for females are based on a very small number of cases and should therefore not be used as the basis of decision-making in forensic contexts. By contrast, in the light of a lower interval boundary of 15.0 years in males, presence of an ossification stage IIIc already supports a diagnosis that the age of 14 years has been reached (Tables 6, 7). While the statistical measures we determined do not provide evidence on assured completion of the 16th year of life in females, this appears, in principle, possible for male persons with ossification stage IV, thus confirming the published results of Jopp et al. However, as there is only a slight difference between the legally relevant age limit of 16 years and the minimum age of the corresponding frequency distribution, this should only be used in age estimation practice in combination with other skeletal maturity indicators. An examination of epiphyseal ossification of the proximal tibia using our MRI protocol is unsuitable for verifying whether an age limit above the age of 16 has been reached. The kappa coefficients calculated for our study material attest to an overall good to very good degree of agreement of the diagnostic results reached by one and/or both examiners. Diagnoses of skeletal age achievable using an MRI examination of the proximal tibial epiphysis can thus be considered reliable and largely independent of the observer. However, contrary to the assertion made by Dedouit et al. [22], the procedure is, in our judgment, scarcely suitable for inexperienced examiners of any specialization. One limitation of our investigation is the fact that, due to the retrospective study design, it was only possible to evaluate one MRI sequence for each subject. It has been proposed for future prospective studies that, in addition to T1-weighted sequences, water-sensitive, fat-suppressed sequences should be generated to represent the epiphyseal cartilage and included in the evaluation.
Key points 1.
Maximum
Verification of the ossification status of the proximal tibial epiphysis using magnetic resonance imaging is a suitable tool for forensic age estimation practice.
2.
3.
4.
Examination of the proximal tibial epiphysis using magnetic resonance imaging makes it possible, in principle, to include a characteristic of skeletal maturity in all areas of application of advisory age estimation practice with due regard to the demands of radiation hygiene. Diagnoses of an ossification stage IIIc according to Kellinghaus et al. in males and an ossification stage IV according to Schmeling et al. in both females and males provide sufficiently reliable evidence of completion of the 14th year of life. Diagnosis of an ossification stage IV according to Schmeling et al. in males provides sufficiently reliable evidence of completion of the 16th year of life. The diagnosis should be in keeping with other indicators of skeletal maturity.
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ORIGINAL ARTICLE
The use of magnetic resonance imaging to examine ossification of the proximal tibial epiphysis for forensic age estimation in living individuals Jan Alexander Kra¨mer • Sven Schmidt Kai-Uwe Ju¨rgens • Markus Lentschig • Andreas Schmeling • Volker Vieth
•
Accepted: 12 March 2014 Ó Springer Science+Business Media New York 2014
Abstract The establishment of radiation-free examination procedures in the field of forensic age diagnostics in living persons is to be considered of special scientific interest so as to minimize necessary exposure to X-rays while facilitating additional assessment of skeletal development in all cases. To this end, the advantages offered by magnetic resonance imaging in securing a practical application which is as unrestricted and complication-free as possible should be among the methods exploited in investigating such indicators of skeletal maturity. Within the framework of a retrospective study, we investigated the ossification status of the proximal tibial epiphysis on the MRI scans of 124 females and 166 males aged between 10 and 30 years. All the images had been generated on a 3.0 T scanner using a T1-weighted turbo spin-echo sequence. When evaluating the ossification stage, a combination of modified classifications proposed by Schmeling et al. and by Kellinghaus et al. was used. The statistical evaluation included calculation of a variety of measures to describe specific ossification stages as well as kappa coefficients to assess intra- and inter-observer agreement on diagnoses of
individual stages. In forensic contexts, completion of the 14th year of life can be adequately evidenced in females with an ossification stage IV according to Schmeling et al. and in males with an ossification stage III c according to Kellinghaus et al. or an ossification stage IV according to Schmeling et al. In forensic contexts, the presence of an ossification stage IV according to Schmeling et al. can prove that the age of 16 years has been exceeded only in the male sex, whereby for age estimation purposes the diagnosis should be in line with other skeletal maturity indicators. The results available displayed a high degree of intra- and inter-observer agreement. Examination of the ossification status of the proximal tibial epiphysis using magnetic resonance imaging represents an effective additional tool for use in radiation-free forensic age diagnostics in living persons. Keywords Forensic age diagnostics Skeletal age Tibia MRI
Introduction J. A. Kra¨mer and S. Schmidt contributed equally to this work. J. A. Kra¨mer V. Vieth Department of Clinical Radiology, University Hospital Mu¨nster, Albert-Schweitzer-Campus 1, 48149 Mu¨nster, Germany S. Schmidt (&) A. Schmeling Institute of Legal Medicine, University Hospital Mu¨nster, Ro¨ntgenstraße 23, 48149 Mu¨nster, Germany e-mail: [email protected] K.-U. Ju¨rgens M. Lentschig Center of Modern Diagnostics, ZEMODI, Schwachhauser Heerstraße 63 a, 28211 Bremen, Germany
Especially high demands are made on the dependability of age diagnoses made for legal purposes. To improve accuracy and enhance reliability, the Study Group on Forensic Age Diagnostics (AGFAD) recommends using a combination of results relating to a variety of maturation systems [1, 2]. In particular, to provide evidence that a certain age has been reached for use in court, it is indispensable to include indicators of skeletal maturation in addition to a variety of characteristics of sexual and dental development. According to the current state of scientific knowledge, the use of computed tomography to monitor the ossification status of the medial clavicular epiphyses is particularly
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suited to providing sufficiently reliable evidence that age limits beyond the 17th year of life have been exceeded [3, 4]. Unlike age estimations with clinical indications, however, such examinations often face a lack of legal support in many areas of the law for X-ray diagnostic procedures to be performed [5]. This conflict, which is crucial to advisory age estimation practice, has provided considerable impetus to scientific efforts to establish radiation-free methods of evaluating skeletal age. In recent years, the use of ultrasound diagnostics to assess skeletal changes caused by maturation for the purpose of forming expert opinions has been studied as a cheap and generally accessible procedure [6–14]. However, any practical applicability of skeletal sonography in a forensic context faces the major obstacle that the interpretation of findings is highly dependent upon the experience of the examiner in question as well as its inadequate potential for objective documentation. For this reason, among others, a number of authors have directed most of their attention toward investigating the applicability of magnetic resonance imaging in determining skeletal maturity. The basic suitability of this imaging procedure in providing evidence of the indicators of maturity of the hand skeleton [15–17] and the clavicle [18–20] recommended by AGFAD have meanwhile been demonstrated. Currently, however, it is also hoped that it will be possible to expand the diagnostic spectrum by integrating maturity-dependent changes to other parts of the skeleton for which an unrestricted and complication-free examination based on magnetic resonance imaging can be secured. Due to its large dimensions and its distance from the trunk, the proximal tibial epiphysis is particularly well suited for this purpose. However, the potential of MRI scans for evaluating epiphyseal ossification of the proximal tibia has scarcely been studied [21–24]. The authors of the two publications available in relation to the forensic area of application differed significantly in some of the results which they achieved [22, 23]. The present study aims to check these discrepant results.
Materials and methods The present study is based on the retrospective analysis of sequences of MRI scans of the knee joint made between July 2010 and December 2012 at the Center of Modern Diagnostics (ZEMODI) in Bremen, Germany. The project was supported by a positive vote of the ethics commission ¨ rztekammer Bremen). of the Bremen Medical Council (A The initial group of patients selected comprised a total of 304 persons aged from 10 to 30 years in whose cases imaging diagnostics became necessary due to traumatic and/or degenerative changes to the joint or to investigate
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Table 1 Case group figures (n = 290) Chronological age (in years)
Female study participants
Male study participants
10
2
3
11
4
0
12
5
6
13
6
5
14
5
6
15
2
9
16 17
9 6
8 7
18
5
7
19
6
7
20
4
9
21
9
13
22
6
8
23
11
9
24
7
10
25
6
12
26
5
9
27
4
12
28
6
8
29
8
8
30
8
10
124
166
R
pain in the knee joint. Due to inadequate clinical information on the one hand, and in view of existing anamnestic indications of the presence of a systemic or a neoplastic disorder (juvenile idiopathic arthritis, rheumatoid arthritis, acute myeloid leukemia) as well as steroid treatment or chemotherapy on the other, the imaging material in 14 of these cases had to be excluded from further evaluation. Table 1 displays the case group data of the remaining 124 females and 166 males organized by chronological age and divided by sex. The MRI diagnostics on which the study is based were performed on two 3.0 T scanners (MAGNETOM Verio, Siemens, Germany; Biograph mMR, Siemens, Germany) with comparable imaging properties using a 15-channel knee coil (high-resolution 15ch Tx/Rx knee coil, QED, USA). For analysis of the scans, a T1-weighted turbo spinecho (T1-TSE) sequence in sagittal orientation was used (TR: 783 ms; TE: 13 ms; matrix: 512 (90 %); FoV: 180 mm; slice thickness: 3.0 mm; FA: 160°; voxel size: 0.4 9 0.4 9 3.0 mm; scan time: 1 min 57 s). A workstation (Multi Modality Work Place, Siemens, Germany) with a high-resolution diagnostic monitor was available for evaluation of the MRI scans. In the course of blinded examinations, all the scans were reviewed by a radiologist who undertook repeated
Forensic Sci Med Pathol Table 2 Projectional radiography stage classification of ossification of the medial clavicular epiphysis according to Schmeling et al. [25] Stage
Description
I
The ossification center has not yet ossified
II
The ossification center has ossified, the epiphyseal cartilage has not ossified
III IV
The epiphyseal cartilage is partially ossified The epiphyseal cartilage is fully ossified
V
The epiphyseal cartilage has fused completely and the epiphyseal scar is no longer visible
Table 3 Computed tomographic differentiation of ossification stages II and III of the medial clavicular epiphysis according to Kellinghaus et al. [3] Stage
Description
II a
The lengthwise epiphyseal measurement is one-third or less compared to the widthwise measurement of the metaphyseal ending The lengthwise epiphyseal measurement is between one-third and two-thirds compared to the widthwise measurement of the metaphyseal ending
II b
II c
The lengthwise epiphyseal measurement is over two-thirds compared to the widthwise measurement of the metaphyseal ending
III a
The epiphyseal–metaphyseal fusion completes one-third or less of the former gap between epiphysis and metaphysis
III b
The epiphyseal–metaphyseal fusion completes between onethird and two-thirds of the former gap between epiphysis and metaphysis
III c
The epiphyseal–metaphyseal fusion completes over twothirds of the former gap between epiphysis and metaphysis
assessment of a randomly selected subset of 10 % of the study population after an interval of 3 months. Moreover, a further independent assessment of this subset was performed by a second radiologist. Assessment of the ossification stage of the proximal tibial epiphysis was performed based on the classification system for the main stages of ossification of the medial clavicular epiphysis proposed by Schmeling et al. (Table 2 [25] ) as well as the classification system for the substages of ossification of the medial clavicular epiphysis put forward by
Kellinghaus et al. (Table 3 [3] ). Figure 1 shows a diagrammatic representation of the ossification stages. To determine the ossification stage, all the MRI slices were evaluated at all times. For stages 1, 2 (including substages 2a, 2b, 2c) and 3 (including substages 3a, 3b, 3c) the slice with the most developed femoral epiphysis was decisive in each case. The requirement for assignment to ossification stage 4 was full ossification of the epiphyseal plate in all slices and an identifiable epiphyseal scar in at least one slice. An ossification stage 5 is present when the epiphyseal plate is fully ossified in all the slices and no epiphyseal scar is definable in any of the slices. Statistical analysis of the data was performed using SPSS 16.0.1 (IBM SPSS Statistics) software. Calculation of a variety of statistical measures of location and dispersion (minimum, maximum, mean value with standard deviation, median with lower and upper quartile) served as the basis for describing the ossification stages ascertained in the material studied. For the statistical interpretation of intra- and inter-observer agreement in relation to the stage diagnoses, we calculated the relevant kappa coefficients.
Results Figures 2, 3, 4, 5, and 6 depict the characteristic MRI findings in relation to ossification stages IIc, IIIa, IIIb, IIIc and IV of the proximal tibial epiphysis which were detected in the study population. Ossification stages I, IIa, IIb and V were not detected among our test persons. In all the cases included in the investigation it was possible to determine the ossification stage of the proximal tibial epiphysis using magnetic resonance imaging. Tables 6 and 7 display the measures of location and dispersion calculated for the statistical characterization of the determined ossification stages, divided by sex. With increasing ossification stages of the proximal tibial epiphysis, the measures for both the female and the male sex display a rise in the mean values and medians of the chronological age of the individual, whereby a tendency toward a maturity advantage of female test persons as compared to males can be ascertained within the age interval seen as a whole.
Fig. 1 Diagrammatic representation of the ossification stages
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1
2 1
2
Fig. 2 Sagittal MRI sectional image of an ossification stage IIc of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. Patellae
Fig. 4 Sagittal MRI sectional image of an ossification stage IIIb of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked areas ossified parts of the epiphyseal cartilage
1
1 2
2
Fig. 5 Sagittal MRI sectional image of an ossification stage IIIc of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked areas ossified parts of the epiphyseal cartilage
Fig. 3 Sagittal MRI sectional image of an ossification stage IIIa of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. patellae, marked area ossified part of the epiphyseal cartilage
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Ossification stage IIc was detected in females before the age of 12, and in males before the age of 13, in all the age categories we considered. Ossification stage IIIa was found in females from the age of 11 until the age of 14, and in males from the age of 12 until the age of 15. Ossification stage IIIb was diagnosed in the females studied in only one
Forensic Sci Med Pathol
1
2
Fig. 6 Sagittal MRI sectional image of an ossification stage IV of the proximal tibial epiphysis; 1 femoral epiphysis, 2 tibial epiphysis, arrow Lig. Patellae
case: the individual concerned had reached the age of 14. The corresponding findings were ascertained among the males between the ages of 13 and 16. Ossification stage IIIc existed among female individuals from the age of 14 to the age of 18, and among male individuals from the age of 15 to the age of 19. In our study population, ossification stage IV was reached in females from the age of 15, and in males from the age of 16. Statistical analysis of the ossification stages determined twice in part of the study population yielded a kappa coefficient of 0.88 in relation to intra-observer agreement and a kappa coefficient of 0.85 in relation to inter-observer agreement.
Discussion Maturity-dependent morphological changes to the proximal tibia have been the focus of various clinical and anthropological studies for many years [26–32]. As a result, the information available today on the relevant individual developmental processes cover a comparatively broad age spectrum. Thus, the Pyle and Hoerr projectional radiography atlas indicates that fusion of the proximal epiphyseal plate of the tibia commences at the age of 13 years in females and 15.5 in males; the fusion process is completed
some 1.5 years later [30]. According to the results of various anatomical studies, complete epiphyseal fusion at the proximal tibia can be observed in females at the age of 18–19 years, and in males between the ages of 17 and 19 [26, 31, 33]. McKern and Steward confirm that complete entry of the entire population into this final ossification stage is not complete until the 23rd year of life [28]. When considering a possible cause for the more or less discrepant results of these studies, it is important to consider the different conceptual definitions used in connection with epiphyseal ossification, as some of these are reflected in diverse stage classifications [29]. Furthermore, as no comparative studies on age-dependent maturation of the proximal tibial epiphysis in one study population exist, evidence gained by scientific studies using a radiological and anatomical approach cannot be directly compared. This is a significant cause of the difficulty of utilizing currently accessible research results in dealing with future issues. This particularly applies to the very specific problems arising in the field of forensic age estimation. In recent years, forensic scientific interest has increasingly focused on establishing maturity indicators that are observable using magnetic resonance imaging, with the intention of facilitating diagnostic procedures to determine skeletal age in all relevant areas of the law. One of the research objectives is to combine the methodological advantages of MRI technology with the investigation of those skeletal elements which ensure that the process of practical application is as complication-free and unrestricted as possible. In this area, the long bones of the extremities play a special role. At present, only two systematic studies can be drawn upon in relation to the changes observable using magnetic resonance imaging during the epiphyseal maturation process at the proximal tibia [22, 23]. In a recently published retrospective study, Dedouit et al. [22] studied ossification of the proximal tibial epiphysis in 152 female and 138 male patients aged between 10 and 30 years who had to undergo an MRI examination of the knee joint due to existing pains. Patients with pathological changes to the knee or hormonal and/or systemic disorders were not included in the study. The sectional images were generated on a 1.5 T scanner (Intera, Philips, Netherlands) using a proton density-weighted fast spin echo (FSE) sequence. The findings, which were based in most cases on coronal image sequences, were used to calculate the intra- and inter-observer agreement of a radiologist and a forensic medical expert. They followed a five-stage classification of tibial epiphyseal ossification (Table 4 [22] ). Due to the MRI sequence used by Dedouit et al. [22], the results of this study are not comparable to our findings. Compared with other imaging methods, magnetic resonance imaging offers a range of potential for targeted contrast optimization. Thus, by selecting the
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Forensic Sci Med Pathol Table 4 Magnetic resonance imaging stage classification of ossification of the proximal tibial epiphysis according to Dedouit et al. [22]
Table 5 Magnetic resonance imaging categorization of ossification of the proximal tibial epiphysis according to Jopp et al. [23]
Stage
Description
Category
Description
I
Continuous horizontal cartilage signal intensity present between the metaphysis and the epiphysis, stripe-like, with a thickness greater than 1.5 mm and a multilaminar appearance (decreased signal intensity in the upper layer, increased signal intensity in the middle layer, and decreased signal intensity in the lower layer)
I
The epiphysis and diaphysis lie exactly over each other. The plate (cartilage strip/‘‘epiphyseal plate’’) shows up over the entire width of the growth plate (physis as a hypointense strip between the metaphysis and the epiphysis [open plate])
II
II
Continuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness greater than 1.5 mm, with increased signal intensity but without a multilaminar appearance
III
Continuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness less than 1.5 mm, with increased signal intensity
The cartilage strip is partially replaced by bone. Maturation begins in the central area of the plate and progresses toward the peripheries. At the medial and lateral periphery the cartilaginous plate can still be seen. The cartilage strip becomes narrower and more hyperintense (centrally closed plate)
III
The epiphysis and diaphysis are joined by bone. The growth plate is partially visible as a thin, dark strip (epiphyseal scar; closed plate)
IV
Discontinuous horizontal linear cartilage signal intensity present between the metaphysis and the epiphysis, with a thickness less than 1.5 mm, with discontinuous increased signal intensity
V
No increased signal intensity between the metaphysis and the epiphysis
weighting of a measuring sequence a characteristic distribution of the signal intensities of different tissues can be achieved. However, as no standard values for specific tissues exist and details of the tissue composition of the maturing epiphyseal plate which provides the contrast are not reliably known, the findings of different studies gained using different MRI weightings cannot be easily compared. The T1-weighted sequences on which our investigations were based frequently display good indirect imaging of bone. For this reason, they are potentially particularly suited to providing very early evidence of initial epiphyseal ossification. With the aid of proton-weighted images on which the study by Dedouit et al. [22] is based, soft-tissue structures such as the epiphyseal cartilage can be represented. Based on the studies existing to date, it appears possible that the ossification stages defined by Dedouit et al. [22] display different chronological processes from the stages used by ourselves. As early as 2010, Jopp et al. [23] analyzed the age dependence of epiphyseal ossification at the proximal tibia using a prospective approach. The study was based on scans of 41 healthy males aged from 15 to 19 years. The Table 6 Ossification stages in relation to age for female test persons (expressed in years)
Stage
Minimum
Maximum
Mean value; standard deviation
Lower quartile; median; upper quartile
II c
3
10.1
12.8
11.2 ± 1.4
–; 10.7; –
III a
15
11.4
14.2
12.8 ± 0.9
12.0; 12.7; 13.5
III b
1
–
–
14.2; –
–; 14.2; –
III c
9
14.3
18.4
16.0 ± 1.4
14.7; 16.1; 17.3
96
15.6
30.8
23.7 ± 4.3
20.4; 23.6; 27.7
IV
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Number of cases
images were generated on a 1.5 T scanner and a 3.0 T scanner (Gyroscan Intera, Philips, Netherlands). A T1weighted turbo spin-echo (T1-TSE) sequence in coronal and sagittal section was available for evaluation. Two radiologists, independently of each other, undertook categorization of the status of epiphyseal ossification based on a three-tier model (Table 5 [23] ). As significant points of criticism relative to the study published by Jopp et al., the authors themselves named the absence of female test persons as well as the small number of cases on which the study was based. The partial congruence of the stage classifications of epiphyseal ossification of the proximal tibia as well as the use of the same MRI weightings explain the similar age intervals of corresponding ossification stages in our study as compared with the results of the investigation by Jopp et al. [23]. In summary, on the basis of the available data, it is possible to confirm the insights gained from numerous other studies according to which the overall maturation process of the proximal tibial epiphysis is completed earlier in females than in males [22]. To provide adequate proof that an individual has reached the age of 14, which is legally significant in many countries [34], only the diagnosis of ossification stage IV is applicable in females, as the results of our study show that this cannot be ascertained before a chronological age of 15.6 years. In relation to ossification stages IIIb and
Forensic Sci Med Pathol Table 7 Ossification stages in relation to age for male test persons (expressed in years)
Stage
Number of cases
Minimum
Mean value; standard deviation
Lower quartile; median; upper quartile
II c
7
10.1
13.6
11.9 ± 1.3
10.8; 12.2; 12.9
III a
16
12.2
15.8
14.4 ± 1.2
13.5; 14.7; 15.4
III b
3
13.9
16.2
15.1 ± 1.2
–; 15.1; –
16
15.0
19.5
16.7 ± 1.3
15.7; 16.6; 17.1
124
16.3
30.8
24.5 ± 3.8
21.4; 24.7; 27.5
III c IV
IIIc, the minimum ages of 14.2 and 14.3 years respectively for females are based on a very small number of cases and should therefore not be used as the basis of decision-making in forensic contexts. By contrast, in the light of a lower interval boundary of 15.0 years in males, presence of an ossification stage IIIc already supports a diagnosis that the age of 14 years has been reached (Tables 6, 7). While the statistical measures we determined do not provide evidence on assured completion of the 16th year of life in females, this appears, in principle, possible for male persons with ossification stage IV, thus confirming the published results of Jopp et al. However, as there is only a slight difference between the legally relevant age limit of 16 years and the minimum age of the corresponding frequency distribution, this should only be used in age estimation practice in combination with other skeletal maturity indicators. An examination of epiphyseal ossification of the proximal tibia using our MRI protocol is unsuitable for verifying whether an age limit above the age of 16 has been reached. The kappa coefficients calculated for our study material attest to an overall good to very good degree of agreement of the diagnostic results reached by one and/or both examiners. Diagnoses of skeletal age achievable using an MRI examination of the proximal tibial epiphysis can thus be considered reliable and largely independent of the observer. However, contrary to the assertion made by Dedouit et al. [22], the procedure is, in our judgment, scarcely suitable for inexperienced examiners of any specialization. One limitation of our investigation is the fact that, due to the retrospective study design, it was only possible to evaluate one MRI sequence for each subject. It has been proposed for future prospective studies that, in addition to T1-weighted sequences, water-sensitive, fat-suppressed sequences should be generated to represent the epiphyseal cartilage and included in the evaluation.
Key points 1.
Maximum
Verification of the ossification status of the proximal tibial epiphysis using magnetic resonance imaging is a suitable tool for forensic age estimation practice.
2.
3.
4.
Examination of the proximal tibial epiphysis using magnetic resonance imaging makes it possible, in principle, to include a characteristic of skeletal maturity in all areas of application of advisory age estimation practice with due regard to the demands of radiation hygiene. Diagnoses of an ossification stage IIIc according to Kellinghaus et al. in males and an ossification stage IV according to Schmeling et al. in both females and males provide sufficiently reliable evidence of completion of the 14th year of life. Diagnosis of an ossification stage IV according to Schmeling et al. in males provides sufficiently reliable evidence of completion of the 16th year of life. The diagnosis should be in keeping with other indicators of skeletal maturity.
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22.
23.
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27. 28.
29.
30. 31.
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