J Forensic Sci, 2015 doi: 10.1111/1556-4029.12739 Available online at: onlinelibrary.wiley.com
TECHNICAL NOTE ANTHROPOLOGY
Kui Zhang,1,2 Ph.D.; Xiao-gang Chen,1 Ph.D.; Huan Zhao,1 M.S.; Xiao-ai Dong,1 M.S.; and Zhen-hua Deng,1 M.S.
Forensic Age Estimation Using Thin-Slice Multidetector CT of the Clavicular Epiphyses Among Adolescent Western Chinese
ABSTRACT: Reaching the age of 18 years is the most significant step for criminal proceedings in China. In this study, a population of 752
individuals was recruited to clarify how strong the chronological age relates to clavicular ossification status revealed by CT scans with 1 mm slice thickness in the West China Han population. Finally, the epiphysis was observed to commence fusion in females at 16.28 years and 16.74 years in males and be fully ossified by 25.97 years in females and 25.81 years in males. These findings suggested that ossification of medial clavicular epiphyseal cartilage can be used in age estimation for West China Han population with the age threshold of 18 years. By comparison with previous German studies, our results suggested that the pace of ossification of medial clavicular epiphyseal cartilage may be potentially affected by socioeconomic status.
KEYWORDS: forensic science, age estimation, skeletal age, ossification, clavicle, computed tomography, socioeconomic status
Correct age estimation of the accused is important during criminal proceedings. Verified documentation of the date of birth is the only way to determine the exact chronological age of an individual. However, in subjects who do not possess proper identification documents, it is of the utmost importance to verify whether these persons should be accepted as juveniles or adults (1–6). The age of relevance to criminal liability changes according to the national interest. In most countries, age thresholds range between 14 and 18 years. In China, the age thresholds of relevance for criminal proceedings are 14, 16 and 18 years, reaching the age of 18 years the most significant step for the legal assessment of numerous aspects of criminal, civil, and asylum law. The international Study Group on Forensic Age Diagnostics (AGFAD; http://agfad.uni-muenster.de), consisting of forensic physicians, radiologists, dentists, and anthropologists, has developed recommendations for age diagnostics in criminal proceedings and other relevant legal fields. The measures proposed comprise radiological assessments of the left hand, the teeth, and, if hand ossification is complete, the clavicles (7). This method was particularly evident in the younger subjects (8,9). Previous studies indicated that fusion times of the long bones occurred before 18–19 years (10–12). In additional, most teeth are fully developed at around the age of 14 years (13). Generally, at this stage, after formation of the premolars and canines, 1 Department of Forensic Pathology, West China School of Preclinical and Forensic Medicine, Sichuan University, Chengdu, Sichuan 610041, China. 2 Department of Forensic Medicine, Zun Yi Medical College, Zun Yi, Guizhou 563003, China. Received 18 Nov. 2013; and in revised form 20 May 2014; accepted 31 May 2014.
© 2015 American Academy of Forensic Sciences
the third molars are the only teeth still developing. To offer a valuable alternative method for assessing 18 years of age, the clavicle is recommended due to its slowest and most prolonged development (14). In CT examination of the medial clavicular epiphysis, it has been noted that, if slice thickness is increased above a certain maximum value, this might lead to errors when assessing ossification status (15,16). To achieve the best possible results and ensure maximum accuracy in age estimation practice, Schulz et al. (17) recommended performing CT scans with 1 mm slice thickness. In addition, previous CT studies dealing with the ossification status of the medial clavicular epiphysis by Schulz et al. (17,18), Kreitner et al. (19,20), and Kellinghaus et al. (21) were related to Caucasians. So far, there is no consistent conclusion about how the ethnicity influences the ossification status of medial clavicular epiphyseal cartilage. Furthermore, it was reported that the socioeconomic status, sex, and method of examination do have an impact on the pace of ossification (22). The aim of this study was to clarify how strong the chronological age relates to clavicular ossification in the West China Han population using CT scans with 1 mm slice thickness. Materials and Methods A retrospective study of the patients undergoing a CT scan of the clavicle at the West China Hospital of Sichuan University between July 2008 and November 2011 was carried out. All participants are West China Han population, with the subjects ranging in age from 15.00 to 25.99 years. Cases were excluded due to medication or diseases that could affect skeletal development, clavicle fractures, imaging artefacts, and cases of normal variation (e.g., funnel-shaped clavicular epiphyses). All the image 1
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materials available were slices of 1.0 mm, and sufficient documentation of the sternoclavicular joint region. The population with reliable examination included 382 female (50.8%) and 370 male (49.2%) individuals. Table 1 shows sample sizes by sex and age group for the 752 cases in which reliable assessment of the ossification status was possible. This study was performed with the approval of the ethics committee of the West China Hospital of Sichuan University. Multidetector computed tomography (MDCT) studies were obtained using a 16-row MDCT system (Somatom Sensation 16; Siemens AG Erlangen, Germany). Technical settings: 120 kV, reference mAs 50-260 using CareDose, Pitch 1.3, collimation 0.6, recon increment 1.0, Kernel B50f. Due to the fact that all the scans analyzed were based on high-resolution thin-slice MDCT imaging, it can be assumed that the scans provided a comparable and sufficient image quality with regard to the evaluation of osseous structures. The CT images were evaluated on screen using a workstation with SIEMENS software (Syngo Somaris 5-VB20B, Germany). The material was viewed in axial images and in multiplanar reconstruction (MPR technique). The developmental status of the medial clavicular epiphyseal cartilage was evaluated referring to the traditional classification systems (23) differentiating four stages of clavicle ossification as follows: Stage 1: Without ossification of the medial clavicular epiphyses. Stage 2: Ossification of the medial clavicular epiphyses, without apparent fusion with the metaphysis. Stage 3: Epiphyseal cartilage partly ossified. Stage 4: Epiphyseal cartilage fully ossified, regardless of epiphyseal scar visible or not. Figure 1 shows the findings corresponding to each of the stages 1–4. All cross-sections were evaluated for the respective epiphysis. The cross-section with the most advanced ossification stage was decisive for the stage diagnosis. All evaluations were made twice by one examiner. Prior to and during analysis of the MDCT images, the age of the individuals was not known to the examiner. Data from both sides were coincidental as no significant differences in maturation were observed between the left and right clavicles. Results are expressed as minimum, maximum, mean SD, and median with lower and upper quartiles. Statistical analyses were performed using SPSS (VERSION 13.0 for WINDOWS, SPSS Inc., Chicago, IL, USA). To cope with outliers and/or skew distributions, sexual differences were analyzed using Mann–Whitney U-test for two independent groups. Significance was assessed at p < 0.05, exact, two-sided.
FIG. 1––CT slice images from the actual study representing the following stages: stage 1, without ossification of the medial clavicular epiphyses; stage 2, ossification of the medial clavicular epiphyses, without apparent fusion with the metaphysis; stage 3, epiphyseal cartilage partly ossified; stage 4, epiphyseal cartilage fully ossified, epiphyseal scar visible. The arrow shows the partially ossified epiphyseal cartilage.
Results Table 2 presents the minimum, maximum, mean SD and median with lower and upper quartiles for stages 1–4 separately for each sex. Mann–Whitney’s U-test revealed no statistic difference between the sexes (p > 0.05) for stage 1–4. t-Test was assessed for interobserver variability, and no significant difference was observed (p < 0.001). We observed the stage 1 in 82 cases (33 males, 19 females), stage 2 in 149 cases (75 males, 74 females), stage 3 in 430 cases (198 males, 232 females), and stage 4 in 121 cases (64 males, 57 females). In male participants, the maximum age for stage 1 was noted at 18.00 years, in female participants at 17.62 years. In both sexes, stage 2 was first noted at 15 years. The earliest occurrence of stage 3 in both male and female participants was observed at 16 years. The minimum age for stage 4 was 20.03 years in male participants and 20 in female participants except for one outlier with the age of 18.89 years.
TABLE 1––Frequency distribution by sex and age cohort. TABLE 2––Statistical parameters in years by sex for ossification stages 1–4. Age (Year)
Male
Female
Total
15 16 17 18 19 20 21 22 23 24 25 Total
28 29 32 34 33 38 37 39 33 43 24 370
28 21 40 37 29 37 36 39 43 40 32 382
56 50 72 71 62 75 73 78 76 83 56 752
Stage 1 2 3 4
Sex
Min–Max
Female Male Female Male Female Male Female Male
15.00–17.62 15.00–18.00 15.00–20.13 15.01–20.63 16.28–25.82 16.74–25.97 18.89–25.97 20.03–25.81
Mean SD 15.59 15.99 17.12 17.30 21.57 21.47 23.70 23.77
0.70 0.86 1.19 1.30 2.31 2.13 1.66 1.31
Median; LQ; UQ 15.21; 15.78; 17.14; 17.16; 21.64; 21.35; 23.98; 23.96;
15.08; 15.15; 16.21; 16.02; 19.90; 19.93; 22.42; 22.81;
16.05 16.69 18.00 18.25 23.46 23.03 25.00 24.86
Min, minimum, Max, maximum, SD, standard deviation, LQ, lower quartile, UQ, upper quartile.
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FIG. 2––Box-and-whiskers-plot for all stages of all clavicles: box represents interquartile range, thick black horizontal line represents median, t-bars represent extremes, and (+) represent outliers.
FIG. 3––Empiric distribution function for all stages of all clavicles: horizontal reference lines at 5, 75, and 95%, vertical reference line at age 18.
The box-and-whiskers plots of all stage values showed no normal distribution (Fig. 2). Therefore, confidence intervals linked to the SD of mean values could not be used, and an empiric distribution function for all stages was calculated (Fig. 3). The empiric distribution function shows that 100% of the participants were below the age of 18 years for stage 1, 70% of the participants were below the age of 18 years for stage 2, 95% of the participants were above the age of 18 years for stage 3, and 100% of the participants were above the age of 18 years for stage 4.
(23) reported that the assessment of ossification stages differed for slice thicknesses of 1 and 3 mm, 3 and 5 mm as well as 5 and 7 mm. Such differences affected stages 2 and 3, stages 3 and 5, and stages 4 and 5. In all cases in which slice thickness made a difference, increased slice thickness resulted in determining higher ossification stages. Based on these findings, it can be concluded that with thick-slice CT imaging, higher ossification stages tend to appear at earlier ages. The partial volume effect occurring with thick-slice CT images is held responsible for the partial or complete visual masking of fine structures such as the epiphyseal plate as well as the epiphyseal scar. In the present study, thin-slice multidetector CT images with 1 mm slice thickness in a recruited population of 752 individuals were evaluated; we observed a stage 4 in 121 cases (64 males, 57 females) occurring first at the age of 20.03 in male participants and 20 in female participants except for one outlier with the age of 18.89 years. Several preliminary CT-based studies have results unseparated by sexes; a comparison between male and female was performed in the studies of Schulz et al. (17) and Kellinghaus et al. (21). There are significant sex differences. They all revealed statistically significant differences for stage 2, with the female patients achieving that stage earlier than the male patients. Our research failed to find statistic difference affected by the sex in West China Han population.
Discussion Reports dealing with radiological changes during the ossification of the medial clavicular epiphysis go back to the 1930s of the past century (12). In 1997 and 1998, Kreitner et al. (19,20) published the first CT-based studies in which the medial epiphyseal ossification of the clavicle was evaluated applying a four-stage scheme. Subsequently, several related studies were published in 2005 (17), 2006 (18), and 2010 (21), respectively. Preliminary CT-based studies have a limited validity due to evaluation of thick-slice images of 7 or 8 mm in the majority of cases (17–20). Slice thickness of CT scans has a decisive influence on the evaluation of the clavicle ossification status. M€ uhler et al.
TABLE 3––Comparison of CT studies dealing with the ossification of the medial clavicular epiphysis.
Study Kreitner et al. (1997)* (19) Kreitner et al. (1998)* (20) Schulz et al. (2005)† (17) Schulz et al. (2006)* (18) Kellinghaus et al. (2010)† (21) Present study
Case Number 279 380 629 100 592 752
Sex Separation No No Yes No Yes Yes
Age (in Years)
Slice Thickness (in mm)
Stage 1 (Age in Years)
Stage 2 (Age in Years)
Stage 3 (Age in Years)
Stage 4 (Age in Years)
Stage 5 (Age in Years)
0–29 0–29 15–30 16–25 10–35 15–25
1–8 1–8 1–7 1–10 0.6–1.5 1.0
— 0–16 — — 10–15 15–18
13–22 11–22 15–23 16–24 13–20 15–20
16–26 16–26 16–28 16–25 16–26 16–25
22–29 22–29 21–30 19–25 21–35 18–25
— — 21–30 — 26–35 —
Classification systems for stages of clavicle ossification in previous studies: *Stage 1 refers to nonunion without ossification of the epiphysis; Stage 2 to nonunion with a separate and ossified epiphysis; Stage 3 to partial; and Stage 4 to complete union. † Stage 1: Ossification center not ossified; Stage 2: Ossification center ossified, epiphyseal cartilage not ossified; Stage 3: Epiphyseal cartilage partly ossified; Stage 4: Epiphyseal cartilage fully ossified, epiphyseal scar visible; Stage 5: Epiphyseal cartilage fully ossified, epiphyseal scar no longer visible.
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Only ethnicity did not significantly affect this probability of being diagnosed with mature clavicles, whereas socioeconomic status, sex, and method of examination are factors that do influence age estimation from this bone (22). All previous CT studies dealing with the ossification of the medial clavicular epiphysis were relating to a population from Germany. Considering that socioeconomic status and method of examination do influence age estimation, this retrospective study was performed. Our result revealed a minimum age of 20 years for stage 4 except for one outlier with the age of 18 years. This result was different from other researchers’ results obtained from studies in German. Kreitner et al. (19,20) reported a minimum age of 22 years for stage 4; Schulz et al. (17) and Kellinghaus et al. (21) observed the stage 4 occurring first at the age of 21. Even performed similarly using thin-slice CT scans, our result was deviant to the result of Kellinghaus et al.’s research (21) with minimum age of 21 years for stage 4. Schulz et al. (18) reported a minimum age of 19 years for stage 4. The reason may not be interpreted simply as a consequence of the partial volume effect. Previous research thought that ethnic origin does not apparently exert any notable influence on the rate of ossification within the relevant age group (24,25). Meijerman et al. (22) grouped the previously studied samples by the HDI (human development index) of the country from where the samples come from. According to their results, a higher HDI, meaning better socioeconomic conditions, is associated to advancement in maturation. By comparison, we considered that socioeconomic status may be the potential effect. Table 3 provides an overview of the mentioned CT studies on the ossification of the medial clavicular epiphysis. In conclusion, our results with 100% of the participants below the age of 18 years for stage 1 and 100% of the participants above the age of 18 years for stage 4 may be used as a method for age estimation in West China Han population. Subsequently, when the existence of stage 4 development is verified, subjects may be considered of legal age beyond reasonable doubt. Furthermore, our results suggested that the pace of ossification of medial clavicular epiphyseal cartilage may potentially affected by ethnicity or socioeconomic status. However, the finding needs to be confirmed with the results of different ethnicities or socioeconomic status. Acknowledgments Supported by the National Natural Science Foundation of China (No. 81373252) and the Applied Basic Research Programs of Science and Technology Commission Foundation of Sichuan Province (No. 2013JY0148). References 1. Cunha E, Baccino E, Martrille L, Ramsthaler F, Prieto J, Schuliar Y, et al. The problem of aging human remains and living individuals: a review. Forensic Sci Int 2009;193(1–3):1–13. 2. Olze A, Reisinger W, Geserick G, Schmeling A. Age estimation of unaccompanied minors. Part II. Dental aspects. Forensic Sci Int 2006;159 (Suppl 1):S65–7. 3. Schmeling A, Reisinger W, Geserick G, Olze A. Age estimation of unaccompanied minors. Part I. General considerations. Forensic Sci Int 2006;159(Suppl 1):S61–4. 4. Aynsley-Green A. Unethical age assessment. Br Dent J 2009;206(7):337. 5. Tawfik Y, Nsungwa-Sabitii J, Greer G, Owor J, Kesande R, Prysor-Jones S. Negotiating improved case management of childhood illness with formal and informal private practitioners in Uganda. Trop Med Int Health 2006;11(6):967–73.
6. Security DoH. Age determination practices for unaccompanied alien children in ICE custody. Washington, DC: Department of Homeland Security, 2009. 7. Schmeling A, Grundmann C, Fuhrmann A, Kaatsch HJ, Knell B, Ramsthaler F, et al. Criteria for age estimation in living individuals. Int J Legal Med 2008;122(6):457–60. 8. Schmidt S, Nitz I, Schulz R, Schmeling A. Applicability of the skeletal age determination method of Tanner and Whitehouse for forensic age diagnostics. Int J Legal Med 2008;122(4):309–14. 9. Schmeling A, Schulz R, Danner B, Rosing FW. The impact of economic progress and modernization in medicine on the ossification of hand and wrist. Int J Legal Med 2006;120(2):121–6. 10. Pyle SI, Hoerr NL. Radiographic atlas of skeletal development of the knee. A standard of reference. Springfield, IL: Charles C Thomas, 1955. 11. Das Gupta SM, Prasad V, Singh S. A roentgenologic study of epiphyseal union around elbow, wrist and knee joints and the pelvis in boys and girls of Uttar Pradesh. J Indian Med Assoc 1974;62(1):10–2. 12. Flecker H. Roentgenographic observations of the times of appearance of epiphyses and their fusion with the diaphyses. J Anat 1932;67(Pt 1):118–64.3. 13. Demirjian A, Goldstein H, Tanner JM. A new system of dental age assessment. Hum Biol 1973;45(2):211–27. 14. Ji L, Terazawa K, Tsukamoto T, Haga K. Estimation of age from epiphyseal union degrees of the sternal end of the clavicle. Hokkaido Igaku Zasshi 1994;69(1):104–11. 15. Brenner DJ. Estimating cancer risks from pediatric CT: going from the qualitative to the quantitative. Pediatr Radiol 2002;32(4):228–3; discussion 42–4. 16. Ramsthaler F, Proschek P, Betz W, Verhoff MA. How reliable are the risk estimates for X-ray examinations in forensic age estimations? A safety update. Int J Legal Med 2009;123(3):199–204. 17. Schulz R, Muhler M, Mutze S, Schmidt S, Reisinger W, Schmeling A. Studies on the time frame for ossification of the medial epiphysis of the clavicle as revealed by CT scans. Int J Legal Med 2005;119(3):142–5. 18. Schulze D, Rother U, Fuhrmann A, Richel S, Faulmann G, Heiland M. Correlation of age and ossification of the medial clavicular epiphysis using computed tomography. Forensic Sci Int 2006;158(2–3):184–9. 19. Kreitner KF, Schweden F, Schild HH, Riepert T, Nafe B. Computerized tomography of the epiphyseal union of the medial clavicle: an auxiliary method of age determination during adolescence and the 3d decade of life? Rofo 1997;166(6):481–6. Die computertomographisch bestimmte Ausreifung der medialen Klavikulaepiphyse–eine additive Methode zur Altersbestimmung im Adoleszentenalter und in der dritten Lebensdekade? 20. Kreitner KF, Schweden FJ, Riepert T, Nafe B, Thelen M. Bone age determination based on the study of the medial extremity of the clavicle. Eur Radiol 1998;8(7):1116–22. 21. Kellinghaus M, Schulz R, Vieth V, Schmidt S, Schmeling A. Forensic age estimation in living subjects based on the ossification status of the medial clavicular epiphysis as revealed by thin-slice multidetector computed tomography. Int J Legal Med 2010;124(2):149–54. 22. Meijerman L, Maat GJ, Schulz R, Schmeling A. Variables affecting the probability of complete fusion of the medial clavicular epiphysis. Int J Legal Med 2007;121(6):463–8. 23. Muhler M, Schulz R, Schmidt S, Schmeling A, Reisinger W. The influence of slice thickness on assessment of clavicle ossification in forensic age diagnostics. Int J Legal Med 2006;120(1):15–7. 24. Schmeling A, Schulz R, Reisinger W, Muhler M, Wernecke KD, Geserick G. Studies on the time frame for ossification of the medial clavicular epiphyseal cartilage in conventional radiography. Int J Legal Med 2004;118(1):5–8. 25. Schmeling A, Reisinger W, Loreck D, Vendura K, Markus W, Geserick G. Effects of ethnicity on skeletal maturation: consequences for forensic age estimations. Int J Legal Med 2000;113(5):253–8. Additional information and reprint requests: Prof. Zhen-hua Deng, M.S. Chengdu People’s Street 16# Department of Forensic Pathology West China School of Preclinical and Forensic Medicine Sichuan University Chengdu 610041 China E-mail: [email protected]
TECHNICAL NOTE ANTHROPOLOGY
Kui Zhang,1,2 Ph.D.; Xiao-gang Chen,1 Ph.D.; Huan Zhao,1 M.S.; Xiao-ai Dong,1 M.S.; and Zhen-hua Deng,1 M.S.
Forensic Age Estimation Using Thin-Slice Multidetector CT of the Clavicular Epiphyses Among Adolescent Western Chinese
ABSTRACT: Reaching the age of 18 years is the most significant step for criminal proceedings in China. In this study, a population of 752
individuals was recruited to clarify how strong the chronological age relates to clavicular ossification status revealed by CT scans with 1 mm slice thickness in the West China Han population. Finally, the epiphysis was observed to commence fusion in females at 16.28 years and 16.74 years in males and be fully ossified by 25.97 years in females and 25.81 years in males. These findings suggested that ossification of medial clavicular epiphyseal cartilage can be used in age estimation for West China Han population with the age threshold of 18 years. By comparison with previous German studies, our results suggested that the pace of ossification of medial clavicular epiphyseal cartilage may be potentially affected by socioeconomic status.
KEYWORDS: forensic science, age estimation, skeletal age, ossification, clavicle, computed tomography, socioeconomic status
Correct age estimation of the accused is important during criminal proceedings. Verified documentation of the date of birth is the only way to determine the exact chronological age of an individual. However, in subjects who do not possess proper identification documents, it is of the utmost importance to verify whether these persons should be accepted as juveniles or adults (1–6). The age of relevance to criminal liability changes according to the national interest. In most countries, age thresholds range between 14 and 18 years. In China, the age thresholds of relevance for criminal proceedings are 14, 16 and 18 years, reaching the age of 18 years the most significant step for the legal assessment of numerous aspects of criminal, civil, and asylum law. The international Study Group on Forensic Age Diagnostics (AGFAD; http://agfad.uni-muenster.de), consisting of forensic physicians, radiologists, dentists, and anthropologists, has developed recommendations for age diagnostics in criminal proceedings and other relevant legal fields. The measures proposed comprise radiological assessments of the left hand, the teeth, and, if hand ossification is complete, the clavicles (7). This method was particularly evident in the younger subjects (8,9). Previous studies indicated that fusion times of the long bones occurred before 18–19 years (10–12). In additional, most teeth are fully developed at around the age of 14 years (13). Generally, at this stage, after formation of the premolars and canines, 1 Department of Forensic Pathology, West China School of Preclinical and Forensic Medicine, Sichuan University, Chengdu, Sichuan 610041, China. 2 Department of Forensic Medicine, Zun Yi Medical College, Zun Yi, Guizhou 563003, China. Received 18 Nov. 2013; and in revised form 20 May 2014; accepted 31 May 2014.
© 2015 American Academy of Forensic Sciences
the third molars are the only teeth still developing. To offer a valuable alternative method for assessing 18 years of age, the clavicle is recommended due to its slowest and most prolonged development (14). In CT examination of the medial clavicular epiphysis, it has been noted that, if slice thickness is increased above a certain maximum value, this might lead to errors when assessing ossification status (15,16). To achieve the best possible results and ensure maximum accuracy in age estimation practice, Schulz et al. (17) recommended performing CT scans with 1 mm slice thickness. In addition, previous CT studies dealing with the ossification status of the medial clavicular epiphysis by Schulz et al. (17,18), Kreitner et al. (19,20), and Kellinghaus et al. (21) were related to Caucasians. So far, there is no consistent conclusion about how the ethnicity influences the ossification status of medial clavicular epiphyseal cartilage. Furthermore, it was reported that the socioeconomic status, sex, and method of examination do have an impact on the pace of ossification (22). The aim of this study was to clarify how strong the chronological age relates to clavicular ossification in the West China Han population using CT scans with 1 mm slice thickness. Materials and Methods A retrospective study of the patients undergoing a CT scan of the clavicle at the West China Hospital of Sichuan University between July 2008 and November 2011 was carried out. All participants are West China Han population, with the subjects ranging in age from 15.00 to 25.99 years. Cases were excluded due to medication or diseases that could affect skeletal development, clavicle fractures, imaging artefacts, and cases of normal variation (e.g., funnel-shaped clavicular epiphyses). All the image 1
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materials available were slices of 1.0 mm, and sufficient documentation of the sternoclavicular joint region. The population with reliable examination included 382 female (50.8%) and 370 male (49.2%) individuals. Table 1 shows sample sizes by sex and age group for the 752 cases in which reliable assessment of the ossification status was possible. This study was performed with the approval of the ethics committee of the West China Hospital of Sichuan University. Multidetector computed tomography (MDCT) studies were obtained using a 16-row MDCT system (Somatom Sensation 16; Siemens AG Erlangen, Germany). Technical settings: 120 kV, reference mAs 50-260 using CareDose, Pitch 1.3, collimation 0.6, recon increment 1.0, Kernel B50f. Due to the fact that all the scans analyzed were based on high-resolution thin-slice MDCT imaging, it can be assumed that the scans provided a comparable and sufficient image quality with regard to the evaluation of osseous structures. The CT images were evaluated on screen using a workstation with SIEMENS software (Syngo Somaris 5-VB20B, Germany). The material was viewed in axial images and in multiplanar reconstruction (MPR technique). The developmental status of the medial clavicular epiphyseal cartilage was evaluated referring to the traditional classification systems (23) differentiating four stages of clavicle ossification as follows: Stage 1: Without ossification of the medial clavicular epiphyses. Stage 2: Ossification of the medial clavicular epiphyses, without apparent fusion with the metaphysis. Stage 3: Epiphyseal cartilage partly ossified. Stage 4: Epiphyseal cartilage fully ossified, regardless of epiphyseal scar visible or not. Figure 1 shows the findings corresponding to each of the stages 1–4. All cross-sections were evaluated for the respective epiphysis. The cross-section with the most advanced ossification stage was decisive for the stage diagnosis. All evaluations were made twice by one examiner. Prior to and during analysis of the MDCT images, the age of the individuals was not known to the examiner. Data from both sides were coincidental as no significant differences in maturation were observed between the left and right clavicles. Results are expressed as minimum, maximum, mean SD, and median with lower and upper quartiles. Statistical analyses were performed using SPSS (VERSION 13.0 for WINDOWS, SPSS Inc., Chicago, IL, USA). To cope with outliers and/or skew distributions, sexual differences were analyzed using Mann–Whitney U-test for two independent groups. Significance was assessed at p < 0.05, exact, two-sided.
FIG. 1––CT slice images from the actual study representing the following stages: stage 1, without ossification of the medial clavicular epiphyses; stage 2, ossification of the medial clavicular epiphyses, without apparent fusion with the metaphysis; stage 3, epiphyseal cartilage partly ossified; stage 4, epiphyseal cartilage fully ossified, epiphyseal scar visible. The arrow shows the partially ossified epiphyseal cartilage.
Results Table 2 presents the minimum, maximum, mean SD and median with lower and upper quartiles for stages 1–4 separately for each sex. Mann–Whitney’s U-test revealed no statistic difference between the sexes (p > 0.05) for stage 1–4. t-Test was assessed for interobserver variability, and no significant difference was observed (p < 0.001). We observed the stage 1 in 82 cases (33 males, 19 females), stage 2 in 149 cases (75 males, 74 females), stage 3 in 430 cases (198 males, 232 females), and stage 4 in 121 cases (64 males, 57 females). In male participants, the maximum age for stage 1 was noted at 18.00 years, in female participants at 17.62 years. In both sexes, stage 2 was first noted at 15 years. The earliest occurrence of stage 3 in both male and female participants was observed at 16 years. The minimum age for stage 4 was 20.03 years in male participants and 20 in female participants except for one outlier with the age of 18.89 years.
TABLE 1––Frequency distribution by sex and age cohort. TABLE 2––Statistical parameters in years by sex for ossification stages 1–4. Age (Year)
Male
Female
Total
15 16 17 18 19 20 21 22 23 24 25 Total
28 29 32 34 33 38 37 39 33 43 24 370
28 21 40 37 29 37 36 39 43 40 32 382
56 50 72 71 62 75 73 78 76 83 56 752
Stage 1 2 3 4
Sex
Min–Max
Female Male Female Male Female Male Female Male
15.00–17.62 15.00–18.00 15.00–20.13 15.01–20.63 16.28–25.82 16.74–25.97 18.89–25.97 20.03–25.81
Mean SD 15.59 15.99 17.12 17.30 21.57 21.47 23.70 23.77
0.70 0.86 1.19 1.30 2.31 2.13 1.66 1.31
Median; LQ; UQ 15.21; 15.78; 17.14; 17.16; 21.64; 21.35; 23.98; 23.96;
15.08; 15.15; 16.21; 16.02; 19.90; 19.93; 22.42; 22.81;
16.05 16.69 18.00 18.25 23.46 23.03 25.00 24.86
Min, minimum, Max, maximum, SD, standard deviation, LQ, lower quartile, UQ, upper quartile.
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FIG. 2––Box-and-whiskers-plot for all stages of all clavicles: box represents interquartile range, thick black horizontal line represents median, t-bars represent extremes, and (+) represent outliers.
FIG. 3––Empiric distribution function for all stages of all clavicles: horizontal reference lines at 5, 75, and 95%, vertical reference line at age 18.
The box-and-whiskers plots of all stage values showed no normal distribution (Fig. 2). Therefore, confidence intervals linked to the SD of mean values could not be used, and an empiric distribution function for all stages was calculated (Fig. 3). The empiric distribution function shows that 100% of the participants were below the age of 18 years for stage 1, 70% of the participants were below the age of 18 years for stage 2, 95% of the participants were above the age of 18 years for stage 3, and 100% of the participants were above the age of 18 years for stage 4.
(23) reported that the assessment of ossification stages differed for slice thicknesses of 1 and 3 mm, 3 and 5 mm as well as 5 and 7 mm. Such differences affected stages 2 and 3, stages 3 and 5, and stages 4 and 5. In all cases in which slice thickness made a difference, increased slice thickness resulted in determining higher ossification stages. Based on these findings, it can be concluded that with thick-slice CT imaging, higher ossification stages tend to appear at earlier ages. The partial volume effect occurring with thick-slice CT images is held responsible for the partial or complete visual masking of fine structures such as the epiphyseal plate as well as the epiphyseal scar. In the present study, thin-slice multidetector CT images with 1 mm slice thickness in a recruited population of 752 individuals were evaluated; we observed a stage 4 in 121 cases (64 males, 57 females) occurring first at the age of 20.03 in male participants and 20 in female participants except for one outlier with the age of 18.89 years. Several preliminary CT-based studies have results unseparated by sexes; a comparison between male and female was performed in the studies of Schulz et al. (17) and Kellinghaus et al. (21). There are significant sex differences. They all revealed statistically significant differences for stage 2, with the female patients achieving that stage earlier than the male patients. Our research failed to find statistic difference affected by the sex in West China Han population.
Discussion Reports dealing with radiological changes during the ossification of the medial clavicular epiphysis go back to the 1930s of the past century (12). In 1997 and 1998, Kreitner et al. (19,20) published the first CT-based studies in which the medial epiphyseal ossification of the clavicle was evaluated applying a four-stage scheme. Subsequently, several related studies were published in 2005 (17), 2006 (18), and 2010 (21), respectively. Preliminary CT-based studies have a limited validity due to evaluation of thick-slice images of 7 or 8 mm in the majority of cases (17–20). Slice thickness of CT scans has a decisive influence on the evaluation of the clavicle ossification status. M€ uhler et al.
TABLE 3––Comparison of CT studies dealing with the ossification of the medial clavicular epiphysis.
Study Kreitner et al. (1997)* (19) Kreitner et al. (1998)* (20) Schulz et al. (2005)† (17) Schulz et al. (2006)* (18) Kellinghaus et al. (2010)† (21) Present study
Case Number 279 380 629 100 592 752
Sex Separation No No Yes No Yes Yes
Age (in Years)
Slice Thickness (in mm)
Stage 1 (Age in Years)
Stage 2 (Age in Years)
Stage 3 (Age in Years)
Stage 4 (Age in Years)
Stage 5 (Age in Years)
0–29 0–29 15–30 16–25 10–35 15–25
1–8 1–8 1–7 1–10 0.6–1.5 1.0
— 0–16 — — 10–15 15–18
13–22 11–22 15–23 16–24 13–20 15–20
16–26 16–26 16–28 16–25 16–26 16–25
22–29 22–29 21–30 19–25 21–35 18–25
— — 21–30 — 26–35 —
Classification systems for stages of clavicle ossification in previous studies: *Stage 1 refers to nonunion without ossification of the epiphysis; Stage 2 to nonunion with a separate and ossified epiphysis; Stage 3 to partial; and Stage 4 to complete union. † Stage 1: Ossification center not ossified; Stage 2: Ossification center ossified, epiphyseal cartilage not ossified; Stage 3: Epiphyseal cartilage partly ossified; Stage 4: Epiphyseal cartilage fully ossified, epiphyseal scar visible; Stage 5: Epiphyseal cartilage fully ossified, epiphyseal scar no longer visible.
4
JOURNAL OF FORENSIC SCIENCES
Only ethnicity did not significantly affect this probability of being diagnosed with mature clavicles, whereas socioeconomic status, sex, and method of examination are factors that do influence age estimation from this bone (22). All previous CT studies dealing with the ossification of the medial clavicular epiphysis were relating to a population from Germany. Considering that socioeconomic status and method of examination do influence age estimation, this retrospective study was performed. Our result revealed a minimum age of 20 years for stage 4 except for one outlier with the age of 18 years. This result was different from other researchers’ results obtained from studies in German. Kreitner et al. (19,20) reported a minimum age of 22 years for stage 4; Schulz et al. (17) and Kellinghaus et al. (21) observed the stage 4 occurring first at the age of 21. Even performed similarly using thin-slice CT scans, our result was deviant to the result of Kellinghaus et al.’s research (21) with minimum age of 21 years for stage 4. Schulz et al. (18) reported a minimum age of 19 years for stage 4. The reason may not be interpreted simply as a consequence of the partial volume effect. Previous research thought that ethnic origin does not apparently exert any notable influence on the rate of ossification within the relevant age group (24,25). Meijerman et al. (22) grouped the previously studied samples by the HDI (human development index) of the country from where the samples come from. According to their results, a higher HDI, meaning better socioeconomic conditions, is associated to advancement in maturation. By comparison, we considered that socioeconomic status may be the potential effect. Table 3 provides an overview of the mentioned CT studies on the ossification of the medial clavicular epiphysis. In conclusion, our results with 100% of the participants below the age of 18 years for stage 1 and 100% of the participants above the age of 18 years for stage 4 may be used as a method for age estimation in West China Han population. Subsequently, when the existence of stage 4 development is verified, subjects may be considered of legal age beyond reasonable doubt. Furthermore, our results suggested that the pace of ossification of medial clavicular epiphyseal cartilage may potentially affected by ethnicity or socioeconomic status. However, the finding needs to be confirmed with the results of different ethnicities or socioeconomic status. Acknowledgments Supported by the National Natural Science Foundation of China (No. 81373252) and the Applied Basic Research Programs of Science and Technology Commission Foundation of Sichuan Province (No. 2013JY0148). References 1. Cunha E, Baccino E, Martrille L, Ramsthaler F, Prieto J, Schuliar Y, et al. The problem of aging human remains and living individuals: a review. Forensic Sci Int 2009;193(1–3):1–13. 2. Olze A, Reisinger W, Geserick G, Schmeling A. Age estimation of unaccompanied minors. Part II. Dental aspects. Forensic Sci Int 2006;159 (Suppl 1):S65–7. 3. Schmeling A, Reisinger W, Geserick G, Olze A. Age estimation of unaccompanied minors. Part I. General considerations. Forensic Sci Int 2006;159(Suppl 1):S61–4. 4. Aynsley-Green A. Unethical age assessment. Br Dent J 2009;206(7):337. 5. Tawfik Y, Nsungwa-Sabitii J, Greer G, Owor J, Kesande R, Prysor-Jones S. Negotiating improved case management of childhood illness with formal and informal private practitioners in Uganda. Trop Med Int Health 2006;11(6):967–73.
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