Only photos on my best side, please! Implications of bilateral asymmetry of the iliac auricular surface in non-adult individuals for sex estimation
Corresponding Author
Álvaro M. Monge Calleja
Research Centre for Anthropology and Health (CIAS), Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, Coimbra, 3000-456 Portugal
Correspondence
Álvaro M. Monge Calleja, Research Centre for Anthropology and Health (CIAS), Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal.
Email: [email protected]
Search for more papers by this authorClaudia M. Aranda
Bioarchaeology and Forensic Anthropology Research Unit (UIBAF), Faculty of Odontology (FOUBA) and Public Health Research Institute (IISAP), University of Buenos Aires, Buenos Aires, Argentina
Search for more papers by this authorLeandro H. Luna
National Council of Scientific and Technical Research (CONICET). Bioarchaeology and Forensic Anthropology Research Unit (UIBAF), Faculty of Odontology (FOUBA) and Public Health Research Institute (IISAP), University of Buenos Aires, Buenos Aires, Argentina
Search for more papers by this authorCorresponding Author
Álvaro M. Monge Calleja
Research Centre for Anthropology and Health (CIAS), Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, Coimbra, 3000-456 Portugal
Correspondence
Álvaro M. Monge Calleja, Research Centre for Anthropology and Health (CIAS), Department of Life Sciences, University of Coimbra, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal.
Email: [email protected]
Search for more papers by this authorClaudia M. Aranda
Bioarchaeology and Forensic Anthropology Research Unit (UIBAF), Faculty of Odontology (FOUBA) and Public Health Research Institute (IISAP), University of Buenos Aires, Buenos Aires, Argentina
Search for more papers by this authorLeandro H. Luna
National Council of Scientific and Technical Research (CONICET). Bioarchaeology and Forensic Anthropology Research Unit (UIBAF), Faculty of Odontology (FOUBA) and Public Health Research Institute (IISAP), University of Buenos Aires, Buenos Aires, Argentina
Search for more papers by this authorAbstract
This study aims to address the overlooked effect of bilateral asymmetry for sex estimation in non-adult paired bone structures. Using a recently developed method, disparities between right and left iliac auricular surfaces (AuSs) were quantified, also verifying the effectiveness between sides regarding the percentages of cases correctly assigned. A sample of 418 AuSs belonging to 209 individuals aged 5 gestational months to 18 years (113 males and 96 females) from the Coimbra, Lisbon, and Granada Identified skeletal collections, were studied. They were grouped into two large age cohorts (≤12 y.o. and 12.1–18 y.o.) based on the onset of menarche. The significant and distinct hormonal fluctuations between sexes in ≤2 y.o. individuals compelled an additional separation. Locomotion issues also imposed grouping individuals for comparison in non-bipedal (≤1 y.o.) and those who were still achieving emerging gait milestones (1.1–6 y.o.). Overall agreements between sides, sexes, age cohorts, and morphometric variables were compared using Cohen's κ and intraclass correlation coefficients, while chi-square and Kolmogorov–Smirnov tests were applied for statistically significant evaluation. Asymmetry directionality was calculated through standardized directional and total asymmetry scores. Slight asymmetries between sides were identified, becoming the pre-pubertal left AuS more useful for non-adult female sexing. Metric variables work better in males, possibly due to the higher variability found in females. Both sexes display a marked age-related change in asymmetry during puberty (12.1–18 y.o.), with a predominance of the right side in females and of the left side in males. Possible explanations for the identified pubertal abrupt shifts are discussed considering the various developmental biomechanical milestones. This pioneering study reinforces the complexity of somatic growth and development that characterizes non-adult phenotype, calling for further refinement of sexing methods considering bilateral asymmetry, and for complementary studies that deepen the study of dextralization and its repercussions in adults.
CONFLICT OF INTEREST STATEMENT
The authors declare no conflicts of interest.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
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oa3361-sup-0001-Supporting_Information.jpgJPEG image, 453.4 KB |
Data S1. Supplemental material 1. Identification of outliers using boxplots graphed and by age cohort, biological sex, and asymmetry directionality scores (SDA and STA) for DE/AD and FEI/CF ratios. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Al-Eisa, E., Egan, D., Deluzio, K., & Wassersug, R. (2006). Effects of pelvic asymmetry and low back pain on trunk kinematics during sitting: A comparison with standing. Spine, 31, E135–E143. https://doi.org/10.1097/01.brs.0000201325.89493.5f
- Alemán, I., Irurita, J., Valencia, A. R., Martínez, A., López-Lázaro, S., Viciano, J., & Botella, M. C. (2012). The Granada osteological collection of identified infants and young children. American Journal of Physical Anthropology, 149, 606–610. https://doi.org/10.1002/ajpa.22165
- Bernis, C. (1977). Edades de menarquia y menopausia en la mujer española. Actas I Congreso Español de Antropología (pp. 475–481). Universidad de Barcelona.
- Best, K. C., Garvin, H. M., & Cabo, L. L. (2017). An investigation into the relationship between human cranial and pelvic sexual dimorphism. Journal of Forensic Sciences, 63, 990–1000. https://doi.org/10.1111/1556-4029.13669
- Bibrowicz, K., Szurmik, T., Ofrodzka-Ciechanowicz, K., Hudakova, Z., Gąsienica-Walczak, B., & Kurzeja, P. (2023). Asymmetry of the pelvis in polish young adults. Frontiers in Psychology, 14, 1148239. https://doi.org/10.3389/fpsyg.2023.1148239
- Bobak, C. A., Barr, P. J., & O'Malley, A. J. (2018). Estimation of an inter-rater intra-class correlation coefficient that overcomes common assumption violations in the assessment of health measurement scales. BMC Medical Research Methodology, 18, 93. https://doi.org/10.1186/s12874-018-0550-6
- Boulay, C., Tadieu, C., Bénaim, C., Hecquet, J., Marty, C., Prat-Pradal, D., Lagaye, J., Duval-Beaupère, G., & Pélissier, J. (2006). Three-dimensional study of pelvic asymmetry on anatomical specimens and its clinical perspectives. Journal of Anatomy, 208, 21–33. https://doi.org/10.1111/j.1469-7580.2006.00513.x
- Cardoso, H. F. V. (2006). Brief communication: The collection of identified human skeletons housed at the Bocage museum (National Museum of Natural History), Lisbon, Portugal. American Journal of Physical Anthropology, 129, 173–176. https://doi.org/10.1002/ajpa.20228
- Chibber, S. R., & Singh, I. (1970). Asymmetry in muscle weight and one sided dominance in the human lower limbs. Journal of Anatomy, 106, 553–556.
- Chiron, C., Jambaque, I., Nabbout, R., Lounes, R., Syrota, A., & Dulac, O. (1997). The right brain hemisphere is dominant in human infants. Brain, 120, 1057–1065. https://doi.org/10.1093/brain/120.6.1057
- Cole, S. J., Hulse, C. N., & Stull, K. E. (2020). The effects of skeletal asymmetry on accurate sex classification. In A. R. Klales (Ed.), Sex estimation of the human skeleton: History, methods, and emerging techniques (pp. 307–325). Academic Press. https://doi.org/10.1016/B978-0-12-815767-1.00019-5
10.1016/B978-0-12-815767-1.00019-5 Google Scholar
- Damen, L., Buyruk, H. M., Güler-Uysal, F., Lotgering, F. K., Snijders, C. J., & Stam, H. J. (2001). Pelvic pain during pregnancy is associated with asymmetric laxity of the sacroiliac joints. Acta Obstetrica et Gynecologica Scandinavica, 80, 1019–1024. https://doi.org/10.1034/j.1600-0412.2001.801109.x
- Franklin, M. E., & Conner-Kerr, T. (1998). An analysis of posture and back pain in the first and third trimesters of pregnancy. Journal of Orthopaedic & Sports Physical Therapy, 28, 133–138. https://doi.org/10.2519/jospt.1998.28.3.133
- Gabbard, C. (1993). Foot laterality during childhood: A review. International Journal of Neuroscience, 72, 175–182. https://doi.org/10.3109/00207459309024106
- Gabbard, C., & Iteya, M. (1996). Foot laterality in children, adolescents, and adults. Laterality, 1, 199–205. https://doi.org/10.1080/713754236
- Gentry, V., & Gabbard, C. (1995). Foot-preference behavior: A developmental perspective. Journal of General Psychology, 122, 37–45. https://doi.org/10.1080/00221309.1995.9921220
- Giorgi, M., Carriero, A., Shefelbine, S. J., & Nowlan, N. C. (2015). Effects of normal and abnormal loading conditions on morphogenesis of the prenatal hip joint: Application to hip dysplasia. Journal of Biomechanics, 48, 3390–3397. https://doi.org/10.1016/j.jbiomech.2015.06.002
- Gnat, R., Saulicz, E., Biały, M., & Kłaptocz, P. (2009). Does pelvic asymmetry always mean pathology? Analysis of mechanical factors leading to the asymmetry. Journal of Human Kinetics, 21, 23–35. https://doi.org/10.2478/v10078-09-0003-8
- Graham, J. H., & Özener, B. (2016). Fluctuating asymmetry of human populations: A review. Symmetry, 8, 154. https://doi.org/10.3390/sym8120154
- Grattan, M. P., Vos, E., Levy, J., & McClintock, M. K. (1992). Asymmetric action in the human newborn: Sex differences in patterns of organization. Child Development, 63, 273–289. https://doi.org/10.1111/j.1467-8624.1992.tb01626.x
- Irurita Olivares, J., & Alemán Aguilera, I. (2016). Validation of the sex estimation method elaborated by Schutkowski in the Granada osteological collection of identified infant and young children: Analysis of the controversy between the different ways of analyzing and interpreting the results. International Journal of Legal Medicine, 130, 1623–1632. https://doi.org/10.1007/s00414-016-1354-z
- Kanchan, T., Kumar, M. T. S., Kumar, G. P., & Yoganarasimha, K. (2008). Skeletal asymmetry. Journal of Forensic and Legal Medicine, 15, 177–179. https://doi.org/10.1016/j.jflm.2007.05.009
- Kiapour, A., Joukar, A., Elgafy, H., Erbulut, D. U., Argawal, A. K., & Goel, V. K. (2020). Biomechanics of the sacroiliac joint: Anatomy, function, biomechanics, sexual dimorphism, and causes of pain. International Journal of Spine Surgery, 14, S3–S13. https://doi.org/10.14444/6077
- Krishan, K., Kanchan, T., & DiMaggio, J. A. (2010). A study of limb asymmetry and its effect on estimation of stature in forensic case work. Forensic Science International, 200, 181.e1–181.e5. https://doi.org/10.1016/j.forsciint.2010.04.015
- Kurki, H. K. (2017). Bilateral asymmetry in the human pelvis. The Anatomical Record, 300, 653–665. https://doi.org/10.1002/ar.23546
- Lanciotti, L., Cofini, M., Leonardi, A., Penta, L., & Esposito, S. (2018). Up-to-date review about minipuberty and overview on hypothalamic-pituitary-gonadal axis activation in fetal and neonatal life. Frontiers in Endocrinology, 9, 410. https://doi.org/10.3389/fendo.2018.00410
- Landis, J. R., & Koch, G. G. (1977). The measurement of observer agreement for categorical data. Biometrics, 33, 159–174. https://doi.org/10.2307/2529310
- Luna, H. L., Aranda, C. M., Monge Calleja, A. M., & Santos, A. L. (2021). Test of the auricular surface sex estimation method in fetuses and non-adults under 5 years old from the Lisbon and Granada reference collections. International Journal of Legal Medicine, 135, 993–1003. https://doi.org/10.1007/s00414-020-02431-9
- Luna, L. H., Aranda, C. M., & Santos, A. L. (2017). New method for sex prediction using the human non-adult auricular surface of the ilium in the collection of identified skeletons of the University of Coimbra. International Journal of Osteoarchaeology, 27, 898–911. https://doi.org/10.1002/oa.2604
- Mameli, D., Pietrobelli, A., Sorrentino, R., Nicolosi, T., Mariotti, V., & Belcastro, M. G. (2024). Entheseal variation and locomotor behavior during growth. Journal of Anatomy, 245(1), 137–155. https://doi.org/10.1111/joa.14023
- Marino, R., Tanganelli, V., Pietrobelli, A., & Belcastro, M. G. (2020). Evaluation of the auricular surface method for subadult sex estimation on Italian modern (19th to 20th century) identified skeletal collections. American Journal of Physical Anthropology, 174, 792–803. https://doi.org/10.1002/ajpa.24146
- Mason, K. A., Schoelwer, M. J., & Rogol, A. D. (2020). Androgens during infancy, childhood, and adolescence: Physiology and use in clinical practice. Endocrine Reviews, 41, 421–456. https://doi.org/10.1210/endrev/bnaa003
- Mays, S., Steele, J., & Ford, M. (1999). Directional asymmetry in the human clavicle. International Journal of Osteoarchaeology, 9, 18–28. https://doi.org/10.1002/(SICI)1099-1212(199901/02)9:1<18::AID-OA455>3.0.CO;2-A
- Mays, S. A. (2002). Asymmetry in metacarpal cortical bone in a collection of British post-mediaeval human skeletons. Journal of Archaeological Science, 29, 435–441. https://doi.org/10.1006/jasc.2002.0729
- Milner, G. R., & Boldsen, J. L. (2012). Transition analysis: A validation study with known-age modern American skeletons. American Journal of Physical Anthropology, 148, 98–110. https://doi.org/10.1002/ajpa.22047
- Monge Calleja, A. M., Aranda, C. M., Santos, A. L., & Luna, L. H. (2020). Evaluation of the auricular surface method for non-adult sex estimation on the Lisbon documented collection. American Journal of Physical Anthropology, 172, 500–510. https://doi.org/10.1002/ajpa.24012
- Monge Calleja, A. M., Luna, L. H., Aranda, C. A., & Santos, A. L. (2023). Methods for sex estimation of prepubertal individuals (< 12 years old): Bibliographic review and future directions. Anthropologischer Anzeiger, 80, 439–469. https://doi.org/10.1127/anthranz/2022/1607
- Nishi, K., Saiki, K., Oyamada, J., Okamoto, K., Ogami-Takamura, K., Hasegawa, T., Moriuchi, T., Sakamoto, J., Higashi, T., Tsurumoto, T., & Manabe, Y. (2020). Sex-based differences in human sacroiliac joint shape: A three-dimensional morphological analysis of the iliac auricular surface of modern Japanese macerated bones. Anatomical Science International, 95, 219–229. https://doi.org/10.1007/s12565-019-00513-2
- Nissinen, M. J., Heliövaara, M. M., Seitsamo, J. T., Könönen, M. H., Humerinta, K. A., & Poussa, M. S. (2000). Development of trunk asymmetry in a cohort of children ages 11 to 22 years. Spine, 25, 570–574. https://doi.org/10.1097/00007632-200003010-00007
- Özener, B. (2010). Fluctuating and directional asymmetry in young human males: Effect of heavy working condition and socioeconomic status. American Journal of Physical Anthropology, 143, 112–120. https://doi.org/10.1002/ajpa.21300
- Plochocki, J. H. (2002). Directional bilateral asymmetry in human sacral morphology. International Journal of Ostearchaeology, 12, 349–355. https://doi.org/10.1002/oa.633
- Porac, C., Coren, S., & Duncan, P. (1980). Life-span age trends in laterality. Journal of Gerontology, 35, 715–721. https://doi.org/10.1093/geronj/35.5.715
- Rocha, M., Padez, C., & Morais, M. (1998). Urbanização e idade da menarca na população Portuguesa: evolução secular (1880-90 a 1980). Antropologia Portuguesa, 15, 59–75.
- Sakamoto, A., Watanabe, G., Morito, T., Katayama, K., Kumagai, H., & Gamada, K. (2021). Changes in pelvic alignment in a woman before and after childbirth, using three-dimensional pelvic models based on magnetic resonance imaging: A longitudinal observation case report. Radiology Case Reports, 16, 3955–3960. https://doi.org/10.1016/j.radcr.2021.09.053
- Santos, A. L. (2000). A skeletal picture of tuberculosis: Macroscopic, radiological, biomolecular and historical evidence from the Coimbra identified skeletal collection. PhD. unpublished thesis. University of Coimbra.
- Schell, L. M., Johnston, F. E., Smit, D. R., & Paolone, A. M. (1985). Directional asymmetry of body dimensions among white adolescents. American Journal of Physical Anthropology, 67, 317–332. https://doi.org/10.1002/ajpa.1330670404
- Scheuer, L. (2002). A blind test of mandibular morphology for sexing mandibles in the first few years of life. American Journal of Physical Anthropology, 119, 189–191. https://doi.org/10.1002/ajpa.10098
- Schunke, G. B. (1938). Anatomy and development of sacroiliac joint in man. Anatomical Record, 72, 313–331. https://doi.org/10.1002/ar.1090720306
- Sutter, R. C. (2003). Nonmetric subadult skeletal sexing traits: I. A blind test of the accuracy of eight previously proposed methods using prehistoric known-sex mummies from northern Chile. Journal of Forensic Sciences, 48, 927–935. https://doi.org/10.1520/JFS2002302
- Tobolsky, V. A., Kurki, H. K., & Stock, J. T. (2016). Patterns of directional asymmetry in the pelvis and pelvic canal. American Journal of Human Biology, 28, 804–810. https://doi.org/10.1002/ajhb.22870
- Ubelaker, D. H., & DeGaglia, C. M. (2017). Population variation in skeletal sexual dimosphism. Forensic Science International, 278, 407.e1–407.e7. https://doi.org/10.1016/j.forsciint.2017.06.012
- van Dongen, S. (2006). Fluctuating asymmetry and developmental instability in evolutionary biology: Past, present and future. Journal of Evolutionary Biology, 19, 1727–1743. https://doi.org/10.1111/j.1420-9101.2006.01175.x
- van Dongen, S. V., Broek, C. T., Bots, J., & Galis, F. (2017). Changes of fluctuating asymmetry with age in human fetuses and young infants. Symmetry, 9, 44. https://doi.org/10.3390/sym9030044
10.3390/sym9030044 Google Scholar
- van Dongen, S. V., Cronille, R., & Lens, L. (2009). Sex and asymmetry in humans: What is the role of developmental instability? Journal of Evolutionary Biology, 22, 612–622. https://doi.org/10.1111/j.1420-9101.2008.01667.x
- Ward, A., & Pitsillides, A. (1998). Development immobilization induces failure of joint cavity formation by a process involving selective local changes in glycosaminoglycan synthesis. Transactions of the Annual Meeting of the Orthopaedic Research Society, 44, 199.
- Wilson, L. A., MacLeod, N., & Humphrey, L. T. (2008). Morphometric criteria for sexing juvenile human skeletons using the ilium. Journal of Forensic Sciences, 53, 269–278. https://doi.org/10.1111/j.1556-4029.2008.00656.x
- Yusof, N. A., Soames, R. W., Cunningham, C. A., & Black, S. M. (2013). Growth of the human ilium: The anomalous sacroiliac junction. The Anatomical Record, 296, 1688–1694. https://doi.org/10.1002/ar.22785
- Zhen, Q.; Xu, K.; Zhan, X.; Huang, F.; Wang, L.; Chen, S.; Li, J.; Yang, C.; Chen, Y.; Fan, S. 2022.
- Zlomislic, V., & Garfin, S. R. (2019). Anatomy and biomechanics of the sacroiliac joint. Techniques in Orthopaedics, 34, 70–75. https://doi.org/10.1097/BTO.0000000000000379