Paleopathological diagnosis of non-adult scurvy and rickets using decision tree analysis

Abstract

Introduction. This publication has a twofold aim: (1) to present a probable case of a metabolic disease in a Late Bronze Age child skeleton from the Southern Trans-Urals, and (2) to examine the diagnostic potential of classification tree algorithms for differentiating infantile scurvy and rickets in osteological material.

Materials and methods. The skeleton of a 4–8-month-old child with pathological changes was found in Kurgan 1 of the Nepluyevsky cemetery, attributed to the Srubnaya-Alakul cultural type. The observed pathological changes are consistent with rickets and/or scurvy. Differential diagnosis between these two conditions was performed using classification tree analysis (Statistica 12.0 package), based on 13 parameters and a dataset of 110 paleopathological cases of metabolic disorders (72 cases of rickets and 38 of scurvy). Two classification models were constructed using CHAID algorithm, each employing a different approach to handling missing data. Accuracy, sensitivity, specificity, and positive likelihood ratio were calculated to assess classification quality. In addition, correlation coefficients were computed for all input variables.

Results and discussion. The combination of macroscopic and radiographic features indicates that the child was suffering from a metabolic disorder, most consistent with rickets. The obtained decision trees demonstrate high classification accuracy (93.6%) and a high positive likelihood ratio.

Conclusion. The child from Kurgan 1 represents one of the earliest and the first reliably documented paleopathological case of rickets from the study region. The resulting decision trees show that rickets and scurvy can be differentiated using three features: long-bone deformity and general thickening, and abnormalities on bone underlying growth plates.

Acknowledgements. The article has been written in accordance with the research plans of the N.N. Miklukho-Maklai Institute of Ethnology and Anthropology RAS (Theme No. 5. Human ultrasociality: Biosocial and cross-cultural aspects – R & D No. 124112200079-1) (V.V. Kufterin). The study was conducted under the state assignment of Lomonosov Moscow State University (M.K. Karapetian).

References

Blöcher J., Brami M., Feinauer I.S., Stolarczyk E., Diekmann Y. et al. Descent, marriage, and residence practice of a 3,800-year-old pastoral community in Central Eurasia. Proc. Natl. Acad. Sci. USA, 2023, 120 (36), e2303574120. https://doi.org/ 10.1073/pnas.2303574120

Boldsen J.L. Epidemiological approach to the paleopathological diagnosis of leprosy. Am. J. Phys. Anthropol., 2001, 115, pp. 380–387.

Botha D., Masiu R., Steyn M. Assessing tuberculosis in the skeleton with the use of decision tree analysis. Anthropol. Anz., 2024, 81 (2), pp. 233–239. https://doi.org/ 10.1127/anthranz/2023/1737

Bourbou C. Evidence of childhood scurvy in a Middle Byzantine Greek population from Crete, Greece (11th – 12th centuries A.D.). Int. J. Paleopathol., 2014, 5, pp. 86–94. https://doi.org/ 10.1016/j.ijpp.2013.12.002

Brickley M., Ives R. Skeletal manifestations of infantile scurvy. Am. J. Phys. Anthropol., 2006, 129, pp. 163–172 https://doi.org/ 10.1002/ajpa.20265

Brickley M., Ives R. The Bioarchaeology of Metabolic Bone Disease. London, Academic Press, 2008. XVI, 333 p. ISBN 978-0-12-370486-3.

Brickley M., Mays S. Metabolic disease. In Ortner’s Identification of Pathological Conditions in Human Skeletal Remains. San Diego, Academic Press, 2019, pp. 531–566. https://doi.org/ 10.1016/B978-0-12-809738-0.00015-6

Brickley M.B., Mays S., George M., Prowse T.L. Analysis of patterning in the occurrence of skeletal lesions used as indicators of vitamin D deficiency in subadult and adult skeletal remains. Int. J. Paleopathol., 2018, 23, pp. 43–53. https://doi.org/ 10.1016/j.ijpp.2018.01.001

Brickley M.B., Morgan B. Assessing diagnostic certainty for scurvy and rickets in human skeletal remains. Am. J. Biol. Anthropol., 2023, 181, pp. 637–645. https://doi.org/ 10.1002/ajpa.24799.

Brown M., Ortner D.J. Childhood scurvy in a Medieval burial from Mačvanska Mitrovica, Serbia. Int. J. Osteoarchaeol., 2011, 21, pp. 197–207. https://doi.org/ 10.1002/oa.1124

Buckley H.R., Kinaston R., Halcrow S.E., Foster A., Spriggs M. et al. Scurvy in a tropical paradise? Evaluating the possibility of infant and adult vitamin C deficiency in the Lapita skeletal sample of Teouma, Vanuatu, Pacific islands. Int. J. Paleopathol., 2014, 5, pp. 72–85. https://doi.org/ 10.1016/j.ijpp.2014.03.001

Byers S.N., Roberts C.A. Bayes’ theorem in paleopathological diagnosis. Am. J. Phys. Anthropol., 2003, 121, pp. 1–9. https://doi.org/ 10.1002/ajpa.10164

Castilla M., Carretero J.-M., Gracia A., Arsuaga J.-L. Evidence of rickets and/or scurvy in a complete Chalcolithic child skeleton from the El Portalón site (Sierra de Atapuerca, Spain). J. Anthropol. Sci., 2014, 92, pp. 257–271. https://doi.org/ 10.4436/JASS.92005

Crandall J.J., Klaus H.D. Advancements, challenges, and prospects in the paleopathology of scurvy: Current perspectives on vitamin C deficiency in human skeletal remains. Int. J. Paleopathol., 2014, 5, pp. 1–8. https://doi.org/ 10.1016/j.ijpp.2014.04.005.

Creo A.L., Thacher T.D., Pettifor J.M., Strand M.A., Fischer P.R. Nutritional rickets around the world: An update. Paediatr. Int. Child Health, 2017, 37 (2), pp. 84–98. https://doi.org/ 10.1080/20469047.2016.1248170

Dangvard Pedersen D., Milner G.R., Kolmos H.J., Boldsen J.L. The association between skeletal lesions and tuberculosis diagnosis using probabilistic approach. Int. J. Paleopathol., 2019, 27, pp. 88–100. https://doi.org/ 10.1016/j.ijpp.2019.01.001

Fedorchuk O.A., Goncharova N.N. Application of the decision tree method for differentiating human groups. Archaeology, Ethnology & Anthropology of Eurasia, 2024, 52 (3), pp. 148–156. (In Russ.). https://doi.org/ 10.17746/1563-0102.2024.52.3.148-156

Ferreira M.T. A scurvy case in an infant from Monte da Cegonha (Vidigueira – Portugal). Antropologia Portuguesa, 2002, 19, pp. 57–63.

Geber J., Murphy E. Scurvy in the Great Irish Famine: Evidence of vitamin C deficiency from a mid-19th century skeletal population. Am. J. Phys. Anthropol., 2012, 148, pp. 512–524. https://doi.org/ 10.1002/ajpa.22066

Giuffra V., Vitiello A., Caramella D., Fornaciari A., Giustini D. et al. Rickets in a high social class of Renaissance Italy: The Medici children. Int. J. Osteoarchaeol., 2015, 25, pp. 608–624. https://doi.org/ 10.1002/oa.2324

Karapetian M.K., Sharapova S.V. Pathological changes on skeletons from the Bronze Age Neplyuevsky cemetery (kurgan 1). The Lower Volga Archaeological Bulletin, 2022, 21 (2), pp. 100–119. (In Russ.). https://doi.org/ 10.15688/nav.jvolsu.2022.2.6.

Klaus H.A. Subadult scurvy in Andean South America: Evidence of vitamin C deficiency in the late pre-Hispanic and Colonial Lambayeque Valley, Peru. Int. J. Paleopathol., 2014, 5, pp. 34–45. https://doi.org/ 10.1016/j.ijpp.2013.09.002

Klaus H.D. Paleopathological rigor and differential diagnosis: Case studies involving terminology, description, and diagnostic framework for scurvy in skeletal remains. Int. J. Paleopathol., 2017, 19, pp. 96–110. https://doi.org/ 10.1016/j.ijpp.2015.10.002

Lewis M. Paleopathology of Children: Identification of Pathological Conditions in the Human Skeletal Remains of Non-Adults. London, Academic Press, 2018. XI, 288 p. ISBN 978-0-12-410402-0.

Littleton J. A Middle Eastern paradox: Rickets in skeletons from Bahrain. J. Paleopath., 1998, 10 (1), pp. 13–30.

Lovász G., Schultz M., Gödde J., Bereczki Z., Pálfi Gy. et al. Skeletal manifestations of infantile scurvy in a late medieval anthropological series from Hungary. Anthropol. Sci., 2013, 121 (3), pp. 173–185. https://doi.org/ 10.1537/ase.130905

Mays S. A likely case of scurvy from Early Bronze Age Britain. Int. J. Osteoarchaeol., 2008, 18, pp. 178–187. https://doi.org/ 10.1002/oa.930

Mays S. The palaeopathology of scurvy in Europe. Int. J. Paleopathol., 2014, 5, pp. 55–62. https://doi.org/ 10.1016/j.ijpp.2013.09.001

Mays S., Brickley M. Vitamin D deficiency in bioarchaeology and beyond: The study of rickets and osteomalacia in the past. Int. J. Paleopathol., 2018, 23, pp. 1–5. https://doi.org/ 10.1016/j.ijpp.2018.05.004

Mays S., Brickley M., Ives R. Skeletal manifestations of rickets in infants and young children in a historic population from England. Am. J. Phys. Anthropol., 2006, 129, pp. 362–374. https://doi.org/ 10.1002/ajpa.20292

Mednikova M.B., Engovatova A.V., Shvedchikova T.Yu., Reshetova I.K., Vasilyeva E.E. “Interlunation children”: New data on the quality of life in Yaroslavl in the 16^th – 17^th cc. according to the anthropological materials from children burials. Brief Communications of the Institute of Archaeology, 2013, 228, pp. 115–126. (In Russ.).

Melikian M., Waldron T. An examination of skulls from two British sites for possible evidence of scurvy. Int. J. Osteoarchaeol., 2003, 13, pp. 207–212. https://doi.org/ 10.1002/oa.674

Narkevich A.N., Vinogradov K.A., Grjibovski A.M. Intelligent data analysis in biomedical research: Classification trees. Human Ecology, 2021, 3, pp. 54–64. (In Russ.). https://doi.org/ 10.33396 /1728-0869-2021-3-54-64

Ortner D.J., Butler W., Cafarella J., Milligan L. Evidence of probable scurvy in subadults from archeological sites in North America. Am. J. Phys. Anthropol., 2001, 114, pp. 343–351.

Ortner D.J., Ericksen M.F. Bone changes in the human skull probably resulting from scurvy in infancy and childhood. Int. J. Osteoarchaeol., 1997, 7, pp. 212–220.

Ortner D.J., Kimmerle E.H., Diez M. Probable evidence of scurvy in subadults from archeological sites in Peru. Am. J. Phys. Anthropol., 1999, 108, pp. 321–331.

Ortner D.J., Mays S. Dry-bone manifestations of rickets in infancy and early childhood. Int. J. Osteoarchaeol., 1998, 8, pp. 45–55.

Pinhasi R., Shaw P., White B., Ogden A.R. Morbidity, rickets and long-bone growth in post-medieval Britain – a cross-population analysis. Ann. Hum. Biol., 2006, 33 (3), pp. 372–389. https://doi.org/ 10.1080/03014460600707503

Pitre M.C., Stark R.J., Gatto M.C. First probable case of scurvy in ancient Egypt at Nag el-Qarmila, Aswan. Int. J. Paleopathol., 2016, 13, pp. 11–19. DOI: 10.1016/j.ijpp.2015.12.003.

Ribot I., Roberts C. A study of non-specific stress indicators and skeletal growth in two Mediaeval subadult populations. J. Archaeol. Sci., 1996, 23, pp. 67–79.

Rothschild B.M., Surmik D., Bertozzo F. Modern Paleopathology, The Study of Diagnostic Approach to Ancient Diseases, their Pathology and Epidemiology. Berlin, Springer Nature, 2023. XXXVI, 851 p. ISBN 978-3-031-28623-0.

Schattmann A.B. The Co-occurrence of Scurvy and Rickets in 16^th to 18^th Century Skeletal Material from Douai, France. MA in Anthropology Thesis. McMaster University, Hamilton, 2014. XIII, 212 p.

Schattmann A., Bertrand B., Vatteoni S., Brickley M. Approaches to co-occurrence: Scurvy and rickets in infants and young children of 16–18th century Douai, France. Int. J. Paleopathol., 2016, 12, pp. 63–75. https://doi.org/ 10.1016/j.ijpp.2015.12.002

Simonit R., Maudet S., Giuffra V., Riccomi G. Infantile scurvy as a consequence of agricultural intensification in the 1st millennium BCE Etruria Campana. Sci. Rep., 2023, 13 (1), 21396. https://doi.org/ 10.1038/s41598-023-48455-0

Snoddy A.M.E., Buckley H.R., Elliott G.E., Standen V.G., Arriaza B.T. et al. Macroscopic features of scurvy in human skeletal remains: A literature synthesis and diagnostic guide. Am. J. Phys. Anthropol., 2018, 167, pp. 876–895. https://doi.org/ 10.1002/ajpa.23699

Srienc-Ściesiek M.T., Richards N., Ladstätter S., Kirchengast S. Evidence of non-adult vitamin C deficiency in three early medieval sites in the Jaun/Podjuna Valley, Carinthia, Austria. Int. J. Paleopathol., 2024, 45, pp. 18–29. https://doi.org/ 10.1016/j.ijpp.2024.02.002

Stark R.J. A proposed framework for the study of paleopathological cases of subadult scurvy. Int. J. Paleopathol., 2014, 5, pp. 18–26. https://doi.org/ 10.1016/j.ijpp.2014.01.005

Veselka B., Hoogland M.L.P., Waters-Rist A.L. Rural rickets: Vitamin D deficiency in a post-Medieval farming community from the Netherlands. Int. J. Osteoarchaeol., 2015, 25, pp. 665–675. https://doi.org/ 10.1002/oa.2329

Vlok M. Technical note: The use and misuse of threshold diagnostic criteria in paleopathology. Am. J. Biol. Anthropol., 2023, 181, pp. 326–335. https://doi.org/ 10.1002/ajpa.24721

Vlok M., Oxenham M., Domett K., Trinh H.H., Minh T.T. et al. High prevalence of adult and nonadult scurvy in an early agricultural transition site from Mainland Southeast Asia was associated with decreased survivorship. Am. J. Biol. Anthropol., 2024, 185, e25011. https://doi.org/ 10.1002/ajpa.25011

Vlok M., Snoddy A.M.E., Ramesh N., Wheeler B., Standen V.G. et al. The role of dietary calcium in the etiology of childhood rickets in the past and the present. Am. J. Hum. Biol., 2023, 35 (2), e23819. https://doi.org/ 10.1002/ajhb.23819

Watts R., Valme S.-R. Osteological evidence for juvenile vitamin D deficiency in a 19th century suburban population from Surrey, England. Int. J. Paleopathol., 2018, 23, pp. 60–68. https://doi.org/ 10.1016/j.ijpp.2018.01.007

Yunkerov V.I., Grigoryev S.G., Rezvantsev M.V. Statistical Processing of Medical Research Data. St. Petersburg, Voyenno-meditsinskaya akademiya Publ., 2011. 318 p. (In Russ.). ISBN 5-94277-011-5.