Klippel-Feil Syndrome: morphological findings in a 19th-century musealized skull from Viana del Bollo (Orense, Spain)

Jesús Herrerín; Enrique Dorado; Francesco M. Galassi; Elena Varotto; Rosa Dinarès Solà

doi:10.18778/1898-6773.85.2.03

Authors

Jesús Herrerín Universidad Autónoma de Madrid, Departamento de Biología, Unidad de Antropología Física, Madrid, Spain https://orcid.org/0000-0002-5175-4385
Enrique Dorado Sección de Antropología Forense, Instituto de Medicina Legal de Madrid, Madrid, Spain https://orcid.org/0000-0002-1137-2016
Francesco M. Galassi FAPAB Research Center, Avola (SR), Sicily, Italy; Department of Anthropology, Faculty of Biology and Environmental Protection, University of Lodz, Lodz, Poland; Archaeology, College of Humanities, Arts and Social Sciences, Flinders University, Adelaide, SA, Australia https://orcid.org/0000-0001-8902-3142
Elena Varotto FAPAB Research Center, Avola (SR), Sicily, Italy; Archaeology, College of Humanities, Arts and Social Sciences, Flinders University, Adelaide, SA, Australia https://orcid.org/0000-0001-6637-9402
Rosa Dinarès Solà Hospital General de Catalunya, Spain

DOI:

https://doi.org/10.18778/1898-6773.85.2.03

Keywords:

Olóriz collection, Klippel-Feil syndrome, atlanto-occipital fusion, basilar impression, facial asymmetry, enlarged parietal foramina

Abstract

The aim of this study is to show the cranial alterations that Klippel-Feil syndrome produced in a case older than 200 years. Few paleopathological case studies diagnosed as Klippel-Feil Syndrome are focused on cranial abnormalities. A skull numbered 778, belonging to the Federico Olóriz Aguilera collection (Spain, 19^thcentury AD), Universidad Complutense de Madrid, belonging to a young man born in a town in the North of Spain, was investigated. This cranium was visually inspected, hence macroscopically and paleoradiologically studied, using the images obtained through conventional radiology and CT scan imaging. In addition to the vertebral fusion between the atlas (C1) and the axis (C2), atlanto-occipital fusion, basilar impression, obliteration of the sagittal suture, enlarged parietal foramina and significant craniofacial asymmetry affecting maxillary bones, sphenoid, orbits, nasal bones and both palatines were observed. Morphological findings make it possible to diagnose a Klippel-Feil syndrome, possibly type-II, although the lack of the rest of the spinal column renders it impossible to verify other spinal anomalies. As a limitation, only the cranium and two cervical vertebrae were preserved, hence the possible involvement of the rest of the skeleton cannot be verified.

Downloads

Download data is not yet available.

References

Adeleye AO, Akinyemi RO. 2010. Cervical Klippel-Feil syndrome predisposing an elderly African man to central cord myelopathy following minor trauma. Afr Health Sci 10:302–4.
View in Google Scholar

Alonso G, Muñoz-Torres M. 2009. Displasia ósea fibrosa en un varón joven. Endocrinol Nutr 56:195–200.
View in Google Scholar DOI: https://doi.org/10.1016/S1575-0922(09)70984-2

Aufderheide AC, Rodríguez-Martín CR. 1998. The Cambridge Encyclopedia of Human Paleopathology. Cambridge: Cambridge University Press.
View in Google Scholar

Barnes E. 1994. Developmental Defects of the Axial Skeleton in Paleopathology. Colorado: University Press of Colorado.
View in Google Scholar

Benhamou J, Gensburger D, Messiaen C, Chapurlat R. 2016. Prognostic factors from and epidemiologic evaluation of fibrous dysplasia of bone in a modern cohort: the FRANCEDYS Study. J Bone and Miner Res 12:2167–72.
View in Google Scholar DOI: https://doi.org/10.1002/jbmr.2894

Boleaga-Durán B, Suárez E, Tomasini Ortiz P, Reyes J. 2006. Anatomía y patología de la unión craneovertebral. Anales de Radiología México 2:153–70.
View in Google Scholar

Bolland MJ, Cundy T. 2013. Paget’s disease of bone: Clinical review and update. J Clin Pathol 66:924–7.
View in Google Scholar DOI: https://doi.org/10.1136/jclinpath-2013-201688

Brown MW, Templeton AW, Hodges FJ. 1964. The incidence of acquired and congenital fusions of the cervical spine. Am J Roentgenol Radium Ther Nucl Med 92:1255–9.
View in Google Scholar

Buikstra JE, Ubelaker DH. 1994. Standards for data collection from human skeletal remains. Fayetteville: Arkansas Archeological Survey Research Series, No. 44.
View in Google Scholar

Chamberlain WE. 1939. Basilar impression (platybasia). A bizarre developmental anomaly of the occipital bone and upper cervical spine with striking and misleding neurologic manifectations. Yale J Biol Med 11:487–96.
View in Google Scholar

Clarke RA, Catalan G, Diwan AD. 1998. Heterogeneity in Klippel-Feil syndrome: a new classification. Pediatr Radiology 28:967–74.
View in Google Scholar DOI: https://doi.org/10.1007/s002470050511

Copley LA, Dormans JP. 1998. Cervical spine disorders in infants and children. J Am Acad Orthop Surg 6:204–14.
View in Google Scholar DOI: https://doi.org/10.5435/00124635-199807000-00002

Corral-Gudino L, Borao-Cengotita M, Pino-Montes J, Ralston S. 2013. Epidemiology of Paget’s disease of bone: A systematic review and meta-analysis of secular changes. Bone 55:347–52.
View in Google Scholar DOI: https://doi.org/10.1016/j.bone.2013.04.024

Daum REO, Jones DJ. 1998. Fiberoptic intubation in Klippel-Feil syndrome. Anaesthesia 43:18–21.
View in Google Scholar DOI: https://doi.org/10.1111/j.1365-2044.1988.tb05416.x

de Rubens-Figueroa J, Zepeda-Orozco G, González-Rosas A. 2005. Síndrome de Klippel-Feil: una enfermedad musculoesquelética, con malformaciones cardiovasculares asociadas. Bol Med Hosp Infant Mex 62:348–55.
View in Google Scholar

Dietz F. 2001. Congenital Abnormalities of the Cervical Spine. In: Weinstein SL, editor. The Pediatric Spine Principles and Practice, Second Edition. Philadelphia: Lippincott Williams & Wilkins, 239–51.
View in Google Scholar

Favus M, Vokes T. 2005. Paget disease and other dysplasias of the bone. In: Kasper DL et al., editors. Harrison’s Principles of Internal Medicine. 16th edition. New York: McGraw-Hill, 2283–4.
View in Google Scholar

Ferembach D, Schwidetzky I, Stloukal M. 1979. Recommandations pour determiner l’age et le sexe sur le squelette. Bull et Mèm. de la Soc. d’Anthrop. de Paris 6 série XIII: 7–45.
View in Google Scholar DOI: https://doi.org/10.3406/bmsap.1979.1945

Fernandes T, Costa C. 2007. Klippel–Feil syndrome with other associated anomalies in a medieval Portuguese skeleton (13th–15th century). J Anat 211:681–5.
View in Google Scholar DOI: https://doi.org/10.1111/j.1469-7580.2007.00809.x

Fietti VG, Fielding JW. 1976. The Klippel-Feil syndrome: Early roentgenographic appearance and progression of the deformity. J Bone Joint Surg 58A:891–2.
View in Google Scholar DOI: https://doi.org/10.2106/00004623-197658060-00030

Fragoso R, Cid-García A, Hernández A, Nazará Z, Cantú JM. 1982. Frontonasal dysplasia in the Klippel-Feil syndrome: a new associated malformation. Clin Genet 22: 270–3.
View in Google Scholar DOI: https://doi.org/10.1111/j.1399-0004.1982.tb01444.x

Galson DL, Roodman GD. 2014. Pathobiology of Paget’s disease of bone. J Bone Metab 21:85–98.
View in Google Scholar DOI: https://doi.org/10.11005/jbm.2014.21.2.85

Giuffra V, Vitiello A, Giusiani S, Fornaciari A, Caramella D, Villari N, Fornaciari G. Rheumatoid arthritis, Klippel-Feil syndrome and Pott’s disease in Cardinal Carlo de’ Medici (1595–1666). 2009. Clin Exp Rheumatol 27:594–602.
View in Google Scholar

Gladykowska-Rzeczycka J. 1997. A serious defect of two cervical vertebrae from a medieval cemetery in Poland; Klippel-Feil syndrome? Acta Biol Szeged 42:49–53.
View in Google Scholar

González-Reimers E, Mas-Pascual A, Arnay-de-LaRosa M, Velasco-Vázquez J, Jimenéz-Gómez MC. 2001. Klippel-Feil syndrome in the prehispanic population of El Hierro (Canary Islands). Ann Rheum Dis 60: 174.
View in Google Scholar DOI: https://doi.org/10.1136/ard.60.2.173a

Gray SW, Romaine CB, Skandalakis JE. 1964. Congenital fusion of the cervical vertebrae. Surg Gynecol Obstet 118:373–85.
View in Google Scholar

Gruber J, Saleh A, Bakhsh W, Rubery PT, Mesfin A. 2018. The prevalence of Klippel-Feil syndrome: a computed tomography-based analysis of 2,917 patients. Spine Deform 6:448–53.
View in Google Scholar DOI: https://doi.org/10.1016/j.jspd.2017.12.002

Gunderson CH, Greenspan RH, Glaser GH, Lubs H. 1967. The Klippel-Feil syndrome: Genetic and clinical reevaluation of cervical fusion. Medicine (Baltimore) 46: 491–512.
View in Google Scholar DOI: https://doi.org/10.1097/00005792-196711000-00003

Henneberg M, Otocki P. 1974. Wyniki badań antropologicznych przypadku zespołu KlippelFeila z rozszczepem podniebienia. Przegląd Antropologiczny 40:349–353.
View in Google Scholar

Hensinger RN, Lang JE, MacEwen GD. 1974. Klippel-Feil syndrome: A constellation of associated anomalies. J Bone Joint Surg 56A:1246–53.
View in Google Scholar DOI: https://doi.org/10.2106/00004623-197456060-00018

Hensinger RM, MacEwen GD. 1986. Anomalías congénitas de la Columna Vertebral. In: Rothman RH, Simeone FA (eds.), La Columna Vertebral. Madrid: Médica Panamericana, D.L. 212–344.
View in Google Scholar

Herman MJ, Pizzutillo PD. 1999. Cervical spine disorders in children. Orthop Clin North Am 30:457–66.
View in Google Scholar DOI: https://doi.org/10.1016/S0030-5898(05)70098-5

Hernández D, Lòpez A, Paz J, Menéndez YA, Amigò YA. 1980. Enfermedad de Pierre Marie–Satnton. Incidencia familiar. Rev Esp Cir Osteoartic 15:47–57.
View in Google Scholar

Herrerín J. 2004. Paleopatología. Necrópolis de El Burgo de Osma (s. XVII–XVIII). Soria, España: Soria Edita.
View in Google Scholar

Herrerín J. 2011. Paleopathological discoveries in an unusual necropolis of mendicants. Soria, Spain: Soria Edita.
View in Google Scholar

Herrerín J, Baxarias J, Garcia-Guixé E, Mas Pascual MA, Mariñoso ML. 2009. La anatomia patologica como factor clave en el diagnóstico de las displasias e hiperplasias craneofaciales: el error diagnóstico y radiológico. In: Polo-Cerda, M., García-Prosper, E. (Eds). Investigaciones histórico-médicas sobre salud y enfermedad en el pasado: actas del IX Congreso Nacional de Paleopatología, Morella (Castelló), 26–29 septiembre de 2007. Valencia: Grupo Paleolab & Sociedad Española de Paleopatología. 299–312.
View in Google Scholar

Hukeľová Z, Krošláková M. 2021. Klippel-Feil syndrome cases from Slovakia. Int J Paleopathol 33:188–195.
View in Google Scholar DOI: https://doi.org/10.1016/j.ijpp.2021.04.011

Jarcho S. 1965. Anomaly of the vertebral column (Klippel-Feil Syndrome) in American Aborigines. JAMA 193:187–8.
View in Google Scholar DOI: https://doi.org/10.1001/jama.1965.03090100089038

Jones K. 2006. Smith’s Recognizable Patterns of Human Malformation. 6th Edition, Philadelphia: Elsevier Saunders, 618–9.
View in Google Scholar

Jovankovičová A, Jakubíková J, Durovčíková D. 2012. A case of Klippel-Feil syndrome with congenital enlarged Eustachian tube. Int J Pediatr Otorhinolaryngol 76:596–600.
View in Google Scholar DOI: https://doi.org/10.1016/j.ijporl.2012.01.007

Juberg RC, Gershanik JJ. 1976. Cervical vertebral fusion (Klippel-Feil) syndrome with consanguineous parents. J Med Genet 13:246–9.
View in Google Scholar DOI: https://doi.org/10.1136/jmg.13.3.246

Kerai S, Saxena K, Taneja B. 2014. Klippel-Feil syndrome and neuraxial anaesthesia. Indian J Anaesth 58:341–3.
View in Google Scholar DOI: https://doi.org/10.4103/0019-5049.135081

Klippel M, Feil A. 1912. Un cas d’absence des vertèbres cervicales, cage thoracique remontant jusqu à la base du crâne. Nouvelle Iconographie de la Salpêtrière 25:223–50.
View in Google Scholar DOI: https://doi.org/10.3406/bmsap.1912.8505

Lewis M. 2019. Identification of Pathological Conditions in Human Skeletal Remains. 3rd Edition. London: Academic Press, 615–37.
View in Google Scholar DOI: https://doi.org/10.1016/B978-0-12-809738-0.00018-1

List CF. 1941. Neurologic syndromes accompanying developmental anomalies of occipital bone, atlas and axis. Arch Neurol Psychiatry 45:577–616.
View in Google Scholar DOI: https://doi.org/10.1001/archneurpsyc.1941.02280160009001

Lowry RB, Jabs EW, Graham GE, Gerritsen J, Fleming J. 2001. Syndrome of coronal craniosynostosis, Klippel-Feil anomaly, and Sprengel shoulder with and without Pro250Arg mutation in the FGFR3 gene. Am J Med Genet 104:112–9.
View in Google Scholar DOI: https://doi.org/10.1002/ajmg.10049

MacCurdy GG. 1923. Human skeletal remains from highlands of Peru. Am J Phys Anthropol 6:217–330.
View in Google Scholar DOI: https://doi.org/10.1002/ajpa.1330060302

Macías-López MM. 2020. Malformaciones congénitas en columna vertebral y colesteatoma en una mujer embarazada del siglo III-IV d. C. hallada en San Fernando (Cádiz). Reconstrucción de su rostro. In: De Miguel Ibáñez MP, Romero Rameta A, Torregrosa Giménez P, Jover Maestre FJ (eds.), Cuidar, curar, morir: la enfermedad leída en los huesos. Universidad de Alicante. Instituto Universitario de Investigación en Arqueología y Patrimonio Histórico, 265–85.
View in Google Scholar

Mahirogullari M, Ozkan H, Yildirim N, Cilli F, Gudemez E. 2006. Klippel–Feil syndrome and associated congenital abnormalities: evaluation of 23 cases. Acta Orthop Traumatol Turc 40:234–9.
View in Google Scholar

Menger RP, Rayi A, Notarianni C. 2022 Jan. Klippel Feil Syndrome. [Updated 2021 Sep 28]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing. Available at: https://www.ncbi.nlm.nih.gov/books/NBK493157/ [Accessed 12.01.2022].
View in Google Scholar

Martínez-Quintana E, Rodríguez-González F. 2015. Brief Report Klippel-Feil syndrome and levo-looped transposition of the great arteries. Cardiol Young 25:591–3.
View in Google Scholar DOI: https://doi.org/10.1017/S1047951114000808

Masset C. 1982. Estimation de l’âge an décès par les sutures crâniennes. Thése de Doctorat d’Etat. Lab-Anthropologie Biologique, Université Paris VII.
View in Google Scholar

Matson DD. 1969. Neurosurgery of infancy and childhood. 2nd Edition. Springfield, Illinois: Charles C. Thomas, 119–21.
View in Google Scholar

McGaughran J. 2004. Klippel–Feil Anomaly and Neural Tube Defects. Am J Med Genet 127A:327–8.
View in Google Scholar DOI: https://doi.org/10.1002/ajmg.a.20304

Menéndez-Bueyes LR, Soler-Fernández MC. 2017. Enfermedad ósea de Paget: aproximación a sus orígenes históricos. Reumatol Clin 13:66–72.
View in Google Scholar DOI: https://doi.org/10.1016/j.reuma.2016.02.008

Mohamed JY, Faqeih E, Alsiddiky A, Alshammari MJ, Ibrahim NA, Alkuraya FS. 2013. Mutations in MEOX1, encoding mesenchyme homeobox 1, cause Klippel-Feil anomaly. Am J Hum Genet 92:157–61.
View in Google Scholar DOI: https://doi.org/10.1016/j.ajhg.2012.11.016

Naikmasur VG, Sattur AP, Kirty RN, Thakur AR. 2011. Type III Klippel-Feil syndrome: case report and review of associated craniofacial anomalies. Odontology 99:197–202.
View in Google Scholar DOI: https://doi.org/10.1007/s10266-011-0004-7

Narang M, Goyal JP. 2006. Uncommon manifestations of Klippel Feil syndrome. Indian Pediatr 43:265–6.
View in Google Scholar

Nouri A, Martin AR, Lange SF, Kotter MRN, Mikulis DJ, Fehlings MG. 2017. Congenital Cervical Fusion as a Risk Factor for Development of Degenerative Cervical Myelopathy. World Neurosurg 100:531–9.
View in Google Scholar DOI: https://doi.org/10.1016/j.wneu.2017.01.048

Ortner D. 2003. Identification of pathological conditions in human skeletal remains. San Diego: Academic Press-Elsevier. 435–43.
View in Google Scholar DOI: https://doi.org/10.1016/B978-012528628-2/50054-5

Pany D, Teschler-Nicola M. 2007. Klippel-Feil Syndrome in an Early Hungarian Period Juvenile Skeleton from Austria. Int J Osteoarchaeol 17:403–15.
View in Google Scholar DOI: https://doi.org/10.1002/oa.880

Papa V, Varotto E, Vaccarezza M, Ballestriero R, Tafuri D, Galassi FM. 2020. The teaching of anatomy throughout the centuries: from Herophilus to plastination. Med Hist 3:69–77.
View in Google Scholar

Papagrigorakis MJ, Synodinos PN, Daliouris CP, Metaxotou C. 2003. De novo inv(2) (p12q34) associated with Klippel-Feil anomaly and hypodontia. Eur J Pediatr 162:594–7.
View in Google Scholar DOI: https://doi.org/10.1007/s00431-003-1262-3

Papathanasiou A. 2005. Health status of the Neolithic population of Alepotrypa Cave, Greece. Am J Phys Anthropol 126(4):377–90.
View in Google Scholar DOI: https://doi.org/10.1002/ajpa.20140

Parekh SG, Donthineni-Rao R, Ricchetti E, Lackman RD. 2004. Fibrous dysplasia. J Am Acad Orthop Surg 5:305–13.
View in Google Scholar DOI: https://doi.org/10.5435/00124635-200409000-00005

Piagkou M, Skotsimara G, Repousi E, Paraskevas G, Natsis K. 2013. Enlarged parietal foramina: a rare finding in a female Greek skull with unusual multiple Wormian bones and a rich parietal vascular network. Anat Sci Int 88:175–80.
View in Google Scholar DOI: https://doi.org/10.1007/s12565-013-0173-2

Raus I, Coroiu RX. 2016. Mc-Albright syndrome: association of fibrous dysplasia, café-au-lait skin spots and hyperthyroidism-case report. Clujul Med 89:559–64.
View in Google Scholar DOI: https://doi.org/10.15386/cjmed-624

Renaud A, Aucourt J, Weill J, Bigot J, Dieux A, Devisme L, Moraux A, Boutry N. 2013. Radiographic features of osteogenesis imperfect. Insights Imaging 4:417–29.
View in Google Scholar DOI: https://doi.org/10.1007/s13244-013-0258-4

Resnick D, Kransdorf MJ. 2006. Huesos y articulaciones en imágenes radiológicas. 3rd edition. Madrid: Elsevier.
View in Google Scholar

Resnik D, Niwayama G: Paget’s disease. 1998. In: Resnik D, Niwayama G, editors. Diagnosis of bone and joint disorders. Philadelphia: W.B. Saunders Company, 2127–70.
View in Google Scholar

Roberts T, Stephen L, Beighton P. 2013. Cleidocranial dysplasia: a review of the dental, historical, and practical implications with an overview of the South African experience. Oral Medicine 115:46–55.
View in Google Scholar DOI: https://doi.org/10.1016/j.oooo.2012.07.435

Roodman GD, Windle JJ. 2005. Paget disease of bone. J Clin Invest 115:200–8.
View in Google Scholar DOI: https://doi.org/10.1172/JCI24281

Russel SA: Skeletal Abnormalities. 2014. In: Coady AM, Bower S, editors. Twining’s Textbook of Fetal Abnormalities. Amsterdam: Elsevier, 417–50.
View in Google Scholar DOI: https://doi.org/10.1016/B978-0-7020-4591-2.00016-4

Sirico A, Maruotti GM, Martinelli P, Lanna M, Anfora R, Setaro A, Sala C. 2015. Airway management with McGrath Series 5 video laryngoscope in a woman with Klippel-Feil syndrome requiring urgent caesarean section. Int J Obstet Anaesth 24:286–8.
View in Google Scholar DOI: https://doi.org/10.1016/j.ijoa.2015.04.004

Strax TE, Baran E. 1975. Traumatic quadriplegia associated with Klippel-Feil syndrome: discussion and case reports. Arch Phys Med Rehabil 56:363–5.
View in Google Scholar

Tachdijian MO. 1990. Pediatric orthopedics, Second Edition. Philadelphia: W.B. Saunders Company, 128.
View in Google Scholar

Taylor-Martínez MA, Villanueva-Castro E, Muñoz-Romero I, De Leo-Vargas R. 2019. Síndrome de Klippel-Feil tipo 3. An Med (Mex) 64:221–4.
View in Google Scholar

Thompson EM, Baraitser M, Hayward RD. 1984. Parietal foramina in Saethre-Chotzen syndrome. J Med Genet 21:369–72.
View in Google Scholar DOI: https://doi.org/10.1136/jmg.21.5.369

Toker S, Kilincoglu V, Unay K, Erturer E, Taser F, Gulcan E, Ilhan D. 2009. Klippel–Feil syndrome with osteopoikilosis in a young lady and her four female relatives with osteopoikilosis. Clin Rheumatol 28:235–8.
View in Google Scholar DOI: https://doi.org/10.1007/s10067-008-1053-3

Urunuela G, Alvarez R. 1994. A report of Klippel-Feil Syndrome in Prehispanic remains from Cholula, Puebla, Mexico. J Paleopathol 6:63–7.
View in Google Scholar

Varotto E, Milanese M, Tognotti E, Caramella D, Montella A, Bandiera P. 2020. Klippel-Feil Syndrome in an ancient Sardinian population (16th century AD) – A paleopathological study of four cases from the S. Michele cemetery in Alghero. In: Spani G, Varotto E, editors. Malattie e medicina tra letteratura, storia e antropologia. Holden, Massachusetts: Quod Manet, 139–53.
View in Google Scholar

Vujasinovic Stupar N, Pavlov-Dolijanovic S, Hatib N, Banko B, Djukic M, Nikolic Jakoba N. 2015. Multiple Major and Minor Anomalies Associated with Klippel-Feil Syndrome: A Case Report. Arch Rheumatol 31:82–6.
View in Google Scholar DOI: https://doi.org/10.5606/ArchRheumatol.2016.5714

Warner WC. 1998. Pediatric Cervical Spine. In: Canale ST, editor. Campbell’s Operative Orthopaedics. 9th Edition. St Louis: Mosby, 2815–47.
View in Google Scholar