The Diagnostic Implications of Two Cases of Known Rheumatoid Arthritis from the CAL Milano Cemetery Skeletal Collection
Corresponding Author
Lucie Biehler-Gomez M.S.
LABANOF, Laboratorio Di Antropologia E Odontologia Forense, Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La Salute, Università Degli Studi Di Milano, Via Mangiagalli 37, Milan, 20133 Italy
Additional information and reprint requests:
Lucie Biehler-Gomez, B.Sc., M.S.
LABANOF, Laboratorio di Antropologia e Odontologia Forense Sezione di Medicina Legale
Dipartimento di Scienze Biomediche per la Salute
Università degli Studi di Milano
Via Mangiagalli 37
20133 Milan
Italy
E-mail: [email protected]
Search for more papers by this authorCristina Cattaneo M.D., Ph.D.
LABANOF, Laboratorio Di Antropologia E Odontologia Forense, Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La Salute, Università Degli Studi Di Milano, Via Mangiagalli 37, Milan, 20133 Italy
Search for more papers by this authorCorresponding Author
Lucie Biehler-Gomez M.S.
LABANOF, Laboratorio Di Antropologia E Odontologia Forense, Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La Salute, Università Degli Studi Di Milano, Via Mangiagalli 37, Milan, 20133 Italy
Additional information and reprint requests:
Lucie Biehler-Gomez, B.Sc., M.S.
LABANOF, Laboratorio di Antropologia e Odontologia Forense Sezione di Medicina Legale
Dipartimento di Scienze Biomediche per la Salute
Università degli Studi di Milano
Via Mangiagalli 37
20133 Milan
Italy
E-mail: [email protected]
Search for more papers by this authorCristina Cattaneo M.D., Ph.D.
LABANOF, Laboratorio Di Antropologia E Odontologia Forense, Sezione Di Medicina Legale, Dipartimento Di Scienze Biomediche per La Salute, Università Degli Studi Di Milano, Via Mangiagalli 37, Milan, 20133 Italy
Search for more papers by this authorAbstract
Rheumatoid arthritis (RA) is the most common erosive arthropathy and is of particular interest to forensic sciences. However, its diagnosis on bones remains challenging. We examined two skeletons from the CAL Milano Cemetery Skeletal Collection diagnosed with the pathology during life, to test the validity of the diagnostic criteria on bones. The first showed typical lesions of RA described in the literature. The second exhibited secondary osteoarthrosis, suggesting long-standing RA. A differential diagnosis including all four seronegative spondyloarthropathies, erosive osteoarthritis, gout and neuropathic arthropathy was also considered. Both shared common features consistent with the literature: symmetric erosions of bones in the hands, wrists and elbows, sparing of the distal interphalangeal joints, and the absence of sacroiliac and spinal fusion. Given the paucity of studies on known RA skeletons, these results strengthen the criteria for diagnosis. This research is, to our knowledge, the first study on identified and known individuals with RA.
References
- 1Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology 2012; 51(Suppl 5): v3–11.
- 2Lee DM, Weinblatt ME. Rheumatoid arthritis. Lancet 2001; 358(9285): 903–11.
- 3Rindfleisch JA, Muller D. Diagnosis and management of rheumatoid arthritis. Am Fam Physician 2005; 72(6): 1037–47.
- 4Silman AJ, Pearson JE. Epidemiology and genetics of rheumatoid arthritis. Arthritis Res Ther 2002; 4(3): S265.
- 5Smolen JS, Aletaha D, McInnes IB. Rheumatoid arthritis. Lancet 2016; 388(10055): 2023–38.
- 6Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003; 423(6937): 356–61.
- 7Vigorita VJ, Ghelman B. Arthritis. In: VJ Vigorita, B Ghelman, editors. Orthopaedic pathology. Philadelphia, PA: Lippincott Williams & Wilkins, 2016; 710–68.
- 8Wright V, Londino AV Jr. Inflammatory arthritis. In: RH Fitzgerald, H Kaufer, AL Malkani, editors. Orthopaedics. St Louis, MO: Mosby, 2002; 819–25.
- 9Ortner DJ. Erosive arthropathies, enthesopathies and miscellaneous pathological conditions of joints. In: DJ Ortner, editor. Identification of pathological conditions in human akeletal eemains. New York, NY: Smithsonian Institution Press, 2003; 561–88.
10.1016/B978-012528628-2/50059-4 Google Scholar
- 10Alamanos Y, Drosos AA. Epidemiology of adult rheumatoid arthritis. Autoimmun Rev 2005; 4(3): 130–6.
- 11Entezami P, Fox DA, Clapham PJ, Chung KC. Historical perspective on the etiology of rheumatoid arthritis. Hand Clin 2011; 27(1): 1–10.
- 12Majithia V, Geraci SA. Rheumatoid arthritis: diagnosis and management. Am J Med 2007; 120(11): 936–9.
- 13McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365(23): 2205–19.
- 14Edwards CJ, Cooper C. Early environmental factors and rheumatoid arthritis. Clin Exp Immunol 2006; 143(1): 1–5.
- 15Henrique da Mota LM, Afonso Cruz B, Viegas Brenol C, Alves Pereira I, Rezende-Fronza LS, Barros Bertolo M, et al. Guidelines for the diagnosis of rheumatoid arthritis. Rev Bras Reumatol Engl Ed) 2013; 53(2): 141–57.
- 16Cojocaru M, Cojocaru IM, Silosi I, Vrabie CD, Tanasescu R. Extra-articular manifestations in rheumatoid arthritis. Mædica 2010; 5(4): 286–91.
- 17Lopez-Mejias R, Castaneda S, Gonzalez-Juanatey C, Corrales A, Ferraz-Amaro I, Genre F, et al. Cardiovascular risk assessment in patients with rheumatoid arthritis: the relevance of clinical, genetic and serological markers. Autoimmun Rev 2016; 15(11): 1013–30.
- 18 AC Aufderheide, C Rodríguez-Martín, editors. Joint diseases. In: The Cambridge encyclopedia of human paleopathology. Cambridge, U.K.: Cambridge University Press, 1998; 93–116.
- 19 T Waldron, editor. Diseases of joints, part 2. In: Paleopathology. Cambridge, U.K.: Cambridge University Press, 2008; 46–71.
10.1017/CBO9780511812569.005 Google Scholar
- 20Rothschild BM. Not the Lucy, not the one. Clin Exp Rheumatol 2002; 20(6): 741–3.
- 21 FS Chew, editor. Approach to joint disease. In: Skeletal radiology: the bare bones. Philadelphia, PA: Lippincott Williams & Wilkins, 2012; 196–206.
- 22Firestein GS. Rheumatoid arthritis. In: HD Humes, HL DuPont, LB Gardner, JW Griffin, ED Harris, WR Hazzard, et al., editors. Kelley's textbook of internal medicine. Philadelphia, PA: Lippincott Williams & Wilkins, 2000; 1347–59.
- 23 CA Roberts, K Manchester, editors. Joint disease. In: The archaeology of disease. Ithaca, NY: Cornell University Press, 1995; 99–123.
- 24Rogers J, Waldron T, Dieppe P, Watt I. Arthropathies in palaeopathology: the basis of classification according to most probable cause. J Archaeol Sci 1987; 14(2): 179–93.
- 25Rogers J, Watt I, Dieppe P. Medical history: arthritis in Saxon and mediaeval skeletons. Br Med J (Clin Res Ed) 1981; 283(6307): 1668–70.
- 26Banks SE. Erosive osteoarthritis: a current review of a clinical challenge. Clin Rheumatol 2010; 29(7): 697–706.
- 27Sommer OJ, Kladosek A, Weiler V, Czembirek H, Boeck M, Stiskal M. Rheumatoid arthritis: a practical guide to state-of-the-art imaging, image interpretation, and clinical implications. Radiographics 2005; 25(2): 381–98.
- 28Erickson AR, Cannella AC, Mikuls TR. Clinical features of rheumatoid arthritis. In: GS Firestein, R Budd, SE Gabriel, IB McInnes, JR O'Dell, editors. Kelley and Firestein's textbook of rheumatology. Philadelphia, PA: Elsevier Health Sciences, 2017; 1167–86.
10.1016/B978-0-323-31696-5.00070-X Google Scholar
- 29Kacki S. Erosive polyarthropathy in a Late Roman skeleton from northern France: a new case of rheumatoid arthritis from the pre-Columbian Old Word? Int J Paleopathol 2013; 3(1): 59–63.
- 30Veale DJ, Fearon U. What makes psoriatic and rheumatoid arthritis so different? RMD Open 2015; 1(1): e000025.
- 31Zias J, Mitchell P. Psoriatic arthritis in a fifth-century Judean Desert monastery. Am J Phys Anthropol 1996; 101(4): 491–502.
10.1002/(SICI)1096-8644(199612)101:4<491::AID-AJPA4>3.0.CO;2-Z CAS PubMed Web of Science® Google Scholar
- 32Middlemiss JH. Ankylosing spondylitis. J Fac Radiol 1956; 7(3): 155–66.
- 33Rothschild BM, Woods RJ. Spondyloarthropathy: erosive arthritis in representative defleshed bones. Am J Phys Anthropol 1991; 85(2): 125–34.
- 34Kim HJ, Nemani VM, Riew KD, Brasington R. Cervical spine disease in rheumatoid arthritis: incidence, manifestations, and therapy. Curr Rheumatol Rep 2015; 17(2): 9.
- 35Jurik AG. Imaging the spine in arthritis – a pictorial review. Insights Imaging 2011; 2(2): 177–91.
- 36Kim DK, Lee IS, Kim W, Lee JS, Koh BJ, Kim MJ, et al. Possible rheumatoid arthritis found in the human skeleton collected from the tomb of Joseon Dynasty, Korea, dating back to the 1700s AD. Int J Osteoarchaeol 2011; 21(2): 136–49.
- 37Leden I, Forslind K, Svensson B. Ankylosis of wrist and small joints of the hand occurs in rheumatoid arthritis: diagnostic implication in paleopathology. Int J Paleopathol 2012; 2(4): 249–51.
- 38Brahee DD, Pierre-Jerome C, Kettner NW. Clinical and radiological manifestations of the rheumatoid wrist. A comprehensive review. J Manipulative Physiol Ther 2003; 26(5): 323–9.
- 39Preston SH. Human mortality throughout history and prehistory. In: JL Simon, editor. The state of humanity. Oxford, U.K.: Blackwell Publishers Ltd, 1995; 30–6.
- 40Thould AK, Thould BT. Arthritis in Roman Britain. Br Med J (Clin Res Ed) 1983; 287(6409): 1909–11.
- 41Blondiaux J, Cotten A, Fontaine C, Hänni C, Bera A, Flipo R. Two Roman and medieval cases of symmetrical erosive polyarthropathy from Normandy: anatomico-pathological and radiological evidence for rheumatoid arthritis. Int J Osteoarchaeol 1997; 7(5): 451–66.
- 42Hacking P, Allen T, Rogers J. Rheumatoid arthritis in a medieval skeleton. Int J Osteoarchaeol 1994; 4(3): 251–5.
10.1002/oa.1390040310 Google Scholar
- 43Cawley WD, Paine RR. Skeletal indicators of reactive arthritis: a case study comparison to other skeletal conditions, such as rheumatoid arthritis, ankylosing spondylitis, ankylosing sero-negative SpA, and DISH. Int J Paleopathol 2015; 11: 70–4.
- 44Rothschild BM, Turner KR, DeLuca MA. Symmetrical erosive peripheral polyarthritis in the Late Archaic Period of Alabama. Science 1988; 241(4872): 1498–501.
- 45Punzi L, Ramonda R, Sfriso P. Erosive osteoarthritis. Best Pract Res Clin Rheumatol 2004; 18(5): 739–58.
- 46Hoffman GS. Polyarthritis: the differential diagnosis of rheumatoid arthritis. Semin Arthritis Rheum 1978; 8(2): 115–41.
- 47Cattaneo C, Mazzarelli D, Cappella A, Castoldi E, Mattia M, Poppa P, et al. A modern documented Italian identified skeletal collection of 2127 skeletons: the CAL Milano Cemetery Skeletal Collection. Forensic Sci Int. 2018.
- 48Ortner DJ. Osteoarthritis and diffuse idiopathic skeletal hyperostosis. In: DJ Ortner, editor. Identification of pathological conditions in human skeletal remains. New York, NY: Smithsonian Institution Press, 2003; 545–60.
10.1016/B978-012528628-2/50058-2 Google Scholar
- 49 T Waldron, editor. Diseases of joints, part 1. In: Paleopathology. Cambridge, U.K.: Cambridge University Press, 2008; 24–45.
10.1017/CBO9780511812569.004 Google Scholar
- 50Ortner DJ. Identification of pathological conditions in human skeletal remains, 3rd edn. New York, NY: Smithsonian Institution Press, 2003.
- 51Aufderheide AC, Rodríguez-Martín C. The Cambridge encyclopedia of human paleopathology. Cambridge, U.K.: Cambridge University Press, 1998.
- 52Benjamin M, McGonagle D. The anatomical basis for disease localisation in seronegative spondyloarthropathy at entheses and related sites. J Anat 2001; 199(5): 503–26.
- 53Šlaus M, Novak M, Čavka M. Four cases of ankylosing spondylitis in medieval skeletal series from Croatia. Rheumatol Int 2012; 32(12): 3985–92.
- 54Mays S, Watt I, Loe L. An unusual erosive arthropathy from Medieval England. Int J Osteoarchaeol 2016; 27(4): 693–9.
- 55Fitzgerald RH, Kaufer H, Malkani AL. Orthopaedics. St Louis, MO: Mosby, 2002.
- 56Waldron T. Paleopathology. Cambridge, U.K.: Cambridge University Press, 2008.
10.1017/CBO9780511812569 Google Scholar
- 57Raychaudhuri SP, Deodhar A. The classification and diagnostic criteria of ankylosing spondylitis. J Autoimmun 2014; 48–49: 128–33.
- 58Braun J, Sieper J. Ankylosing spondylitis. Lancet 2007; 369(9570): 1379–90.
- 59Jadon DR, McHugh NJ. Other seronegative spondyloarthropathies. Medicine (Baltimore) 2014; 42(5): 257–61.
10.1016/j.mpmed.2014.02.008 Google Scholar
- 60Lahu A, Backa T, Ismaili J, Lahu V, Saiti V. Modes of presentation of reactive arthritis based on the affected joints. Med Arch 2015; 69(1): 42–5.
- 61Resende GG, Lanna CCD, Bortoluzzo AB, Gonçalves CR, Sampaio-Barros PD, da Silva JAB, et al. Enteropathic arthritis in Brazil: data from the Brazilian registry of spondyloarthritis. Rev Bras Reumatol Engl Ed 2013; 53(6): 452–9.
- 62Richette P, Bardin T. Gout. Lancet 2010; 375(9711): 318–28.
- 63Monu JUV, Pope TL Jr. Gout: a clinical and radiologic review. Radiol Clin North Am 2004; 42(1): 169–84.
- 64Stanley JC, Collier AM. Charcot osteo-arthropathy. Curr Orthop 2008; 22(6): 428–33.