Recognition of sickle cell anemia in skeletal remains of children

American Journal of Physical Anthropology

Volumn 104, Issue 2, 1997, Pages 213-226

  Hershkovitz, Israel ^a,c   Rothschild, Bruce M ^b   Latimer, Bruce ^a,d   Dutour, Olivier ^e   Léonetti, Georges ^e   Greenwald, Charles M ^a   Rothschild, Christine ^b   Jellema, Lyman M ^a  

^a CLEVELAND MUSEUM OF NATURAL HISTORY   (United States)

^b NORTHEAST OHIO MEDICAL UNIVERSITY   (United States)

^c TEL AVIV UNIVERSITY   (Israel)

^d CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

Anemia; Bone pathology; Children; Iron deficiency

Indexed keywords

BONE DISEASE; CALVARIA; CASE REPORT; CHILD; CONFERENCE PAPER; CONTROLLED STUDY; CORTICAL BONE; DEMINERALIZATION; FEMUR; HUMAN; HUMAN TISSUE; HYPEROSTOSIS; IRON DEFICIENCY ANEMIA; MALE; OSTEOPOROSIS; SICKLE CELL ANEMIA; SKELETON; TIBIA;

ADOLESCENT; ANEMIA, IRON-DEFICIENCY; ANEMIA, SICKLE CELL; BONE AND BONES; CHILD; CHILD, PRESCHOOL; DIAGNOSIS, DIFFERENTIAL; FEMALE; FEMUR; HEMATOPOIETIC SYSTEM; HUMANS; HYPEROSTOSIS; MALE; METACARPUS; OSTEOPOROSIS; PELVIC BONES; RADIUS; SHOULDER; SKULL; SPINE; THALASSEMIA; TIBIA; ULNA;

EID: 0030665565     PISSN: 00029483     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-8644(199710)104:2<213::AID-AJPA8>3.0.CO;2-Z     Document Type: Conference Paper

References (103)

1. Aksoy M, Camli N, and Erdem S (1966) Roentgenographic bone changes in chronic iron deficiency anemia. Blood 27:677-685.
2. Angel JL (1966) Porotic hyperostosis. anemias, malarias in marshes in the prehistoric eastern Mediterranean. Science 153:760-763.
3. Argen RJ and Sullivan MA (1966) Bone changes in sickle cell disease. N.Y. State J. Med. 5:1238-1243
4. Arman MI, Butun B, Doseyen A, Bircan I, and Guven A (1992) Frequency and features of rheumatic findings in thalassaemia minor: A blind controlled study. Br. J. Rheumatol. 31:197-199.
5. Babhulkar SS, Pande K, and Babhulkar S (1995) The hand-foot syndrome in sickle-cell heamoglobinopathy. J. Bone Joint Surg. 77[B]:310-312.
6. Baker M, and Demos TC (1982) Skeletal manifestations of blood disorders. Orthopedics 5:754-773.
7. Barton CJ, and Cockshott WP (1962) Bone changes in hemoglobin SC disease. Am. J. Roentgenol. 88:523-532
8. Bass WM (1987) Human Osteology. Columbia, Missouri Archaeological Society (no. 2).
9. Bastian HM (1995) Hematologic disorders including sickle-cell syndromes, hemophilia and B-thalassemia. Curr. Opin. Rheumatol. 7:70-72.
10. Britton HA, Canby JP, and Kohler CM (1960) Iron deficiency anemia producing evidence of marrow hyperplasia in calvarium. Pediatrics 25:621-628.
11. Buikstra JE, Pozanaski A, Cerna ML, and Hoshower LM (1990) A case of juvenile rheumatoid arthritis from pre-Columbian Peru. In: A Life in Science: Papers in Honour of J. Lawrence Angel. Chicago: Center for American Archaeology Scientific Papers no. 6, pp. 99-137.
12. Burko H, Mellins HZ, and Watson J (1961) Skull changes in iron deficiency anemia simulating congenital hemolithic anemia. Am. J. Roentgen. Rad. Ther. 86:447-452.
13. Burko H, Watson J, and Robinson M (1963) Unusual bone changes in sickle-cell disease in childhood. Radiology 80:957-962.
14. Caffey J (1937) The skeletal changes in the chronic hemolytic anemias. Am. J. Roentgenol. 37:293-324.
15. Caffey J (1952) Cooley's erythroblastic anemia: Some skeletal findings in adolescents and young adults. Am. J. Roentgenol. 65:547-560.
16. Carroll DS (1957) Roentgen manifestations of sickle cell disease. South. Med. J. 50:1486-1490.
17. Carroll DS, and Evans JW (1949) Roentgen findings in sickle-cell anemia. Radiology 53:834-845.
18. Cassady JR, Berdon WE, and Baker DH (1967) The "typical" spine changes of sickle-cell anemia in a patient with thalassemia major (Cooley's anemia). Radiology 89:1065-1068.
19. Coley TB, and Lee P (1926) The sickle cell phenomenon. Am. J. Dis. Child 32:334-340.
20. Cooley TB, Witwer ER, and Lee P (1927) Anemia in children with splenomegaly and peculiar changes in bones. Am. J. Dis. Child 34:347-363.
21. Currarino G, and Erlandson ME (1964) Premature fusion of the epiphyses in Cooley's anemia. Radiology 83:656-664.
22. Dardel R, and Gerster J-C (1983)Arthrities recidivantes au cours de la thalassemie mineure. Rhumatologie 35:221-225.
23. deCeulaer K, Forbes M, Roper D, and Serjeant GR (1984) Non-gouty arthritis in sickle cell disease: Report of 37 consecutive cases. Ann. Rheum. Dis. 43:599-603.
24. Demirjian A (1980) Dental development: A measure of physical maturation. In FE Johnston, AF Roche, and C Susanna (eds.): Human Physical Growth and Maturation: Methodologies and Factors. New York: Plenum, pp. 83-100.
25. Diggs LW (1967) Bone and joint lesions in sickle-cell disease. Clin. Orthop. 52:119-143.
26. Diggs LW, Pulliam HN, and King JC (1937) The bone changes in sickle-cell anemia. South. Med. J. 30:249-259.
27. Dorwart BB, and Schumacher HR (1981) Arthritis in B thalassaemia trait: Clinical and pathological features. Ann. Rheum. Dis. 40:185-189.
28. Ehrenpreis B, and Schwinger HN (1952) Sickle-cell anemia. Am. J. Roentgenol. 68:28-36.
29. El-Najjar MY, and Robertson A (1976) Spongy bone in prehistoric America. Science 193:141-143.
30. El-Najjar MY, Lozoff B, and Ryan J (1975) The paleoepidemiology of porotic hyperostosis in the American Southwest: Radiological and ecological considerations. Am. J. Roentgenol. 25:918-924.
31. Eng LL (1958) Chronic iron deficiency anemia with bone changes resembling Cooley's anemia. Acta Haematol. 19:263-268.
32. Espinoza LR, Spilberg I, and Osterland CK (1974) Joint manifestations of sickle cell disease. Medicine 53:295-305.
33. Exarchou E, Politou C, Vretou E, Pasparakis D, Madessis G, and Caramerou A (1984) Fractures and epiphyseal deformities in beta-thalassemia. Clin. Orthop. 189:229-233.
34. Fairbanks VF, and Beutler E (1995) Iron Deficiency. In E Beutler, MALichtman, BS Coller, and TJ Kipps (eds.): Williams Hematology. 5th ed. New York: McGraw-Hill, pp. 490-535.
35. Finch CA (1970) Diagnostic value of different methods to detect iron deficiency. In L Hallberg, HG Harwerth, and A Vannotti (eds.): Iron Deficiency, Pathogenesis, Clinical Aspects, Therapy. New York: Academic, pp. 409-421.
36. Fink IJ, Pastakaia B, and Barranger JA (1984) Enlarged phalangeal foramina in Gaucher disease and B-thalassemia major. Am. J. Roentgenol. 143:647-649.
37. Gorriz L, De Leon C, Herrero-Beaumont G, and del Vallado PF (1983) Arthritis in beta-thalassemia minor. Arthritis Rheum. 26:1292-1923.
38. Graham GS (1924) Case of sickle cell anemia with necropsy. Arch. Intern. Med. 34:778-800.
39. Gratwick GM, Bullough PG, Bohne WH, Markenson AL, and Peterson CM (1978) Thalassemic osteoarthropathy. Ann. Intern. Med. 88:494-501.
40. Hanker GJ, and Amstutz HC (1988) Osteonecrosis of the hip in the sickle-cell diseases. J. Bone Joint Surg. 70[A]:499-506.
41. Hernigou P, Galacteros F, Bachir D, and Goutallier D (1989) Etude de 164 necroses epiphysaires (hanches, epaules, genoux) chez 55 patients drepanocytaires: Caracteristiques, aspect epidemiologique et etiopathogenique. Rev. Rhum. 56:869-875.
42. Hernigou P, Galacteros F, Bachir D, and Goutallier D (1991) Deformities of the hip in adults who have sickle-cell disease and had avascular necrosis in childhood. J. Bone Joint Surg. 73[A]:81-92.
43. Herrick JB (1910) Peculiar elongated sickle-shaped red blood corpuscles in a case of severe anemia. Arch. Intern. Med. 6:517-523.
44. Hershkovitz I, Ring B, Speirs M, Galili E, Kislev M, Edelson G, and Hershkovitz A (1991) Possible congenital hemolytic anemia in prehistoric coastal inhabitants of Israel. Am. J. Phys. Anthropol. 85:7-13.
45. Herskovitz MJ (1924) Some observation on the growth of colored boys. Am. J. Phys. Anthropol. 7:439-446.
46. Hewett B, and van Nice CM (1964) Radiographic manifestations of sickle-cell anemia. Radiol. Clin. North Am. 2:249-259.
47. Hooton EA (1930) Indians of Pecos Pueblo. New Haven: Yale University Press.
48. Johanson NA (1990) Musculoskeltal problems in hemoglobinopathy. Orthop. Clin. North Am. 21:191-198.
49. Kaklamanis P (1984) Osteoartieular manifestations in sickle-cell disorders. Clin. Rheumatol. 3:419-434.
50. Kanyerezi BR, Ndugwa C, Owor R, Sinagabula SM, Masembe J, Nzaro E, and Bosa JL (1974) The spinal column in sickle cell disease. J. Rheumatol. 1(Suppl 1):21.
51. Karayalcin G, Dorfman J, Rosner F, and Aballi AJ (1976) Radiologie changes in 127 patients with sickle-cell anemia. Am. J. Med. Sci. 271:133-144.
52. Keitel W, Fuchs R, Weber G, and Lutze G (1976) Ungewohnliche Gelenkbeteiligung bei Sichelzellanaemie. Zschr. Inn. Med. 31:998-1000.
53. Korovessis PG, Milis ZT, Spastris PM, Urania P, and Spyropoulos P (1990) Acetabular protrusion in thalassemia. Clin. Orthop. 254:199-204.
54. Lagundoye SB (1970) Radiological features of sickle-cell anaemia and related haemoglobinopathies in Nigeria. Afr. J. Med. Sci. 1:315-342.
55. Lallo J, Armelagos G, and Mensforth R (1977) The role of diet, disease and physiology in the origin of porotic hyperostosis. Hum. Biol. 49:471-483.
56. Lanzkowsky P (1968) Radiologic features of iron-deficiency anemia. Am. J. Dis. Child 116:16-29.
57. Lawson JP, Ablow RC, and Pearson HA (1981) The ribs in thalassemia. II. The pathogenesis of the changes. Radiology 140:673-679.
58. Lawson JP, Ablow RC, and Pearson HA (1984) Calvarial and phalangeal vascular impressions in thalassemia. Am. J. Roentgenol. 143:641-645.
59. Lee RE, Golding JS, and Serjeant GR (1981) The radiological features of avascular necrosis of the femoral head in homozygous sickle cell disease. Clin. Radiol. 32:205-214.
60. Leichtman DA, Bigongiari LR, and Wicks JD (1978) The incidence and significance of tibiotalar slant in sickle cell anemia. Skeletal Radiol. 3:99-101.
61. Levine MS, Borden S, and Gill FM (1982) Sternal cupping: A new finding in childhood sickle-cell anemia. Radiology 142:367-370.
62. Mensforth R (1985) The pathogenetic and biodemographic consequences of porotic hyperostosis and periosteal reactions in earlier human groups. Am. J. Phys. Anthropol. 66:206 (abstract).
63. Mensforth R, Lovejoy CO, Lallo J, and Armelagos G (1978) The role of constitutional factors, diet and infectious disease in the etiology of porotic hyperostosis and periosteal reactions in prehistoric infants and children. Med. Anthropol. 2:1-59.
64. Moore S (1929) Bone changes in sickle cell anemia with a note on similar changes in skulls of ancient Mayan Indians. J. Missouri Med. Assoc. 26:561-564.
65. Moseley JE (1929a) Patterns of bone change in the anemias. J. Mount Sinai Hosp. 29:109-120.
66. Moseley JE (1929b) The thalassemias: Variants and roentgen bone changes. J. Mount Sinai Hosp. 29:199-214.
67. Moseley JE (1963) Bone Changes in Hematologic Disorders. New York: Grune and Stratton.
68. Moseley JE (1974) Skeletal changes in the anaemias. Semin. Roentgenol. 9:169-184.
69. Mourshed F, and Tuckson CR (1974) A study of radiographic features of the jaws in sickle cell anemia. Oral. Surg. 37:812-000.
70. Ortner D, and Putschar W (1981) Identification of pathological conditions in human skeletal remains. Smithsonian Contributions to Anthropology, no. 28.
71. Orzincolo C, Castaldi G, Scutellari PN, and Franceschini F (1989) The "lamellated" skull in B-thalasaemia. Skeletal Radiol. 18:313-376.
72. Palmer DW (1975) Septic arthritis in sickle-cell thalassemia. Arthritis Rheum. 18:339-345.
73. Palkovich AM (1987) Endemic disease patterns in paleopathology: Porotic hyperostosis. Am. J. Phys. Anthropol. 14:527-537.
74. Patel A (1973) Arthropathy in sickle cell disease. N. Engl. J. Med. 288:970-972.
75. Prowler JR, and Smith EW (1955) Dental bone changes occuring in sickle-cell diseases and abnormal hemoglobin traits. Radiology 65:762-769.
76. Redman DS, and Nelson CL (1985) Osteoarthropathy in thalassemia minor. Orthopedics 8:81-83.
77. Resnick D, and Niwayama G (1988) Diagnosis of Bone and Joint Disorders. Philadelphia: Saunders.
78. Reynolds J (1966) A re-evaluation of the "fish vertebra" sign in sickle cell hemoglobinopathy. Radiology 57:693-707.
79. Reynolds MD (1983) Gout and hyperuricemia associated with sickle-cell anemia. Semin. Arthritis Rheum. 12: 404-413.
80. Rioja L, Girot R, Garabedian M, and Cournot-Witmer G (1990) Bone disease in children with homozygous B-thalassemia. Bone Mineral 8:69-86.
81. Robinson IB, and Sarnat EG (1962) Roentgen studies of the maxillae and manible in sickle-cell anemia. Radiology 58:517-523.
82. Rodnan GP (1965) Arthritis associated with hematologic disorders. Bull. Rheumatic Dis. 16:392-395.
83. Rothschild BM, and Sebes JI (1981) Calcaneal abnormalities and erosive bone disease associated with sickle cell anemia. Am. J. Med. 71:427-430.
84. Rothschild BM, and Martin LD (1993) Paleopathology: Disease in the Fossil Record. London: CRC.
85. Rothschild BM, and Rothschild C (1995) Treponemal disease revisited: Skeletal discriminators for yaws, bejel, and veneral syphilis. Clin. Infect. Dis. 20:1402-1408.
86. Scutellari PN, Orzincolo C, and Tamarozzi R (1985) Xeroradiography in B-thalassaemia. Skeletal Radiol. 13:39-43.
87. Sebes JI, and Diggs LW (1979) Radiographic changes of the skull in sickle cell anemia. Am. J. Roentgenol. 132:373-377.
88. Shahidi NT and Diamond LK (1960) Skull changes in infants with chronic iron-deficiency anemia. New Eng. J. Med. 262:137-139.
89. Shaub MS, Rosen R, Boswell W, and Gordonson J (1975) Tibiotalar slant: A new observation in sickle cell anemia. Radiology 117:551-552.
90. Simmons K (1944) The Brush Foundation study of child growth and development. Part II. Physical growth and development. Monographs of the Society for Research in Child growth and Development. V. IX, No. 1, pp. 8-87.
91. Simmons K, and Todd TW (1938) Growth of well children: Analysis of stature and weight 2 month to 13 years. Growth 2:93-134.
92. Soni NN (1966) Microradiographic study of dental tissue in sickle cell anemia. Arch. Oral Biol. 11:561-000.
93. Sherman M (1959) Pathogenesis of disintegration of the hip in sickle cell anemia. South. Med. J. 52:632-637.
94. Stuart-Macadam P (1987a) A radiographic study of porotic hyperostosis. Am. J. Phys. Anthropol. 74:511-520.
95. Stuart-Macadam P (1987b) Porotic hyperostosis: New evidence to support the anemia theory. Am. J. Phys. Anthropol. 74:521-526.
96. Trowell HC, Raper AB, and Welbourn HF (1957) The natural history of homozygous sickle-cell anemia in Central Africa. Q. J. Med. 26:401-123.
97. Uhelaker DH (1987) Estimating age at death from immature human skeletons: An overview. J. Forensic Sci. 32:1254-1263.
98. Ubelaker DH (1989) The estimation of age at death from immature human bones. In MY Iscan (ed.): Age Markers in the Human Skeleton. Springfield, IL: CC Thomas, pp. 55-70.
99. Walker P (1985) Anemia among prehistonc Indians ot the American Southwest. In CF Merbs and RJ Miller (eds.): Health and Disease in the Prehistoric Southwest. Arizona State University Anthropological Research Papers, no. 34, pp. 139-164.
100. Walker P (1986) Porotic hyperostosis in marine-dependent California Indian populations. Am. J. Phys. Anthropol. 69:345-354.
101. Watson RJ, Burko H, Megas H, and Robinson M (1963) The hand-foot syndrome in sickle-cell disease in young children. Pediatrics 31:975-982.
102. Worrall VT and Butera V (1976) Sickle-cell dactylitis. J. Bone Joint Surg. 58[A]:1161-1163.
103. Zimmerman MR, and Kelley MA (1982) Atlas of Human Paleopathology. New York: Praeger.