Differentiating human bone from animal bone: A review of histological methods

Journal of Forensic Sciences

Volumn 52, Issue 2, 2007, Pages 249-263

  Hillier, Maria L ^a   Bell, Lynne S ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Cortical bone; Forensic anthropology; Forensic science; Histology; Histomorphometry; Human identification; Mammals; Microscopy; Scanning electron microscopy; Species determination

Indexed keywords

BONE STRUCTURE; BONE TISSUE; BUFFALO; CADAVER; CAT; CERCOPITHECIDAE; CHIMPANZEE; CORTICAL BONE; COW; DEER; DIAGENESIS; GOAT; HARE; HAVERSIAN CANAL; HISTOLOGY; HORSE; HUMAN; MACACA; MAMMAL; MICROSCOPY; NONHUMAN; PRIMATE; PRIORITY JOURNAL; RACCOON DOG; REVIEW; SHEEP; SPECIES DIFFERENCE; SWINE; TISSUE TYPES;

AGE DETERMINATION BY SKELETON; ANIMALS; BONE AND BONES; BUFFALOES; CATS; CATTLE; DEER; DOGS; FORENSIC ANTHROPOLOGY; GOATS; HORSES; HUMANS; MICROSCOPY, ELECTRON, SCANNING; MUSTELIDAE; POSTMORTEM CHANGES; PRIMATES; RABBITS; RACCOON DOGS; RATS; SEX CHARACTERISTICS; SHEEP; SPECIES SPECIFICITY; SWINE;

EID: 33847147231     PISSN: 00221198     EISSN: 15564029     Source Type: Journal    
DOI: 10.1111/j.1556-4029.2006.00368.x     Document Type: Review

References (129)

1. Mayne Correia P, Beattie O. A critical look at methods for recovering, evaluating and interpreting cremated human remains. In: Haglund W, Sorg M, editors. Advances in forensic taphonomy: method, theory and archaeological perspectives. London: CRC Press, 2001:435-50.
2. Warren MW, Eisenberg LE, Walsh-Haney H, Saul JM. Anthropology at fresh kills: recover and identification of the World Trade Center victims. In: Proceedings of the 55th annual meeting of the American Academy of Forensic Sciences; February 17-22, 2003. Chicago, IL. Colorado Springs, CO: American Academy of Forensic Sciences, 2003:278.
3. Zelson Mundorff A. The role of anthropology during the identification of victims from the World Trade Center disaster. In: Proceedings of the 55th annual meeting of the American Academy of Forensic Sciences; February 17-22, 2003. Chicago, IL. Colorado Springs, CO: American Academy of Forensic Sciences, 2003:277-8.
4. Rodriguez WC. Attack on the Pentagon: the role of forensic anthropology in the examination and identification of victims and remains of the '9/11' terrorist attack. In: Proceedings of the 55th Annual Meeting of the American Academy of Forensic Sciences; February 17-22, 2003. Chicago, IL. Colorado Springs, CO: American Academy of Forensic Sciences, 2003:280-1.
5. Owsley DW, Mires AM, Keith MS. Case involving differentiation of deer and human bone fragments. J Forensic Sci 1984;30(2):572-8.
6. Dix JD, Stout SD, Mosley J. Bones, blood, pellets, glass and no body. J Forensic Sci 1991;36(3):949-52.
7. Harsányi L. Differential diagnosis of human and animal bone. In: Grupe G, Garland AN, editors. Histology of ancient human bone: methods and diagnosis. Proceedings of the Palaeohistopathology Workshop; Ocober 3-5, 1990, Göttingten, Germany. London: Springer-Verlag, 1993:79-94.
8. Rajtová V, Briancin J, Kokardova M. Lamellar bone structure in small ruminants. Folia Vet 1995;39:59-64.
9. Hidaka S, Matsumoto M, Ohsako S, Toyoshima Y, Nishinakagawa H. A histometrical study on the long bones of raccoon dogs, Nyctereutes procyonoides and badgers, Meles meles. J Vet Med Sci 1998;60(3):323-6.
10. Mulhern DM, Ubelaker DH. Differences in osteon banding between human and nonhuman bone. J Forensic Sci 2001;46:220-2.
11. Benedix D. Differentiation of fragmented bone from Southeast Asia: the histological evidence [dissertation]. Knoxville, TN: University of Tennessee-Knoxville, 2004.
12. Whitman EJ. Differentiating between human and non-human secondary osteons in human, canine and bovine rib tissue [thesis]. East Lansing, MI: Michigan State University, 2004.
13. Lackey WL. Distinguishing between human and canine bone using Haversian system size and Haversian canal diameter. Proceedings of the 53rd Annual Meeting of the American Academy of Forensic Sciences; February 19-24, 2001; Seattle, WA. Colorado Springs, CO: American Academy of Forensic Sciences, 2001:251.
14. Walter TL, Paine RR, Horni H. Histological examination of bone-tempered pottery from mission Espíritu Santo (41VT11), Victoria County, Texas. J Arch Sci 2004;31:393-8.
15. Stout SD, Ross LM. Bone fragments a body can make. J Forensic Sci 1991;36(3):953-7.
16. Quekett J. On the intimate structure of bone as composing the skeleton in the four great classes of animals: mammals, birds, reptiles, and fishes, with some remarks on the great value of the knowledge of such structure in determining the affinities of minute fragments of organic remains. Trans Microsc Soc Lond 1849;2:40-2.
17. Foote JS. A contribution to the comparative histology of the femur. Smithsonian Contrib Knowl 1913;35(3):1-242.
18. Enlow DH, Brown SO. A comparative histological study of fossil and recent bone tissue, part I. Tex J Sci 1956;7(4):405-43.
19. Enlow DH, Brown SO. A comparative histological study of fossil and recent bone tissue, part II. Tex J Sci 1957;9(2):186-214.
20. Enlow DH, Brown SO. A comparative histological study of fossil and recent bone tissue, part III. Tex J Sci 1958;10(2):187-230.
21. Singh IJ, Tonna EA, Gandel CP. A comparative histological study of mammalian bone. J Morphol 1974;144:421-38.
22. Enlow DH. An evaluation of the use of bone histology in forensic medicine and anthropology. In: Evans FG, editor. Studies on the anatomy and function of bones and joints. Springer-Verlag: Berlin, 1966:93-112.
23. Garland AN. Microscopic analysis of fossil bone. Appl Geochem 1989;4:215-29.
24. Stout SD, Simmons DJ. Use of histology in ancient bone research. Yearb Phys Anthropol 1979;22:228-49.
25. Bell LS, Piper K. An introduction to paleohistopathology. In: Cox M, Mays S, editors. Human osteology in archaeology and forensic science. London: Greenwich Medical Media, 2000:255-74.
26. Schultz M. Paleohistopathology of bone: a new approach to the study of ancient diseases. Yearb Phys Anthropol 2001;44:106-47.
27. Martin DL. Microstructural examination: possibilities for skeletal analysis. In: Martin DL, Bumstead MP, editors. Biocultural adaptation: comprehensive approaches to skeletal analysis. Research reports number 20. Amherst, MA: University of Massachusetts Press, 1981:96-104.
28. Schultz M. Microscopic investigation of excavated skeletal remains: a contribution to paleopathology and forensic medicine. In: Haglund WD, Sorg MH, editors. Forensic taphonomy: the postmortem fate of human remains. London: CRC Press, 1997b:201-22.
29. Stout SD. The effects of long-term immobilization on the histomorphology of human cortical bone. Calcif Tissue Int 1982;34:337-42.
30. Burr DB, Ruff CB, Thompson DD. Patterns of skeletal histologic change through time: comparison of an Archaic Native American population with modern populations. Anat Rec 1990;226:307-13.
31. Mulhern DM, Van Gerven DP. Patterns of femoral bone remodeling dynamics in a Medieval Nubian population. Am J Phys Anthropol 1997;104:133-46.
32. Thompson DD. Age changes in bone mineralization, cortical thickness and Haversian canal area. Calcif Tissue Int 1980;31:5-11.
33. Burr DB. The relationship among physical, geometrical, and mechanical properties of bone, with a note on the properties of nonhuman primate bone. Yearb Phys Anthropol 1980;23:109-46.
34. Cho H, Stout S, Madsen RW, Streeter MA. Population-specific histological age-estimating method: a model for known African-American and European-American skeletal remains. J Forensic Sci 2002;47(1):12-8.
35. Pfeiffer S. Variability in osteon size in recent human populations. Am J Phys Anthropol 1998;106(2):219-27.
36. Abbott S, Trinkaus E, Burr DB. Dynamic bone remodeling in later Pleistocene fossil hominids. Am J Phys Anthropol 1996;99:585-601.
37. Kerley ER. The microscopic determination of age in human bone. Am J Phys Anthropol 1965;23:149-64.
38. Ahlqvist J, Damsten O. A modification of Kerley's method for the microscopic determination of age in human bone. J Forensic Sci 1969;14:205-12.
39. Kerley ER, Ubelaker DH. Revisions in the microscopic method of estimating age at death in human cortical bone. Am J Phys Anthropol 1978;49:545-6.
40. Thompson DD. Age changes in bone mineralization, cortical thickness and Haversian canal area. Calcif Tissue Int 1989;31:5-11.
41. Stout SD. The use of cortical bone histology to estimate age at death. In: Ican MY, editor. Age markers on the human skeleton. Springfield, IL: Charles C. Thomas, 1989:195-207.
42. Stout SD, Paine RR. Brief communication: histological age estimation using rib and clavicle. Am J Phys Anthropol 1992;87:111-5.
43. Ubelaker DH. Estimation of age at death from histology of human bone. In: Zimmerman MR, Angel JA, editors. Dating and age determination of biological materials. London: Croom Helm, 1986:240-7.
44. Stout SD. Methods of determining age at death using bone microstructure. In: Saunders SD, Katzenberg MA, editors. Skeletal biology of past peoples: research methods. Chichester: Wiley-Liss, 1992:21-36.
45. Ubelaker DH. The evolving role of the microscope in forensic anthropology. In: Reichs KJ, editor. Forensic osteology: advances in the identification of human remains. 2. Springfield, IL: Charles C. Thomas, 1998:514-52.
46. Symes SS, Berryman HE, Smith OC. Saw marks in bone: introduction and examination of residual kerf contour. In: Reichs KJ, editor. Forensic osteology: advances in the identification of human remains. 2. Springfield, IL: Charles C. Thomas, 1998:389-409.
47. Bartelink EJ, Wiersema JM, Demaree RS. Quantitative analysis of sharp-force trauma: an application of scanning electron microscopy in forensic anthropology. J Forensic Sci 2001;46(6):1288-93.
48. Tucker BR, Hutchinson DL, Gilliland MFG, Charles TIM, Daniel HJ, Wolfe LD. Microscopic characteristics of hacking trauma. J Forensic Sci 2001;46(2):234-40.
49. Herrmann B. Light microscopy of excavated human bone. In: Grupe G, Garland AN, editors. Histology of ancient human bone: methods and diagnosis. Proceedings of the palaeohistopathology workshop; October 3-5, 1990. Göttingten, Germany. London: Springer-Verlag, 1993:17-26.
50. Ubelaker DH. Human skeletal remains: excavation, analysis, interpretation. 2. Washington: Taraxacum, 1989.
51. Bell LS, Skinner MF, Jones SJ. The speed of post mortem change to the human skeleton and its taphonomic significance. Forensic Sci Int 1996;82:129-40.
52. Bell LS. Postmortem microstructural change to the skeleton [dissertation]. London, UK: University College London, 1996.
53. Bell LS, Boyde A, Jones SJ. Diagenetic alteration of teeth in situ illustrated by backscattered electron imaging. Scanning 1991;13:173-83.
54. Bell LS, Jones SJ. Macroscopic and microscopic evaluation of archaeological pathological bone: backscattered electron imaging of putative Paget's disease. Int J Osteoarchaeol 1991;1:179-84.
55. Bell LS, Wong FS, Elliott JC, Boyde A, Jones SJ. Postmortem changes in buried human bone. J Anat 1996;183:196.
56. Jans MME, Nielsen-Marsh CM, Smith CI, Collins MJ, Kars H. Characterisation of microbial attack on archaeological bone. J Arch Sci 2004;31:87-95.
57. Bradtmiller B, Buikstra JE. Effects of burning on human bone microstructure: a preliminary study. J Forensic Sci 1984;29:535-40.
58. Shipman P, Foster G, Schoeninger M. Burnt bones and teeth: an experimental study of color, morphology, crystal structure and shrinkage. J Arch Sci 1984;2:307-25.
59. Nelson R. A microscopic comparison of fresh and burned bone. J Forensic Sci 1992;37:1055-60.
60. Cattaneo C, Dimartino S, Scali S, Craig OE, Grandi M, Sokol RJ. Determining the human origin of fragments of burnt bone: a comparative study of histological, immunological and DNA techniques. Forensic Sci Int 1999;102:181-91.
61. Tersigni MA. Frozen human bone: a histological investigation [thesis]. Knoxville, TN: University of Tennessee-Knoxville, 2002.
62. Andrews P, Nesbit Evans EM. Small mammal bone accumulations produced by mammalian carnivores. Paleobiology 1983;9(3):289-307.
63. Andrews P. Owls, caves and fossils. London: National History Museum, 1990.
64. Bell LS, Cox G, Sealy JC. Determining life history trajectories using bone density fractionation and stable light isotope analysis: a new approach. Am J Phys Anthrop 2001;116:66-79.
65. Schultz M. Microscopic structure of bone. In: Haglund WD, Sorg MH, editors. Forensic taphonomy: the postmortem fate of human remains. London: CRC Press, 1997a:187-99.
66. Martin RB. Skeletal biology. In: Martin RB, Burr DB, Sharkey NA, editors. Skeletal tissue mechanics. New York: Springer, 1998.
67. Klevezal GA. Recording structures of mammals: determination of age and reconstruction of life history. Rotterdam: A.A. Balkema, 1996.
68. Francillon-Viellot H, de Buffrénil V, Castanet J, Géraudie J, Meunier FJ, Sire JY et al. Microstructure and mineralization of vertebrate skeletal tissues. In: Carter JG, editor. Skeletal biomineralization: patterns, processes and evolutionary trends, Vol. 1. New York: Van Nostrand Reinhold, 1997:471-530.
69. Enlow DH. Principles of bone remodeling. Springfield, IL: Charles C. Thomas, 1963.
70. Currey JD. The many adaptations of bone. J Biomech 2003;36:1487-95.
71. Sommerfeldt DW, Rubin CT. Biology of bone and how it orchestrates the form and function of the skeleton. Eur Spine J 2001;10:S86-S95.
72. Currey JD. Bones: structures and mechanics. Oxford: Princeton University Press, 2002.
73. Jowsey J. Age and species differences in bone. Cornell Vet 1968;58:74-94.
74. Malluche HH, Faugere MC. Bone biopsies: histology and histomorphometry of bone. In: Avioli LV, Krane Sm, editors. Metabolic bone disease. London: WB Saunders, 1990:283-328.
75. de Ricqlès A, Meunier FJ, Castanet J, Francillon-Viellot H. Comparative microstructure of bone. In: Hall BK, editor. Bone. Vol. 3: bone matrix and bone specific products. London: CRC Press, 1990:1-78.
76. Ten Cate AR. Oral histology: development, structure, and function. 2. St. Louis: Mosby-Year Book, 1985.
77. Jaworski ZFG. Three dimensional view of the gross and microscopic structures of adult human bone. In: Jaworski ZFG, editor. Proceedings of the first workshop on bone morphometry; March 28-1, 1973, Ottawa, Canada. Ottawa, Canada: University of Ottawa Press, 1976:3-7.
78. Stout SD. Small bones of contention. In: Steadmen DW, editor. Hard evidence: case studies in forensic anthropology. Upper Saddle River, NJ: Prentice Hall, 2003:234-44.
79. Enlow DH. Handbook of facial growth. Philadelphia: W.B. Saunders, 1975.
80. Bartisiokas A. Hominid cranial bone structure: a histological study of Omo 1 specimen from Ethiopia using different microscopic techniques. Anat Rec 2002;267:52-9.
81. Curtis JM. Estimation of age at death from the microscopic appearance of the frontal bone [thesis]. Indianapolis, IN: University of Indianapolis, 2003.
82. Stout SD. Estimating time since death: the use of histological methods in forensic anthropology. In: Reichs KJ, editor. Forensic osteology: advances in the identification of human remains. 2. Springfield, IL: Charles C. Thomas, 1998:237-52.
83. Stout SD, Lueck R. Bone remodeling rates and skeletal maturation in three archaeological skeletal population. Am J Phys Anthropol 1995;98:161-71.
84. Pratte DG, Pfeiffer S. Histological age estimation of a cadaveral sample of diverse origins. Can Soc Forensic Sci J 1999;32(4):155-67.
85. Dudar CJ, Pfeiffer S, Saunders SR. Evaluation of morphological and histological adult skeletal age-at-death estimation techniques using ribs. J Forensic Sci 1993;38(3):677-85.
86. Georgia R, Albu I. The Haversian canal network in the femoral compact bone in some vertebrates. Morphol Histol Embryol: Morphol Embryol 1998;34(3):155-9.
87. Albu I, Georgia R, Georoceanu M. The canal system in the diaphyseal compacta of the femur in some animals. Anat Anzeiger 1990;170(3/4):181-7.
88. Skedros JG, Sybrowsky CL, Parry TR, Bloebaum RD. Regional differences in cortical bone organization and microdamage prevalence in Rocky Mountain mule deer. Anat Rec 2003;274A:837-50.
89. Skedros JG, Hunt KJ, Bloebaum RD. Relationships of loading history and structural and material characteristics of bone: development of the mule deer calcaneus. J Morphol 2004;259:281-307.
90. Stover SM, Pool RR, Martin RB, Morgan JP. Histological features of the dorsal cortex of the third metacarpal bone mid-diaphysis during postnatal growth in thoroughbred horses. J Anat 1992;181:455-69.
91. Mori R, Kodaka T, Sano T, Yamagishi N, Asari M, Nait Y. Comparative histology of the laminar bone between young calves and foals. Cell Tissues Org 2003;175:43-50.
92. Mulhern DM, Ubelaker DH. Histological examination of bone development in juvenile chimpanzees. Am J Phys Anthropol 2003;122(2):127-33.
93. Burr DB. Estimated intracortical bone turnover in the femur of growing macaques: implications for their use as models in skeletal pathology. Anat Rec 1992;232:180-9.
94. Havill LM. Osteon remodeling dynamics in Macaca mulatta: normal variation with regard to age, sex and skeletal maturity. Calcified Tissue Int 2004;74:95-102.
95. Havill LM. Osteon remodeling dynamics in the Cayo Santiago Macaca mulatta: the effect of the matriline. Am J Phys Anthropol 2003;121:354-60.
96. Pirock DJ, Ramser JR, Takahashi H, Villaneuva AR, Frost HM. Normal histological, tetracycline and dynamic parameters in human, mineralized bone section. Henry Ford Hosp Med J 1966;14:195-218.
97. Jowsey J. Studies of Haversian systems in man and some animals. J Anat 1966;100(4):857-64.
98. Mulhern DM. Rib remodeling dynamics in a skeletal population from Kulubnarti, Nubia. Am J Phys Anthropol 2000;111:519-30.
99. Frost HM. Human Haversian system measurements. Henry Ford Hosp Med J 1961;9:145-7.
100. Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV. Osteonal structure in the equine third metacarpus. Bone 1996;19(2):165-71.
101. Baltadjiev G. Micromorphometric characteristics of osteons in compact bone of growing tibiae of human fetuses. Acta Anat 1995;154:181-5.
102. Scheuer L, Black S. Developmental juvenile osteology. London: Academic Press, 2000.
103. Singh IJ, Gunberg DL. Estimation of age at death in human males from quantitative histology of bone fragments. Am J Phys Anthropol 1970;33:373-81.
104. Przybeck TR. Histomorphology of the rib: bone mass and cortical remodeling. In: Davis RT, Leathers CW, editors. Behaviour and pathology in aging rhesus monkeys. New York: Alan R. Liss, 1985:303-26.
105. Evans FG. Bone and bone. J Biomech Eng 1982;104:1-5.
106. Weinstein RS. Clinical use of bone biopsy. In: Coe FL, Favus MJ, editors. Disorders of bone and mineral metabolism. New York: Raven Press, 1992:455-74.
107. Evans FG, Bang S. Physical and histological differences between human fibular and femoral compact bone. In: Evans FG, editor. Studies on the anatomy and function of bones and joints. Berlin: Springer-Verlag, 1966:142-55.
108. Schaffler MB, Burr DB. Primate cortical bone microstructure: relationship to locomotion. Am J Phys Anthropol 1984;65:191-7.
109. Fazekas IG, Kósa F. Forensic fetal osteology. Budapest: Akadémiai Kiádo, 1978.
110. Weiner S, Traub W, Wagner HD. Lamellar bone: structure-function relations. J Struct Biol 1999;126:241-55.
111. Bell LS. Palaeopathology and diagenesis: an SEM evaluation of structural changes using backscattered electron imaging. J Arch Sci 1990;17:85-102.
112. Smith RW, Walker RR. Femoral expansion in aging women: implications for osteoporosis and fractures. Science 1964;145:156-7.
113. Ruff CB, Hayes WC. Subperiosteal expansion and cortical remodeling of the human femur and tibia with aging. Science 1982;217:945-8.
114. Bell KL, Loveridge N, Reeve J, Thomas CDL, Feik SA, Clement JG. Super-osteons (remodeling clusters) in the cortex of the femoral shaft: influence of age and gender. Anat Rec 2000;264:378-86.
115. Mason MW, Skedros JG, Bloebaum RD. Evidence of strain-mode-related cortical adaptation in the diaphysis of the horse radius. Bone 1995;17(3):229-37.
116. Currey JD. Some effects of ageing in human Haversian systems. J Anat 1964;98(1):69-75.
117. Evans FG. Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 1976;185:1-12.
118. Burton P, Nyssen-Behets C, Dhem A. Haversian bone remodeling in the human fetus. Acta Anat 1989;135:171-5.
119. Currey JD. Differences in the tensile strength of bone of different histological types. J Anat 1959;93:87-95.
120. Martin RB, Burr DB. Structure, function and adaptation of compact bone. New York: Raven Press, 1989.
121. Jaworski ZFG. Bone histomorphometry: outline of theory and practice. In: Kunin AS, Simmons DJ, editors. Skeletal research: an experimental approach, Vol. 2. London: Academic Press, 1983:238-76.
122. Kanis JA. Pathophysiology and treatment of Paget's disease of bone. 2. Martin Dunitz: London, 1998.
123. Roodman DG, Windle JJ. Paget disease of bone. J Clin Invest 2005;115(2):200-8.
124. Simon LS. Osteoporosis. In: Rubenstein E, Dale DC, Federman DD, editors. Scientific American medicine. New York: Scientific American, 1997:5-13.
125. Meunier PJ. Assessment of bone turnover by histomorphometry in osteoporosis. In: Riggs BL, Melton LJ, editors. Osteoporosis: etiology, diagnosis and management. New York: Raven Press, 1988:317-32.
126. Chaplin RE. The study of animal bones form archaeological sites. London: Seminar Press, 1971.
127. Young DR, Niklowitz WJ, Brown RJ, Jee WSS. Immobilization-associated osteoporosis in primates. Bone 1986;7:109-17.
128. Lyman RL. Vertebrate taphonomy. Cambridge manual in archaeology. New York: Cambridge University Press, 1994.
129. Ericksen MF. Comparison of two methods of estimating age at death in a Chilean preceramic population. Int J Osteoarchaeol 1997;7:65-70.