Invited article
Inferring bone attribution to species through micro-Computed Tomography: A comparison of third metapodials from Homo sapiens and Ursus americanus

https://doi.org/10.1016/j.jofri.2019.08.001Get rights and content

Highlights

  • A critical knowledge gap exists regarding quantitative bear bone microarchitectural data.

  • Ca.N is significantly different between black bear and human metacarpals/pooled metapodials.

  • Osteon banding and resorption spaces are more prevalent in bear metapodials.

  • 3D analysis of bear cortical bone provides an accurate means to infer species origin.

  • 3D data reveal the usefulness of desktop µCT as a diverse tool for anthropologists.

Abstract

Gross similarities between human hand/foot bones and bear paws have been well-documented. Macroscopic skeletal analyses provide insight into species origin when whole bones are recovered but are frequently rendered inapplicable when bones are fragmented. In these scenarios, histological techniques are often applied; though specific research focusing on the quantification of bear bone microstructure remains scarce. We hypothesized that 3D analysis of bear cortical bone microarchitecture provides a more representative and accurate means to infer bone attribution to species from fragmented metapodials. Methods included visualizing and quantifying bone microstructural parameters using micro-Computed Tomography (µCT). Third metacarpals and metatarsals from mature black bears and humans were assessed using 3D analyses. Micro-CT experiments were carried out using a laboratory X-ray system at The University of Akron. Projections were reconstructed and cylindrical Volumes of Interest (VOIs) were identified within each bone sample. Variables measured within the VOIs included: total volume (TV), total canal volume (Ca.V), canal number (Ca.N), average canal diameter (Ca.Dm), and cortical porosity (Ca.V/TV). Between-species t-tests revealed that both Ca.N and Ca.Dm significantly differed between human and bear metapodials. Qualitative features including osteon banding and resorption bays were more prevalent in bear metapodials. The 3D data for this study were obtained non-destructively and reveal the usefulness of laboratory µCT as a diverse and novel tool for the anthropologist. Results demonstrated differences between the human and black bear third metapodials, supporting the hypothesis that a microstructural comparison is necessary for fragmentary bone identification of human and bear metapodials.

Introduction

The morphological similarities between human hand/foot bones and bear paws have been described extensively in the literature [1], [2], [3], [4]. While applicable when intact bones are encountered, gross morphological comparisons may prove ineffective in the context of fragmented, damaged, and/or commingled skeletal remains. Many medicolegal professionals (e.g., law enforcement) are not experts in mammalian osteological identification [5]. As such, when highly fragmented skeletal remains are encountered, standard macroscopic approaches may prove insufficient. Bone fragment identification methods must shift from the gross anatomical to histological in these scenarios in order to decipher human from nonhuman bone. A histological approach traditionally involves evaluating certain qualitative microstructural features, such as plexiform-type bone, that are considered specific to nonhuman species. In the absence of such features, distinguishing Haversian bone as either human or nonhuman may prove difficult. Determining species origin is critical in forensic contexts as the misinterpretation of bone morphology can result in detrimental mistakes, potentially leading to the misidentification of humans as nonhuman mammals or vice versa [2].

Similar to the macroscopic osteology of other mammals, black bear (Ursus americanus) front paws and human hands are composed of comparable skeletal elements (e.g., phalanges, metacarpals, and carpals) as are black bear hind paws and human feet (e.g., phalanges, metatarsals, and tarsals). When skeletal remains of black bear paws are discovered without distal phalanges and their associated claws, the metapodials are remarkably similar to human hands/feet on a gross anatomical scale [2]. The macroscopic evidence, however, only supports the morphological similarities of black bear and human metacarpals and metatarsals when intact metapodials are recovered [6]. If a partial diaphysis is encountered, for example, identification may be problematic due to gross macromorphological similarities. There is a current lack of literature comparing the histological structure of human and black bear microarchitecture on a quantitative level [2]. For example, only two studies to date include information on bear cortical bone histomorphology and focus solely on femora [7], [8]. This has implications in forensic contexts as it may result in challenges in identifying species origin, and thus impact human identification efforts when partial remains are recovered.

Using traditional two-dimensional (2D) histomorphological methods, the qualitative analysis of cortical bone primarily relies on the identification of bone type, pattern, and the organization of bone tissue. Mammalian bone often contains fibrolamellar, lamellar, woven, and/or Haversian bone tissue types [2]. Laminar fibrolamellar bone is distinguishable by circumferential lamellar layers. A brick-like pattern of fibrolamellar bone, often referred to as plexiform bone, is commonly identified in nonhuman mammalian bone and is characterized by alternating sheets of woven and lamellar bone [2], [9]. This plexiform-type arrangement of fibrolamellar bone is rarely observed in mature human bone. Haversian bone, or secondary osteonal bone, is more difficult to distinguish between human and nonhuman species. This bone type refers to bundles of lamellar bone tissue with a central Haversian (vascular) canal. The concentric lamellae are defined by a cement or reversal line, which is the primary distinguishing feature of secondary osteonal bone tissue. Haversian bone is documented in various avian, reptilian, and mammalian species, including humans [10]. Thus, the presence of Haversian bone is not diagnostic of human bone as it is less distinctive between humans and nonhumans.

Primary and secondary osteons are recognized to form linear bands, particularly in young fast-growing animals or species with localized growth rates. This pattern, described as distinct rows of five or more primary and/or secondary osteons [11] has been reported as a strong indicator of nonhuman bone [6], [11], [12], [13], [14]. A recent study by Andronowski et al. [15], however, documented the first three-dimensional (3D) examination of inter-element variation in osteon banding in adult human cortical bone. The authors warn that though osteon banding can be suggestive of nonhuman bone, the frequent occurrence of osteon banding and the presence of multiple bands within single human specimens, indicate that this histomorphological feature alone is not diagnostic of nonhuman bone.

A critical knowledge gap exists regarding quantitative bear bone microarchitectural data. This lack of information is considered significant due to the global presence of bear species. Thus, the objectives of the current research are to investigate whether: (1) microstructural differences exist between human and black bear metacarpals and metatarsals through the use of a novel non-destructive 3D imaging approach (i.e., micro-Computed Tomography; µCT) and (2) these microstructural data can aid in species identification efforts when bone fragments are discovered in a forensic context. It is hypothesized that the 3D analysis of bear cortical bone microstructure provides a more representative and accurate means to infer species origin from fragmented metapodials.

Section snippets

Materials and methods

Adult black bear (Ursus americanus) metapodials were loaned from the Department of Vertebrate Zoology at the Cleveland Museum of Natural History, with metacarpals and metatarsals each examined from five mature individuals. Adult human metacarpal (n = 5) and metatarsal (n = 5) specimens were sourced from cadaveric donors at The University of Toledo, College of Medicine and Life Sciences. Bear bone and human bone maturity were based on epiphyseal fusion with no visible fusion lines. Documented

Results

Descriptive statistics, including sample mean, range, standard error (SEM), and standard deviation were computed for all variables. Homogeneity of variance was assessed using Levene's test. Normality of raw data was examined using Kolmogorov-Smirnov tests, which revealed that certain data were not normally distributed. A log transformation was employed to correct this issue.

Independent samples t-tests demonstrated that Ca.N was significantly different between black bear and human metacarpals (t

Discussion

To our knowledge, the work presented here represents the first use of µCT to document microarchitectural differences between black bear and human metapodials. The microstructural data we offer addresses an evident knowledge gap in nonhuman bone literature within the field of forensic anthropology. Although μCT imaging is not available to all forensic anthropologists, the ultimate goal of this work was to quantitatively assess the microstructural differences between black bear and human

Conclusion

Macroscopic skeletal analyses provide insight into species origin when whole bones are recovered but are frequently rendered insufficient when skeletal remains are fragmented. The current work demonstrated that µCT is a valuable tool for 3D reconstructions of bear bone microarchitecture and can be used for species identification in forensic contexts. We hypothesized that our microarchitectural data will provide a more representative and accurate means to infer species origin from fragmented

Funding

JMA is supported through start-up research funds provided by The University of Akron. RAD is funded by a graduate assistantship provided by The University of Akron.

Declaration of Competing Interest

None.

Acknowledgments

The authors would like to thank the Cleveland Museum of Natural History Mammal Department, specifically Dr. Tim Matson, for access to the black bear specimens and Beth Dalzell at The University of Toledo College of Medicine and Life Sciences for granting access to cadaveric samples for this study. The authors would further like to thank Dr. Andrew Knoll of The University of Akron National Polymer Innovation Center for his assistance with imaging using the SkyScan 1172 µCT system, and Dr. Mary

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