Anatomical Science International

, Volume 92, Issue 4, pp 554–568 | Cite as

Anatomy, histology and elemental profile of long bones and ribs of the Asian elephant (Elephas maximus)

  • Korakot NganvongpanitEmail author
  • Puntita Siengdee
  • Kittisak Buddhachat
  • Janine L. Brown
  • Sarisa Klinhom
  • Tanita Pitakarnnop
  • Taweepoke Angkawanish
  • Chatchote Thitaram
Original Article


This study evaluated the morphology and elemental composition of Asian elephant (Elephas maximus) bones (humerus, radius, ulna, femur, tibia, fibula and rib). Computerized tomography was used to image the intraosseous structure, compact bones were processed using histological techniques, and elemental profiling of compact bone was conducted using X-ray fluorescence. There was no clear evidence of an open marrow cavity in any of the bones; rather, dense trabecular bone was found in the bone interior. Compact bone contained double osteons in the radius, tibia and fibula. The osteon structure was comparatively large and similar in all bones, although the lacuna area was greater (P < 0.05) in the femur and ulna. Another finding was that nutrient foramina were clearly present in the humerus, ulna, femur, tibia and rib. Twenty elements were identified in elephant compact bone. Of these, ten differed significantly across the seven bones: Ca, Ti, V, Mn, Fe, Zr, Ag, Cd, Sn and Sb. Of particular interest was the finding of a significantly larger proportion of Fe in the humerus, radius, fibula and ribs, all bones without an open medullary cavity, which is traditionally associated with bone marrow for blood cell production. In conclusion, elephant bones present special characteristics, some of which may be important to hematopoiesis and bone strength for supporting a heavy body weight.


Bone CT scan Elephant Mineral Osteon 



Magnesium (12)


Aluminum (13)


Silicon (14)


Phosphorus (15)


Sulfur (16)


Potassium (19)


Calcium (20)


Titanium (22)


Vanadium (23)


Chromium (24)


Manganese (25)


Iron (26)


Nickel (28)


Copper (29)


Zinc (30)


Zirconium (30)


Silver (47)


Cadmium (48)


Tin (50)


Antimony (51)


Lead (82)


Light element from H = hydrogen (1) to Na = sodium (11)



The authors are grateful for research funding from the Chiang Mai University (CMU) through the research administration office, which provided a budget to the Center of Excellence in Elephant Research and Education.

Authors’ contribution

KN. is a major contributor and designed and conducted all the experiments. K.N. and S.K. scanned all samples in this study using XRF. K.N. performed the CT scans and histology of compact bone. T.P. measured the osteon structures. C.T. and T.A. gave advice and supplied rare samples used in this study. K.N., K.B. and P.S. analyzed all data and performed statistical analysis. K.N, K.B. and J.B. assisted in discussions and writing of the manuscript. All authors read and approved the manuscript to published.

Compliance with ethical standards

Ethical approval

No ethical approval was required for this study.

Conflict of interest

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.


  1. Amr AM (2011) Trace elements in Egyptian teeth. Int J Phys Sci 6:6241–6245Google Scholar
  2. Bessis MC, Breton-Gorius J (1962) Iron metabolism in the bone marrow as seen by electron microscopy: a critical review. Blood 19:635–663PubMedGoogle Scholar
  3. Brodziak-Dopierała B, Kwapuliński J, Sobczyk K, Wiechuła D (2015) Analysis of the content of cadmium and zinc in parts of the human hip joint. Biol Trace Elem Res 163:73–80CrossRefPubMedGoogle Scholar
  4. Buddhachat K, Klinhom S, Siengdee P et al (2016a) Elemental analysis of bone, teeth, horn and antler in different animal species using non-invasive handheld X-ray fluorescence. PLoS One 11:e0155458CrossRefPubMedPubMedCentralGoogle Scholar
  5. Buddhachat K, Thitaram C, Brown JL et al (2016b) Use of handheld X-ray fluorescence as a non-invasive method to distinguish between Asian and African elephant tusks. Sci Rep 6:24845CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chanpiwat P, Sthiannopkao S (2014) Status of metal levels and their potential sources of contamination in Southeast Asian rivers. Environ Sci Pollut Res Int 21:220–223CrossRefPubMedGoogle Scholar
  7. Chongsuvivatwong V, Kaeosanit S, Untimanon O (2011) Twenty-six tons of lead oxide used per year in wooden boat building and repairing in southern Thailand. Environ Geochem Health 33:301–307CrossRefPubMedGoogle Scholar
  8. Chovancová H, Martiniaková M, Omelka R, Grosskopf B, Toman T (2011) Structural changes in femoral bone tissue of rats after intraperitoneal administration of nickel. Pol J Environ Stud 20:1147–1152Google Scholar
  9. Christensen AM, Smith MA, Thomas RM (2012) Validation of X-ray fluorescence spectrometry for determining osseous or dental origin of unknown material. J Forensic Sci 57:47–51CrossRefPubMedGoogle Scholar
  10. Curtin AJ, Macdowell AA, Schaible EG, Roth VR (2012) Noninvasive histological comparison of bone growth patterns among fossil and extant neonatal elephantids using synchrotron radiation X-ray microtomography. J Vertebr Paleontol 32:939–955CrossRefGoogle Scholar
  11. Dermience M, Lognay G, Mathieu F, Goyens P (2015) Effects of thirty elements on bone metabolism. J Trace Elem Med Biol 32:86–106CrossRefPubMedGoogle Scholar
  12. Dickerson JW (1962) The effect of development on the composition of a long bone of the pig, rat and fowl. Biochem J 82:47–55CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dollwet HH, Sorenson JR (1988) Roles of copper in bone maintenance and healing. Biol Trace Elem Res 18:39–48CrossRefPubMedGoogle Scholar
  14. Fischer A, Wiechuła D, Przybyła-Misztela C (2013) Changes of concentrations of elements in deciduous teeth with age. Biol Trace Elem Res 154:427–432CrossRefPubMedPubMedCentralGoogle Scholar
  15. Frandson RD, Wilke WL, Fails AD (2009) Anatomy and physiology of farm animals. Wiley-Blackwell, IowaGoogle Scholar
  16. Hammer A (2015) The paradox of Wolff’s theories. Ir J Med Sci 184:13–22CrossRefPubMedGoogle Scholar
  17. Hillier ML, Bell LS (2007) Differentiating human bone from animal bone: a review of histological methods. J Forensic Sci 52:249–263CrossRefPubMedGoogle Scholar
  18. Hori H (2002) The forensic application of comparative mammalian bone histology. Texas Tech University, Texas, p 82Google Scholar
  19. Houssaye A, Fernandez V, Billet GJ (2015) Hyperspecialization in some South American endemic ungulates revealed by long bone microstructure. J Mammal Evol October 28:1–15Google Scholar
  20. Hutchinson JR, Delmer C, Miller CE, Hildebrandt T, Pitsillides AA, Boyde A (2011) From flat foot to fat foot: structure, ontogeny, function, and evolution of elephant “sixth toes”. Science 334:1699–1703CrossRefPubMedGoogle Scholar
  21. Kierdorf U, Stoffels D, Kierdorf H (2014) Element concentrations and element ratios in antler and pedicle bone of yearling red deer (Cervus elaphus) stags-a quantitative X-ray fluorescence study. Biol Trace Elem Res 162:124–133CrossRefPubMedGoogle Scholar
  22. Legros R, Balmin N, Bonel G (1987) Age-related changes in mineral of rat and bovine cortical bone. Calcif Tissue Int 41:137–144CrossRefPubMedGoogle Scholar
  23. Lewis KD, Shepherdson DJ, Owens TM, Keele M (2010) A survey of elephant husbandry and foot health in North American zoos. Zoo Biol 29:221–236PubMedGoogle Scholar
  24. Martiniaková M, Grosskopf B, Vondráková M, Omelka R, Fabis M (2006) Differences in femoral compact bone tissue microscopic structure between adult cows (Bos taurus) and pigs (Sus scrofa domestica). Anat Histol Embryol 35:167–170CrossRefPubMedGoogle Scholar
  25. Mikota SK (2006) Hemolymphatic system. In: Fowler ME, Mikota SK (eds) Biology, medicine, and surgery of elephants. Blackwell, Iowa, pp 325–345CrossRefGoogle Scholar
  26. Miller MA, Hogan JN, Meehan CL (2016) Housing and demographic risk factors impacting foot and musculoskeletal health in African elephants [Loxodonta africana] and Asian elephants [Elephas maximus] in North American zoos. PLoS One 11:e0155223CrossRefPubMedPubMedCentralGoogle Scholar
  27. Morales JP, Roa HI, Zavando D, Suazo GI (2012) Determination of the species from skeletal remains through histomorphometric evaluation and discriminant analysis. Int J Morphol 30:1035–1041CrossRefGoogle Scholar
  28. Mori R, Kodaka T, Sano T, Yamagishi N, Asari M, Naito Y (2003) Comparative histology of the laminar bone between young calves and foals. Cells Tissues Organs 175:43–50CrossRefPubMedGoogle Scholar
  29. Netter FH (2014) Atlas of human anatomy. Saunders Elsevier, PhiladelphiaGoogle Scholar
  30. Nganvongpanit K, Brown JL, Buddhachat K, Somgird C, Thitaram C (2015a) Elemental analysis of Asian elephant (Elephas maximus) teeth using X-ray fluorescence and a comparison to other species. Biol Trace Elem Res 170:94–105CrossRefPubMedGoogle Scholar
  31. Nganvongpanit K, Phatsara M, Settakorn J, Mahakkanukrauh P (2015b) Differences in compact bone tissue microscopic structure between adult humans (Homo sapiens) and Assam macaques (Macaca assamensis). Forensic Sci Int 254:e1–e5CrossRefGoogle Scholar
  32. Nganvongpanit K, Buddhachat K, Brown JL (2016a) Comparison of bone tissue elements between normal and osteoarthritic pelvic bones in dogs. Biol Trace Elem Res 171:344–353CrossRefPubMedGoogle Scholar
  33. Nganvongpanit K, Pradit W, Pitakarnnop T, Phatsara M, Chomdej S (2016b) Differences in osteon structure histomorphometry between Golden Retriever puppy and adult stages. Anat Sci Int. doi: 10.1007/s12565-016-0345-y Google Scholar
  34. Nielsen FH (1991) Nutritional requirements for boron, silicon, vanadium, nickel, and arsenic: current knowledge and speculation. FASEB J 5:2661–2667PubMedGoogle Scholar
  35. Nielsen FH, Zimmerman TJ, Shuler TR, Brossart B, Uthus EO (1989) Evidence for a cooperative metabolic relationship between Nickel and vitamin B12 in rats. J Trace Elem Exp Med 2:21–29Google Scholar
  36. Panagiotopoulou O, Pataky TC, Hill Z, Hutchinson JR (2012) Statistical parametric mapping of the regional distribution and ontogenetic scaling of foot pressures during walking in Asian elephants (Elephas maximus). J Exp Biol 215:1584–1593CrossRefPubMedGoogle Scholar
  37. Pankovich AM, Simmons DJ, Kulkarni VV (1974) Zonal osteons in cortical bone. Clin Orthop Relat Res 100:356–363CrossRefGoogle Scholar
  38. Parkpian P, Leong ST, Laortanakul P, Thunthaisong N (2003) Regional monitoring of lead and cadmium contamination in a tropical grazing land site, Thailand. Environ Monit Assess 85:157–173CrossRefPubMedGoogle Scholar
  39. Poonkothai M, Vijayavathai BS (2012) Nickel as an essential element and a toxicant. IJES 1:285–288Google Scholar
  40. Rey C, Combes C, Drouet C, Glimcher MJ (2009) Bone mineral: update on chemical composition and structure. Osteoporos Int 20:1013–1021CrossRefPubMedPubMedCentralGoogle Scholar
  41. Roth VL (1984) How elephants grow: heterochrony and the calibration of developmental stages in some living and fossil species. J Vert Paleont 4:126–145CrossRefGoogle Scholar
  42. Seeman E (2006) Bone structure and strength. In: Seibel M, Robins SP, Bilezikian JP (eds) Dynamics of bone and cartilage metabolism. Academic, London, pp 213–220CrossRefGoogle Scholar
  43. Shil SK, Quasem MA, Rahman ML, Kibria ASMG, Uddin M, Ahasan ASML (2013) Macroanatomy of the bones of pelvis and hind limb of an Asian elephant (Elephas maximus). Int J Morphol 31:1473–1478CrossRefGoogle Scholar
  44. Skedros JG, Sorenson SM, Jenson NH (2007) Are distributions of secondary osteon variants useful for interpreting load history in mammalian bones? Cells Tissues Organs 185:285–307CrossRefPubMedGoogle Scholar
  45. Smuts MM, Bezuidenhout AJ (1993) Osteology of the thoracic limb of the African elephant (Loxodonta africana). Onderstepoort J Vet Res 60:1–14PubMedGoogle Scholar
  46. Smuts MM, Bezuidenhout AJ (1994) Osteology of the pelvic limb of the African elephant (Loxodonta africana). Onderstepoort J Vet Res 61:51–66PubMedGoogle Scholar
  47. Todd NE (2010) Qualitative comparison of the cranio-dental osteology of the extant elephants, Elephas Maximus (Asian elephant) and Loxodonta africana (African elephant). Anat Rec (Hoboken) 293:62–73CrossRefGoogle Scholar
  48. Tzaphidou M, Zaichick V (2004) Sex and age related Ca/P ration in cortical bone of iliac crest of healthy humans. J Radioanal Nucl Chem 259:347–349CrossRefGoogle Scholar
  49. van der Merwe NJ, Bezuidenhout AJ, Seegers CD (1995) The skull and mandible of the African elephant (Loxodonta africana). Onderstepoort J Vet Res 62:245–260PubMedGoogle Scholar
  50. Weissengruber GE, Egger GF, Hutchinson JR et al (2006) The structure of the cushions in the feet of African elephants (Loxodonta africana). J Anat 209:781–792CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wopenka B, Pasteris JD (2005) A mineralogical perspective on the apatite in bone. Mat Sci Eng C25:131–143CrossRefGoogle Scholar
  52. Yamaguchi M, Sugii K, Okada S (1982) Tin decreases femoral calcium independently of calcium homeostasis in rats. Toxicol Lett 10:7–10CrossRefPubMedGoogle Scholar
  53. Zougrou IM, Katsikini M, Pinakidou F, Paloura EC, Papadopoulou L, Tsoukala E (2014) Study of fossil bones by synchrotron radiation micro-spectroscopic techniques and scanning electron microscopy. J Synchrotron Radiat 21:149–160CrossRefPubMedGoogle Scholar

Copyright information

© Japanese Association of Anatomists 2016

Authors and Affiliations

  • Korakot Nganvongpanit
    • 1
    • 2
    Email author
  • Puntita Siengdee
    • 1
  • Kittisak Buddhachat
    • 1
  • Janine L. Brown
    • 3
  • Sarisa Klinhom
    • 2
  • Tanita Pitakarnnop
    • 1
  • Taweepoke Angkawanish
    • 4
  • Chatchote Thitaram
    • 2
  1. 1.Animal Bone and Joint Research Laboratory, Department of Veterinary Biosciences and Public Health, Faculty of Veterinary MedicineChiang Mai UniversityChiang MaiThailand
  2. 2.Faculty of Veterinary Medicine, Center of Excellence in Elephant Research and EducationChiang Mai UniversityChiang MaiThailand
  3. 3.Smithsonian Conservation Biology Institute, Center for Species SurvivalFront RoyalUSA
  4. 4.National Elephant Institute, Forest Industry OrganizationLampangThailand

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