Skip to main content
Top
Published in: International Journal of Legal Medicine 3/2019

01-05-2019 | Original Article

Histomorphometric analysis of osteocyte lacunae in human and pig: exploring its potential for species discrimination

Authors: Marco Cummaudo, Annalisa Cappella, Francesca Giacomini, Caterina Raffone, Nicholas Màrquez-Grant, Cristina Cattaneo

Published in: International Journal of Legal Medicine | Issue 3/2019

Login to get access

Abstract

In recent years, several studies have focused on species discrimination of bone fragments by histological analysis. According to literature, the most consistent distinguishing features are Haversian canal and Haversian system areas. Nonetheless, there is a consistent overlap between human and non-human secondary osteon dimensions. One of the features that have never been analyzed for the purpose of species discrimination is the osteocyte lacuna, a small oblong cavity in which the osteocyte is locked in. The aim of this study is to verify whether there are significant quantitative differences between human and pig lacunae within secondary osteons with similar areas. Study sample comprises the midshaft of long bones (humerus, radius, ulna, femur, tibia, and fibula) of a medieval human adult and a juvenile pig. Sixty-eight secondary osteons with similar areas have been selected for each species and a total of 1224 osteocyte lacunae have been measured. For each osteon, the total number of lacunae was counted, and the following measurements were taken: minimum and maximum diameter, area, perimeter, and circularity of nine lacunae divided between inner, intermediate, and outer lacunae. Statistical analysis showed minimal differences between human and pig in the number of lacunae per osteons and in the minimum diameter (P > 0.05). On the contrary, a significant difference (P < 0.001) has been observed in the maximum diameter, perimeter, area, and circularity. Although there is the need for further research on different species and larger sample, these results highlighted the potential for the use of osteocyte lacunae as an additional parameter for species discrimination. Concerning the difference between the dimensions of osteocyte lacunae based on their position within the osteon (inner, intermediate, and outer lacunae), results showed that their size decreases from the cement line towards the Haversian canal both in human and pig.
Literature
4.
go back to reference Cuijpers AGFM (2009) Distinguishing between the bone fragments of medium-sized mammals and children. A histological identification method for archaeology. Anthropol Anz 67(2):181–203PubMed Cuijpers AGFM (2009) Distinguishing between the bone fragments of medium-sized mammals and children. A histological identification method for archaeology. Anthropol Anz 67(2):181–203PubMed
15.
go back to reference Martiniaková M, Grosskopf B, Omelka R, Dammers K, Vondráková M, Bauerová M (2007b) Histological study of compact bone tissue in some mammals: a method for species determination. Int J Osteoarchaeol 17:82–90. https://doi.org/10.1002/oa.856 Martiniaková M, Grosskopf B, Omelka R, Dammers K, Vondráková M, Bauerová M (2007b) Histological study of compact bone tissue in some mammals: a method for species determination. Int J Osteoarchaeol 17:82–90. https://​doi.​org/​10.​1002/​oa.​856
16.
go back to reference Urbanová P, Novotný V (2005) Distinguishing between human and non-human bones: histometric method for forensic anthropology. Anthropologie 43:77–85 Urbanová P, Novotný V (2005) Distinguishing between human and non-human bones: histometric method for forensic anthropology. Anthropologie 43:77–85
19.
go back to reference Albu I, Georgia R, Georoceneau M (1990) The canal system in the diaphyseal compacta of the femur in some mammals. Anat Anz 170(3–4):191–187 Albu I, Georgia R, Georoceneau M (1990) The canal system in the diaphyseal compacta of the femur in some mammals. Anat Anz 170(3–4):191–187
20.
go back to reference Dittman K (2003) Histomorphometrische untersuchung der knochenmikrostructur von primate and haustieren mit dem ziel der speziesdentifikaton unter berücksichtingung von domestikationseffekten. Anthropol Anz 61(2):175–188 Dittman K (2003) Histomorphometrische untersuchung der knochenmikrostructur von primate and haustieren mit dem ziel der speziesdentifikaton unter berücksichtingung von domestikationseffekten. Anthropol Anz 61(2):175–188
21.
go back to reference Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV (1996) Osteonal structure in the equine third metacarpus. Bone 19(2):165–171PubMed Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV (1996) Osteonal structure in the equine third metacarpus. Bone 19(2):165–171PubMed
22.
24.
go back to reference Stout SD, Crowder C (2011) Bone remodeling, histomorphology, and histomorphometry. In: Crowder C, Stout SD (eds) Bone histology: an anthropological perspective. CRC Press, Boca Raton, pp 1–21 Stout SD, Crowder C (2011) Bone remodeling, histomorphology, and histomorphometry. In: Crowder C, Stout SD (eds) Bone histology: an anthropological perspective. CRC Press, Boca Raton, pp 1–21
26.
go back to reference Nijweide PJ, Burger EH, Klein-Nulend J (2002) The osteocyte. In: Bilezikian JP, Raisz LG, Rodan GA (eds) Principles of bone biology, 2nd edn. Academic, San Diego, pp 93–107 Nijweide PJ, Burger EH, Klein-Nulend J (2002) The osteocyte. In: Bilezikian JP, Raisz LG, Rodan GA (eds) Principles of bone biology, 2nd edn. Academic, San Diego, pp 93–107
27.
go back to reference Parfitt AM (2005) Targeted and nontargeted remodeling: relationship to basic multicellular unit organization and progression. Bone 30(1):5–7 Parfitt AM (2005) Targeted and nontargeted remodeling: relationship to basic multicellular unit organization and progression. Bone 30(1):5–7
28.
go back to reference Martin RB (2000) Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26(1):71–78PubMed Martin RB (2000) Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26(1):71–78PubMed
29.
go back to reference Qiu S, Rao DS, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between Black and White American women. Bone 38:130–135PubMed Qiu S, Rao DS, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between Black and White American women. Bone 38:130–135PubMed
30.
go back to reference Sissons HA, O’Connor P (1977) Quantitative histology of osteocyte lacunae in normal human cortical bone. Calcif Tissue Res 22(Suppl):530–533PubMed Sissons HA, O’Connor P (1977) Quantitative histology of osteocyte lacunae in normal human cortical bone. Calcif Tissue Res 22(Suppl):530–533PubMed
31.
go back to reference Ascenzi MG, Gill J, Lomovtsev A (2008) Orientation of collagen at the osteocyte lacunae in human secondary osteons. J Biomech 41(16):3426–3435PubMed Ascenzi MG, Gill J, Lomovtsev A (2008) Orientation of collagen at the osteocyte lacunae in human secondary osteons. J Biomech 41(16):3426–3435PubMed
35.
go back to reference Teti A, Zallone A (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44:11–16PubMed Teti A, Zallone A (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44:11–16PubMed
36.
go back to reference Stern AR, Nicolella DP (2013) Measurement and estimation of osteocyte mechanical strain. Bone 54(2):191–195PubMed Stern AR, Nicolella DP (2013) Measurement and estimation of osteocyte mechanical strain. Bone 54(2):191–195PubMed
37.
go back to reference Bach-Gansmo FL, Brüel A, Jensen MV, Ebbesen EN, Birkedal H, Thomsen JS (2016) Osteocyte lacunar properties and cortical microstructure in human iliac crest as a function of age and sex. Bone 91:11–19PubMed Bach-Gansmo FL, Brüel A, Jensen MV, Ebbesen EN, Birkedal H, Thomsen JS (2016) Osteocyte lacunar properties and cortical microstructure in human iliac crest as a function of age and sex. Bone 91:11–19PubMed
38.
go back to reference Skedros JG, Grunander TR, Hamrick MW (2005) Spatial distribution of osteocyte lacunae in equine radii and third metacarpals: considerations for cellular communication, microdamage detection and metabolism. Cells Tissues Organs 180:215–236PubMed Skedros JG, Grunander TR, Hamrick MW (2005) Spatial distribution of osteocyte lacunae in equine radii and third metacarpals: considerations for cellular communication, microdamage detection and metabolism. Cells Tissues Organs 180:215–236PubMed
39.
go back to reference Hobdell MH, Howe CE (1971) Variation in bone matrix volume associated with osteocyte lacunae in mammalian and reptilian bone. Isr J Med Sci 7:492–493PubMed Hobdell MH, Howe CE (1971) Variation in bone matrix volume associated with osteocyte lacunae in mammalian and reptilian bone. Isr J Med Sci 7:492–493PubMed
40.
go back to reference Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113PubMed Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113PubMed
41.
go back to reference Mullender MG, Tan SD, Vico L, Alexandre C, Klein-Nulend J (2005) Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77:291–296PubMed Mullender MG, Tan SD, Vico L, Alexandre C, Klein-Nulend J (2005) Differences in osteocyte density and bone histomorphometry between men and women and between healthy and osteoporotic subjects. Calcif Tissue Int 77:291–296PubMed
42.
go back to reference Qiu S, Rao DS, Palnitkar S, Parfitt AM (2003) Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 18:1657–1663PubMed Qiu S, Rao DS, Palnitkar S, Parfitt AM (2003) Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 18:1657–1663PubMed
43.
go back to reference van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone 45:321–329PubMed van Hove RP, Nolte PA, Vatsa A, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2009) Osteocyte morphology in human tibiae of different bone pathologies with different bone mineral density—is there a role for mechanosensing? Bone 45:321–329PubMed
44.
go back to reference Marotti G, Favia A, Zallone A (1972) Quantitative analysis on the rate of secondary bone mineralization. Calcif Tissue Res 10(1):67–81 Marotti G, Favia A, Zallone A (1972) Quantitative analysis on the rate of secondary bone mineralization. Calcif Tissue Res 10(1):67–81
45.
go back to reference Marotti G (1979) Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae. Metab Bone Dis Relat 333:325–333 Marotti G (1979) Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae. Metab Bone Dis Relat 333:325–333
46.
go back to reference Pokines JT (2015) Identification of nonhuman remains received in a medical examiner setting. J Forensic Identif 65(3):223–246 Pokines JT (2015) Identification of nonhuman remains received in a medical examiner setting. J Forensic Identif 65(3):223–246
47.
go back to reference Maat GJR, Van Den Bos RPM, Aarents MJ (2001) Manual preparation of ground sections for the microscopy of natural bone tissue: update and modification of Frost’s “rapid manual method”. Int J Osteoarchaeol 11(5):366–374. https://doi.org/10.1002/oa.578 Maat GJR, Van Den Bos RPM, Aarents MJ (2001) Manual preparation of ground sections for the microscopy of natural bone tissue: update and modification of Frost’s “rapid manual method”. Int J Osteoarchaeol 11(5):366–374. https://​doi.​org/​10.​1002/​oa.​578
48.
go back to reference Frasca P, Harper RA, Katz JL (1977) Collagen fibre orientations in human secondary osteons. Acta Anat (Basel) 98:1–13 Frasca P, Harper RA, Katz JL (1977) Collagen fibre orientations in human secondary osteons. Acta Anat (Basel) 98:1–13
50.
go back to reference Remaggi F, Canè V, Palumbo C, Ferretti M (1998) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 103(4):145–155PubMed Remaggi F, Canè V, Palumbo C, Ferretti M (1998) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. I. Woven-fibered and parallel-fibered bones. Ital J Anat Embryol 103(4):145–155PubMed
51.
go back to reference Ferretti M, Muglia MA, Remaggi F, Canè V, Palumbo C (1999) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. II. Parallel-fibered and lamellar bones. Ital J Anat Embryol 104(3):121–131PubMed Ferretti M, Muglia MA, Remaggi F, Canè V, Palumbo C (1999) Histomorphometric study on the osteocyte lacuno-canalicular network in animals of different species. II. Parallel-fibered and lamellar bones. Ital J Anat Embryol 104(3):121–131PubMed
53.
go back to reference Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria—is there a role for mechanosensing? Bone 43:452–458PubMed Vatsa A, Breuls RG, Semeins CM, Salmon PL, Smit TH, Klein-Nulend J (2008) Osteocyte morphology in fibula and calvaria—is there a role for mechanosensing? Bone 43:452–458PubMed
54.
go back to reference Britz HM, Thomas CDL, Clement JG, Cooper DML (2009) The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:77–83PubMed Britz HM, Thomas CDL, Clement JG, Cooper DML (2009) The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:77–83PubMed
56.
go back to reference Evans FG (1976) Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 185(1):12 Evans FG (1976) Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 185(1):12
57.
go back to reference Mulhern DM, Van Gerven DP (1997) Patterns of femoral bone remodeling dynamics in a medieval Nubian population. Am J Phys Anthropol 104:133–146PubMed Mulhern DM, Van Gerven DP (1997) Patterns of femoral bone remodeling dynamics in a medieval Nubian population. Am J Phys Anthropol 104:133–146PubMed
58.
go back to reference Thompson DD (1980) Age changes in bone mineralization, cortical thickness and Haversian canal area. Calcif Tissue Int 31:5–11PubMed Thompson DD (1980) Age changes in bone mineralization, cortical thickness and Haversian canal area. Calcif Tissue Int 31:5–11PubMed
Metadata
Title
Histomorphometric analysis of osteocyte lacunae in human and pig: exploring its potential for species discrimination
Authors
Marco Cummaudo
Annalisa Cappella
Francesca Giacomini
Caterina Raffone
Nicholas Màrquez-Grant
Cristina Cattaneo
Publication date
01-05-2019
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Legal Medicine / Issue 3/2019
Print ISSN: 0937-9827
Electronic ISSN: 1437-1596
DOI
https://doi.org/10.1007/s00414-018-01989-9

Other articles of this Issue 3/2019

International Journal of Legal Medicine 3/2019 Go to the issue