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


Journal

International journal of legal medicine
ISSN: 1437-1596
Titre abrégé: Int J Legal Med
Pays: Germany
ID NLM: 9101456

Informations de publication

Date de publication:
May 2019
Historique:
received: 06 06 2018
accepted: 19 12 2018
pubmed: 27 1 2019
medline: 30 5 2019
entrez: 26 1 2019
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 30680528
doi: 10.1007/s00414-018-01989-9
pii: 10.1007/s00414-018-01989-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

711-718

Références

Blau S, Briggs C (2011) The role of forensic anthropology in disaster victim identification (DVI). Forensic Sci Int 205(1–3):29–35. https://doi.org/10.1016/j.forsciint.2010.07.038
pubmed: 20797826
Brits D, Steyn M, L’Abbe EN (2014) A histomorphological analysis of human and non-human femora. Int J Legal Med 128(2):369–377. https://doi.org/10.1007/s00414-013-0854-3
pubmed: 23604414
Cuijpers AGFM (2006) Histological identification of bone fragments in archaeology: telling humans apart from horses and cattle. Int J Osteoarchaeol 16:465–480. https://doi.org/10.1002/oa.848
Cuijpers AGFM (2009) Distinguishing between the bone fragments of medium-sized mammals and children. A histological identification method for archaeology. Anthropol Anz 67(2):181–203
pubmed: 19739468
Hillier ML, Bell LS (2007) Differentiating human bone from animal bone: a review of histological methods. J Forensic Sci 52(2):249–263. https://doi.org/10.1111/j.1556-4029.2006.00368.x
pubmed: 17316219
Locke M (2004) Structure of long bones in mammals. J Morphol 262:546–565. https://doi.org/10.1002/jmor.10282
pubmed: 15376271
Mulhern DM, Ubelaker DH (2001) Differences in osteon banding between human and nonhuman bone. J Forensic Sci 46(2):220–222. https://doi.org/10.1520/JFS14952J
pubmed: 11305421
Sawada J, Nara T, Fukui J, Dodo Y, Hirata K (2014) Histomorphological species identification of tiny bone fragments from a paleolithic site in the northern Japanese archipelago. J Archaeol Sci 46:270–280. https://doi.org/10.1016/j.jas.2014.03.025
Cattaneo C, Porta D, Gibelli D, Gamba C (2009) Histological determination of the human origin of bone fragments. J Forensic Sci 54:531–533. https://doi.org/10.1111/j.1556-4029.2009.01000.x
pubmed: 19298464
Crescimanno A, Stout SD (2012) Differentiating fragmented human and nonhuman long bone using osteon circularity. J Forensic Sci 57(2):287–294. https://doi.org/10.1111/j.1556-4029.2011.01973.x
pubmed: 22103892
Dominguez VM, Crowder CM (2012) The utility of osteon shape and circularity for differentiating human and non-human Haversian bone. Am J Phys Anthropol 149(1):84–91. https://doi.org/10.1002/ajpa.22097
pubmed: 22700390
Martiniaková M, Grosskopf B, Omelka R, Vondráková M, Bauerová M (2006a) Differences among species in compact bone tissue microstructure of mammalian skeleton: use of a discriminant function analysis for species identification. J Forensic Sci 51(6):1235–1239. https://doi.org/10.1111/j.1556-4029.2006.00260.x
pubmed: 17199608
Martiniaková M, Grosskopf B, Vondráková M, Omelka R, Fabĭs M (2006b) Differences in femoral compact bone tissue microscopic structure between adult cows (Bos taurus) and pigs (Sus scrofa domestics). Anat Histol Embryol 35:167–170. https://doi.org/10.1111/j.1439-0264.2005.00652.x
pubmed: 16677211
Martiniaková M, Grosskopf B, Omelka R, Vondráková M, Bauerová M (2007a) Histological analysis of ovine compact bone tissue. J Vet Med Sci 69:409–411. https://doi.org/10.1292/jvms.69.409
pubmed: 17485930
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
Urbanová P, Novotný V (2005) Distinguishing between human and non-human bones: histometric method for forensic anthropology. Anthropologie 43:77–85
Mulhern DM, Ubelaker DH (2011) Differentiating human from nonhuman bone microstructure. In: Crowder C, Stout SD (eds) Bone histology: an anthropological perspective. CRC Press, Boca Raton, pp 109–134. https://doi.org/10.1201/b11393-6
doi: 10.1201/b11393-6
Cummaudo M, Cappella A, Biraghi M, Raffone C, Màrquez-Grant N, Cattaneo C (2018) Histomorphological analysis of the variability of the human skeleton: forensic implications. Int J Legal Med 132:1493–1503. https://doi.org/10.1007/s00414-018-1781-0
pubmed: 29352750
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
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
Martin RB, Gibson VA, Stover SM, Gibeling JC, Griffin LV (1996) Osteonal structure in the equine third metacarpus. Bone 19(2):165–171
pubmed: 8853861
Zerwekh JE (1992) Bone metabolism. Semin Nephrol 12:79–90
pubmed: 1561499
Freemont AJ (1993) Basic bone cell biology: a review. Int J Exp Pathol 74:411–416
pubmed: 8398815 pmcid: 2001858
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
Qiu S, Fyhrie DP, Palnitkar S, Rao DS (2003) Histomorphometric assessment of Haversian canal and osteocyte lacunae in different-sized osteons in human rib. Anat Rec 272a(2):520–525. https://doi.org/10.1002/ar.a.10058
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
Parfitt AM (2005) Targeted and nontargeted remodeling: relationship to basic multicellular unit organization and progression. Bone 30(1):5–7
Martin RB (2000) Does osteocyte formation cause the nonlinear refilling of osteons? Bone 26(1):71–78
pubmed: 10617159
Qiu S, Rao DS, Palnitkar S, Parfitt AM (2006) Differences in osteocyte and lacunar density between Black and White American women. Bone 38:130–135
pubmed: 16112633
Sissons HA, O’Connor P (1977) Quantitative histology of osteocyte lacunae in normal human cortical bone. Calcif Tissue Res 22(Suppl):530–533
pubmed: 912582
Ascenzi MG, Gill J, Lomovtsev A (2008) Orientation of collagen at the osteocyte lacunae in human secondary osteons. J Biomech 41(16):3426–3435
pubmed: 19013574
Carter Y, Thomas CDL, Clement JG, Peele AG, Hannah K, Cooper DML (2013) Variation in osteocyte lacunar morphology and density in the human femur - a synchrotron radiation micro-CT study. Bone 52(1):126–132. https://doi.org/10.1016/j.bone.2012.09.010
pubmed: 22995461
Dong P, Haupert S, Hesse B, Langer M, Gouttenoire PJ, Bousson V, Peyrin F (2014) 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone 60:172–185. https://doi.org/10.1016/j.bone.2013.12.008
pubmed: 24334189
Hannah KM, Thomas CDL, Clement JG, De Carlo F, Peele AG (2010) Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 47(5):866–871. https://doi.org/10.1016/j.bone.2010.07.025
pubmed: 20691298
Teti A, Zallone A (2009) Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44:11–16
pubmed: 18977320
Stern AR, Nicolella DP (2013) Measurement and estimation of osteocyte mechanical strain. Bone 54(2):191–195
pubmed: 23369990
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 91:11–19
pubmed: 27397700
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 180:215–236
pubmed: 16330878
Hobdell MH, Howe CE (1971) Variation in bone matrix volume associated with osteocyte lacunae in mammalian and reptilian bone. Isr J Med Sci 7:492–493
pubmed: 5567527
Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113
pubmed: 8833204
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 77:291–296
pubmed: 16307389
Qiu S, Rao DS, Palnitkar S, Parfitt AM (2003) Reduced iliac cancellous osteocyte density in patients with osteoporotic vertebral fracture. J Bone Miner Res 18:1657–1663
pubmed: 12968675
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 45:321–329
pubmed: 19398046
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 (1979) Osteocyte orientation in human lamellar bone and its relevance to the morphometry of periosteocytic lacunae. Metab Bone Dis Relat 333:325–333
Pokines JT (2015) Identification of nonhuman remains received in a medical examiner setting. J Forensic Identif 65(3):223–246
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
Frasca P, Harper RA, Katz JL (1977) Collagen fibre orientations in human secondary osteons. Acta Anat (Basel) 98:1–13
Ardizzoni A (2001) Osteocyte lacunar size-lamellar thickness relationships in human secondary osteons. Bone 28(2):215–219. https://doi.org/10.1016/S8756-3282(00)00417-8
pubmed: 11182381
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):145–155
pubmed: 9882957
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):121–131
pubmed: 10575824
van Oers RFM, Wang H, Bacabac RG (2015) Osteocyte shape and mechanical loading. Curr Osteoporos Rep 13(2):61–66. https://doi.org/10.1007/s11914-015-0256-1
pubmed: 25663071 pmcid: 4352610
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 43:452–458
pubmed: 18625577
Britz HM, Thomas CDL, Clement JG, Cooper DML (2009) The relation of femoral osteon geometry to age, sex, height and weight. Bone 45:77–83
pubmed: 19303955
Currey JD (1964) Some effects of ageing in human Haversian systems. J Anat 98(1):69–75
pubmed: 14109815 pmcid: 1261313
Evans FG (1976) Mechanical properties and histology of cortical bone from younger and older men. Anat Rec 185(1):12
Mulhern DM, Van Gerven DP (1997) Patterns of femoral bone remodeling dynamics in a medieval Nubian population. Am J Phys Anthropol 104:133–146
pubmed: 9331458
Thompson DD (1980) Age changes in bone mineralization, cortical thickness and Haversian canal area. Calcif Tissue Int 31:5–11
pubmed: 6770973

Auteurs

Marco Cummaudo (M)

LABANOF (Laboratorio di Antropologia e Odontologia Forense) Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, via Mangiagalli 37, 20133, Milan, Italy. m.cummaudo@cranfield.ac.uk.
Cranfield Forensic Institute, Defence Academy of the United Kingdom, Cranfield University, Shrivenham, SN6 8LA, UK. m.cummaudo@cranfield.ac.uk.

Annalisa Cappella (A)

LABANOF (Laboratorio di Antropologia e Odontologia Forense) Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, via Mangiagalli 37, 20133, Milan, Italy.

Francesca Giacomini (F)

LABANOF (Laboratorio di Antropologia e Odontologia Forense) Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, via Mangiagalli 37, 20133, Milan, Italy.

Caterina Raffone (C)

LABANOF (Laboratorio di Antropologia e Odontologia Forense) Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, via Mangiagalli 37, 20133, Milan, Italy.

Nicholas Màrquez-Grant (N)

Cranfield Forensic Institute, Defence Academy of the United Kingdom, Cranfield University, Shrivenham, SN6 8LA, UK.

Cristina Cattaneo (C)

LABANOF (Laboratorio di Antropologia e Odontologia Forense) Dipartimento di Scienze Biomediche per la Salute, Università degli Studi di Milano, via Mangiagalli 37, 20133, Milan, Italy.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH