Article
Bone histomorphometry: Standardization of nomenclature, symbols, and units: Report of the asbmr histomorphometry nomenclature committee
A. Michael Parfitt M.D.,
Marc K. Drezner,
Francis H. Glorieux,
John A. Kanis,
Hartmut Malluche,
Pierre J. Meunier,
Susan M. Ott,
Robert R. Recker,
Corresponding Author
A. Michael Parfitt M.D.
Chairman
Bone and Mineral Research Laboratory, Department of Medicine, Henry Ford Hospital, Detroit, MI
Bone and Mineral Research Laboratory Henry Ford Hospital 2799 West Grand Boulevard Detroit, MI 48202Search for more papers by this authorMarc K. Drezner
Bone and Mineral Metabolism Section, Division of Metabolism, Endocrinology and Genetics, Department of Medicine, Duke University Medical Center, Durham, NC
Search for more papers by this authorFrancis H. Glorieux
Genetics Unit, Shriners Hospital for Crippled Children, Montreal, Quebec, Canada
Search for more papers by this authorJohn A. Kanis
Department of Human Metabolism and Clinical Biochemistry, University of Sheffield, Sheffield, UK
Search for more papers by this authorHartmut Malluche
Department of Medicine, Division of Nephrology, Bone and Mineral Metabolism, University of Kentucky College of Medicine, Lexington, KT
Search for more papers by this authorPierre J. Meunier
INSERM Unit 234, Faculte Alexis Carrel, Lyon, France
Search for more papers by this authorSusan M. Ott
Department of Medicine, Harborview Medical Center, University of Washington, Seattle, WA
Search for more papers by this authorRobert R. Recker
Metabolic Research Unit, Department of Internal Medicine, Creighton University School of Medicine, Omaha, NB
Search for more papers by this authorA. Michael Parfitt M.D.,
Marc K. Drezner,
Francis H. Glorieux,
John A. Kanis,
Hartmut Malluche,
Pierre J. Meunier,
Susan M. Ott,
Robert R. Recker,
Corresponding Author
A. Michael Parfitt M.D.
Chairman
Bone and Mineral Research Laboratory, Department of Medicine, Henry Ford Hospital, Detroit, MI
Bone and Mineral Research Laboratory Henry Ford Hospital 2799 West Grand Boulevard Detroit, MI 48202Search for more papers by this authorMarc K. Drezner
Bone and Mineral Metabolism Section, Division of Metabolism, Endocrinology and Genetics, Department of Medicine, Duke University Medical Center, Durham, NC
Search for more papers by this authorFrancis H. Glorieux
Genetics Unit, Shriners Hospital for Crippled Children, Montreal, Quebec, Canada
Search for more papers by this authorJohn A. Kanis
Department of Human Metabolism and Clinical Biochemistry, University of Sheffield, Sheffield, UK
Search for more papers by this authorHartmut Malluche
Department of Medicine, Division of Nephrology, Bone and Mineral Metabolism, University of Kentucky College of Medicine, Lexington, KT
Search for more papers by this authorPierre J. Meunier
INSERM Unit 234, Faculte Alexis Carrel, Lyon, France
Search for more papers by this authorSusan M. Ott
Department of Medicine, Harborview Medical Center, University of Washington, Seattle, WA
Search for more papers by this authorRobert R. Recker
Metabolic Research Unit, Department of Internal Medicine, Creighton University School of Medicine, Omaha, NB
Search for more papers by this author
References
- 1
Parfitt AM
1976
Terminology and symbols in bone morphometry.
In: Jaworski ZFG (ed) Proceedings of the First International Workshop on Bone Morphometry. Ottawa University Press, Ottawa,
pp 331–335.
- 2
Dorland's Illustrated Medical Dictionary,
26th ed
1981
WB Saunders, Philadelphia.
- 3
Fawcett DW
1986
A Textbook of Histology,
II ed.
WB Saunders, Philadelphia.
- 4
Malluche HH,
Faugere M-C
1986
Atlas of Mineralized Bone Histology.
S. Karger AG, New York.
- 5
Revell PA
1986
Pathology of Bone.
Springer-Verlag, Berlin.
- 6
Cowin SC
1986
Wolff's Law of trabecular architecture at remodeling equilibrium.
J Biomechanical Engineering
108:
83–88.
- 7
Arnold JS,
Wei LT
1972
Quantitative morphology of vertebral trabecular bone.
In: B Stover,
WSS Jee (eds)
Radiobiology of Plutonium.
The J.W. Press, Salt Lake City,
pp 333–354.
- 8
Whitehouse WJ
1977
Cancellous bone in the anterior part of the iliac crest.
Calc Tiss Res
23:
67–76.
- 9
Elias H,
Sherrick JC
1969
Morphology of the Liver.
Academic Press, New York.
- 10
Singh I
1978
The architecture of cancellous bone.
J Anat
127:
305–310.
- 11
Robinson RA
1960
Chemical analysis and electron microsopcy of bone.
In: K Rodahl,
JT Nicholson,
EM Brown (eds)
Bone as a Tissue.
McGraw-Hill, New York,
pp 186–250.
- 12
Courpron P,
Meunier P,
Bressot C,
Giroux JM
1976
Amount of bone in iliac crest biopsy.
Significance of the trabecular bone volume. In: Meunier PJ (ed) Bone Histomorphometry. Second International Workshop, Armour Montagu, Paris,
pp 39–53.
- 13
Malluche HH,
Sherman DS,
Meyer W,
Massry SG
1982
A new semiautomatic method for quantitative static and dynamic bone histology.
Calcif Tissue Int
34:
439–448.
- 14
Frost HM
1964
Bone Remodelling Dynamics.
C.C. Thomas, Springfield.
- 15
Carter DR,
Spengler DM
1978
Mechanical properties and composition of cortical bone.
Clin Orthop
135:
192–217.
- 16
Vaughan JM
1976
The Physiology of Bone,
2 ed.
The Clarendon Press, Oxford.
- 17
Dunstan CR,
Evans RA
1980
Quantitative bone histology: A new method.
Pathology
12:
255–264.
- 18
Chappard D,
Alexandre C,
Riffat G
1983
Histochemical identification of osteoclasts. Review of current methods and reappraisal of a simple procedure for routine diagnosis on undecalcified iliac bone biopsies. Bas. Appl.
Histochem
27:
75–83.
- 19
Parfitt AM
1983
The stereologic basis of bone histomorphometry. Theory of quantitative microscopy and reconstruction of the third dimension.
In: R Recker (ed)
Bone Histomorphometry. Techniques and Interpretations.
CRC Press, Boca Raton,
pp 53–87.
- 20
Aherne WA,
Dunnill MS
1982
Morphometry.
Edward Arnold, London.
- 21
Elias H,
Hyde DM
1983
A Guide to Practical Stereology.
Karger, Basel.
- 22
Vesterby A,
Kragstrup J,
Gundersen HJG,
Melsen F
1987
Unbiased stereological estimation of surface density in bone using ‘vertical sections’.
Bone
8:
13–17.
- 23
Whitehouse WJ
1974
The quantitative morphology of anisotropic trabecular bone.
J Microsc
101:
153–168.
- 24
Schwartz MP,
Recker RR
1981
Comparison of surface density and volume of human iliac trabecular bone measured directly and by applied stereology.
Calcif Tissue Int
33:
561–565.
- 25
Baddeley AJ,
Gundersen HJG,
Cruz-Orive LM
1986
Estimation of surface area from vertical sections.
J Microsc
142:
259–276.
- 26
Gundersen HJG
1986
Stereology of arbitrary particles.
J Microsc
143:
3–45.
- 27
DeHoff RT
1983
Quantitative serial sectioning analysis: preview.
J Microsc
131:
259–263.
- 28
Schenk RK
1976
Comments on terminology and symbols.
In: Jaworski ZFG (ed) Proceedings of the First Workshop on Bone Morphometry. University of Ottawa Press, Ottawa,
p 336.
- 29
Frost HM
1983
Bone histomorphometry: Analysis of trabecular bone dynamics.
In: R Recker (ed)
Bone Histomorphometry. Techniques and Interpretations.
CRC Press, Boca Raton,
pp 109–131.
- 30
Parfitt AM,
Rao DS,
Stanciu J,
Villanueva AR,
Kleerekoper M,
Frame B
1985
Irreversible bone loss in osteomalacia: Comparison of radial photon absorptiometry with iliac bone histomorphometry during treatment.
J Clin Invest
76:
2403–2412.
- 31
Parfitt AM,
Simon LS,
Villanueva AR,
Krane SM
1987
Pro-collagen type 1 carboxy-terminal extension peptide in serum as a marker of collagen biosynthesis in bone.
Correlation with iliac bone formation rales and comparison with total alkaline phosphatase. J Bone Min Res (in press).
- 32
Boyce BF,
Courpon P,
Meunier PJ
1978
Amount of bone in osteoporosis and physiological senile osteopenia. Comparison of two histomorphometric parameters.
Metab Bone Dis & Rel Res
1:
35–38.
- 33
Horsman A
1976
Bone mass.
In: BEC Nordin (ed)
Calcium, Phosphate and Magnesium Metabolism.
Churchill-Livingstone, Edinburgh.
- 34
Eiuclid, Book 1, Proposition 35.
- 35
Keshawarz NM,
Recker RR
1984
Expansion of the medullary cavity at the expense of cortex in postmenopausal osteoporosis.
Metab Bone Dis & Rel Res
5:
223–228.
- 36
Compston JE,
Vedi S,
Stellon AJ
1986
Inter-observer and intraobserver variation in bone histomorphometry.
Calcif Tissue Int
38:
67–70.
- 37
Duncan H
1973
Cortical porosis; a morphological evaluation.
In: Jaworski ZFG (ed) First Workshop on Bone Histomorphometry. University of Ottawa Press,
p 78.
- 38
Arnold JS,
Bartley MH,
Tont SA,
Jenkins DP
(1966)
Skeletal changes in aging and disease.
Clin Orthop Relat Res
49:
17–38.
- 39
Olah AJ
1980
Effects of microscopic resolution on histomorphometrical estimates of structural and remodeling parameters in cancellous bone.
Path Res Pract
166:
313–322.
- 40
Rasmussen H,
Bordier PJ
1974
The Physiological and Cellular Basis of Metabolic Bone Disease.
Williams and Wilkins, Baltimore.
- 41
Martin RB
1984
Porosity and specific surface of bone.
CRC Crit Rev Biomed Engineering
10:
179–222.
- 42
Eriksen EF
1986
Normal and pathological remodeling of human trabecular bone: Three dimensional reconstruction of the remodeling sequence in normals and in metabolic bone disease.
Endocrine Reviews
7:
379–408.
- 43
Parfitt AM
1984
The cellular basis of bone remodeling. The quantum concept re-examined in light of recent advances in cell biology of bone.
Calc Tissue Int
36:
S37–S45.
- 44
Kragstrup J,
Gundersen HJG,
Melsen F,
Mosekilde L
1982
Estimation of the three-dimensional wall thickness of completed remodeling sites in iliac trabecular bone.
Metab Bone Dis Rel Res
4:
113–119.
- 45
Parfitt AM,
Villanueva AR,
Mathews CHE,
Aswani JA
1981
Kinetics of matrix and mineral apposition in osteoporosis and renal osteodystrophy: Relationship to rate of turnover and to cell morphology.
In: Jee WSS, Parfitt AM (eds) Bone Histomorphometry. Third International Workshop, Armour-Montagu, Paris,
pp 213–219.
- 46
Parfitt AM
1987
Osteomalacia and related disorders.
In: LV Avioli,
SM Krane (eds)
Metabolic Bone Disease.
2 ed.
Grune and Stratton. New York
(in press).
- 47
Baylink D,
Stauffer M,
Wergedal J,
Rich C
1970
Formation, mineralization and resorption of bone in vitamin D deficient rats.
J Clin Invest
49:
1122.
- 48
Teitelbaum S,
Hruska KA,
Shieber W,
Debnam JW,
Nichols SH
1977
Tetracycline fluorescence in uremic and primary hyper-parathyroid bone.
Kidney Int
12:
366.
- 49
Courpron P
1981
Bone tissue mechanisms underlying osteoporoses.
Orthop Clin North Am
12:
513–545.
- 50
Broulik P,
Kragstrup J,
Mosekilde L,
Melsen F
1982
Osteon cross-sectional size in the iliac crest.
Acta Path Microbiol Immunol Scand Sect A
90:
339–344.
- 51
Merz WA,
Schenk RK
1970
Quantitative structural analysis of human cancellous bone.
Acta Anat (Basel)
75:
54–66.
- 52
Malluche HH,
Meyer W,
Sherman D,
Massry SG
1982
Quantitative bone histology in 84 normal American subjects.
Calcif Tissue Int
34:
449–455.
- 53
Garrahan NJ,
Mellish RW,
Compston JE
1986
A new method for the two dimensional analysis of bone structure in human iliac crest biopsies.
J Microsc
142:
341–344.
- 54
Compston JE,
Mellish RWE,
Garrahan NJ
1987
Age-related changes in iliac crest trabecular macroanatomic bone structure in man.
Bone (in press).
- 55
Parfitt AM,
Mathews CHE,
Villanueva AR,
Kleerekoper M,
Frame B,
Rao DS
1983
Relationship between surface, volume and thickness of iliac trabecular bone in aging and in osteoporosis: Implications for the microanatomic and cellular mechanisms of bone loss.
J Clin Invest
72:
1396–1409.
- 56
Weinstein RS,
Hutson MS
1987
Decreased trabecular width and increased trabecular spacing contribute to bone loss with aging.
Bone
8:
137–142.
- 57
Aaron JE,
Makins, NB,
Francis RM,
Peacock M
1984
Staining of the calcification front in human bone using contrasting fluorochromes in vitro.
J Histochemistry and Cytochemistry
32:
1251–1261.
- 58
Tam CS,
Anderson W
1980
Tetracycline labelling of bone in vivo.
Calcif Tissue Int
30:
121–125.
- 59
Parfitt AM
1983
The physiologic and clinical significance of bone histomorphometric data.
In: R Recker (ed)
Bone Histomorphometry. Techniques and Interpretations.
CRC Press, Boca Raton,
pp 143–223.
- 60
Melsen F,
Mosekilde L
1978
Dynamic studies of trabecular bone formation and osteoid maturation in normal and certain pathological conditions.
Metab Bone Dis & Rel Res
1:
45–48.
- 61
Frost HM
1969
Tetracycline-based histological analysis of bone remodeling. Editorial.
Calc Tiss Res
3:
211–237.
- 62
Jaworski ZFG
1983
Bone histomorphometry: Outline of theory and practice.
In: OJ Simmons,
AS Kunin (eds)
Skeletal Research,
vol 2.
Academic Press, New York,
pp 237–276.
- 63
Parfitt AM,
Mathews C,
Rao D,
Frame B,
Kleerekoper M,
Villanueva AR
1981
Impairerd osteoblast function in metabolic bone disease.
In: HF DeLuca,
H Frost,
W Jee,
C Johnston,
AM Parfitt (eds)
Osteoporosis: Recent Advances in Pathogenesis and Treatment.
University Park Press, Baltimore,
pp 321–330.
- 64
Parfitt AM,
Villanueva AR
1982
Hypophosphatemia and osteoblast function in human bone disease. In: Massry SG, Letteri JM, Ritz E (eds) Proc 5th International Workshop in Phosphate and Other Minerals. Regulation of Phosphate and Mineral Metabolism.
Adv Exp Med Biol
151:
209–216.
- 65
Wu K,
Jett S,
Frost HM
1967
Bone resorption rates in rib in physiological, senile, and postmenopausal osteoporoses.
J Lab Clin Med
69:
810–818.
- 66
Gruber HE,
Ivey JL,
Thompson ER,
Chestnut CH III,
Baylink DJ
1986
Osteoblast and osteoclast cell number and cell activity in postmenopausal osteoporosis.
Mineral Electrolyte Metab
12:
246–254.
- 67
Evans RA,
Flynn J,
Dunstan CR,
George CRP,
McDonnell GD
1982
Bone metabolism in chronic renal failure.
Mineral Electrolyte Metab
7:
207–218.
- 68
Frost HM
1983
Bone histomorphometry: Correction of the labeling “escape error”.
In: RR Recker (ed)
Bone Histomorphometry. Techniques and Interpretations.
CRC Press, Boca Raton,
pp 133–142.
- 69
Arlot M,
Edouard C,
Meunier PJ,
Neer RM,
Reeve J
1984
Impaired osteoblast function in osteoporosis: Comparison between calcium balance and dynamic histomorphometry.
Br Med J
289:
517–520.
- 70
Jones SJ,
Boyde A,
Ali NN,
Maconnachie E
1985
A review of bone cell and substratum interactions. An illustration of the role of scanning electron microscopy.
Scanning
7:
5–24.
- 71
Kragstrup J,
Melsen F
1983
Three-dimensional morphology of trabecular bone osteons reconstructed from serial sections. Metab.
Bone Dis & Rel Res
5:
127–130.
- 72
Frost HM
1987
Vital Biomechanics.
Proposed general concepts for skeletal adaptations to mechanical usage. Calcif Tissue Int (in press).
- 73
Riggs DS
1963
The Mathematical Approach to Physiologic Problems.
Williams and Wilkins, Baltimore.
- 74
Young DS
1987
Implementation of SI units for clinical laboratory data. Style specifications and conversion tables.
Ann Intern Med
10:
114–129.
