Histomorphometric,CT Arthrographic,and Biomechanical Mapping of the Human Ankle

Abstract

Background:

The specific morphological and biomechanical characteristics of the osteochondral unit of the ankle joint are not yet fully understood. This anatomical study aimed to map regional thickness of the articular hyaline uncalcified cartilage and its adjacent layers of mineralized cartilage and subchondral bone as well as to measure the regional indentation stiffness of human ankle joint cartilage.

Materials and Methods:

A total of 20 pairs of human cadaver ankle joints (median age: 78 years) were evaluated by histomorphometry and multidetector row double-contrast CT arthrography for cartilage thickness in 17 distinct anatomical regions. In addition, regional distribution of the subchondral bone plate and of the mineralized cartilage was scrutinized histologically. Cartilage indentation stiffness was measured using an arthroscopic handheld device (Artscan200), especially validated for use in thin cartilage. The correlation between the thickness of different components of the osteochondral unit and the cartilage indentation stiffness was evaluated.

Results:

The thinnest uncalcified cartilage was measured at the anterior talar dome and the distal fibula. The thickest uncalcified cartilage was found in the mid and posterior talar dome, as well as in the tibial plafond. Mineralized cartilage and subchondral bone showed highest values at the anteromedial talar dome. Cartilage indentation stiffness showed a bicentric distribution pattern in 14/20 ankle pairs and was highest in regions with thin cartilage. Positive correlation between the thickness of the mineralized cartilage and the subchondral bone plate was found. No correlation between the thickness of the uncalcified and the mineralized cartilage could be identified.

Conclusion:

This anatomical study provides a comprehensive mapping of the osteochondral unit of the human ankle joint in elderly people. Articular hyaline uncalcified cartilage and the subchondral bone plate showed clear regional differences and were reciprocally distributed. Cartilage indentation stiffness was inversely correlated to cartilage thickness in elderly people.

Clinical Relevance:

Thorough understanding of the osteochondral unit of the ankle joint could be helpful for clinicians and researchers in the development of improved operative repair techniques for osteochondral defects in the ankle joint, for example, in constructing specific tissue-engineered osteochondral plugs.

Keywords

ankle joint regional thickness hyaline uncalcified cartilage mineralized cartilage subchondral bone double-contrast CT arthrography cartilage indentation stiffness

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References

Adam

Eckstein

Milz

. The distribution of cartilage thickness within the joints of the lower limb of elderly individuals. J Anat. 1998;193(pt 2):203-214.

Appleyard

Swain

Khanna

. The accuracy and reliability of a novel handheld dynamic indentation probe for analysing articular cartilage. Phys Med Biol. 2001;46:541-550.

Athanasiou

Niederauer

Schenck

Jr.

Biomechanical topography of human ankle cartilage. Ann Biomed Eng. 1995;23:697-704.

Bae

Temple

Amiel

. Indentation testing of human cartilage: sensitivity to articular surface degeneration. Arthritis Rheum. 2003;48:3382-3394.

Canale

Belding

. Osteochondral lesions of the talus. J Bone Joint Surg Am. 1980;62:97-102.

Cole

Margulis

Kuettner

. Distinguishing ankle and knee articular cartilage. Foot Ankle Clin. 2003;8:305-316.

Demetriades

Strauss

Gallina

. Osteoarthritis of the ankle. Clin Orthop Relat Res. 1998;349:28-42.

Duncan

Jundt

Riddle

. The tibial subchondral plate: a scanning electron microscopic study. J Bone Joint Surg Am. 1987;69:1212-1220.

El-Khoury

Alliman

Lundberg

. Cartilage thickness in cadaveric ankles: measurement with double-contrast multi-detector row CT arthrography versus MR imaging. Radiology. 2004;233:768-773.

10.

Elias

Zoga

Morrison

. Osteochondral lesions of the talus: localization and morphologic data from 424 patients using a novel anatomical grid scheme. Foot Ankle Int. 2007;28:154-161.

11.

Erben

. Embedding of bone samples in methylmethacrylate: an improved method suitable for bone histomorphometry, histochemistry, and immunohistochemistry. J Histochem Cytochem. 1997;45:307-313.

12.

Gobbi

Nunag

Malinowski

. Treatment of full thickness chondral lesions of the knee with microfracture in a group of athletes. Knee Surg Sports Traumatol Arthrosc. 2005;13:213-221.

13.

Hangody

Feczko

Bartha

. Mosaicplasty for the treatment of articular defects of the knee and ankle. Clin Orthop Relat Res. 2001;391:S328-S336.

14.

Hayes

Keer

Herrmann

. A mathematical analysis for indentation tests of articular cartilage. J Biomech. 1972;5:541-551.

15.

Kempson

. Age-related changes in the tensile properties of human articular cartilage: a comparative study between the femoral head of the hip joint and the talus of the ankle joint. Biochim Biophys Acta. 1991;1075:223-230.

16.

Koepp

Eger

Muehleman

. Prevalence of articular cartilage degeneration in the ankle and knee joints of human organ donors. J Orthop Sci. 1999;4:407-412.

17.

Kuettner

Cole

. Cartilage degeneration in different human joints. Osteoarthritis Cartilage. 2005;13:93-103.

18.

Laasanen

Toyras

Hirvonen

. Novel mechano-acoustic technique and instrument for diagnosis of cartilage degeneration. Physiol Meas. 2002;23:491-503.

19.

Lyyra

Jurvelin

Pitkanen

. Indentation instrument for the measurement of cartilage stiffness under arthroscopic control. Med Eng Phys. 1995;17:395-399.

20.

Lyyra

Kiviranta

Vaatainen

. In vivo characterization of indentation stiffness of articular cartilage in the normal human knee. J Biomed Mater Res. 1999;48:482-487.

21.

Lyyra-Laitinen

Niinimaki

Toyras

. Optimization of the arthroscopic indentation instrument for the measurement of thin cartilage stiffness. Phys Med Biol. 1999;44:2511-2524.

22.

Mak

Lai

Mow

. Biphasic indentation of articular cartilage—I. Theoretical analysis. J Biomech. 1987;20:703-714.

23.

Millington

Grabner

Wozelka

. Quantification of ankle articular cartilage topography and thickness using a high resolution stereophotography system. Osteoarthritis Cartilage. 2007;15:205-211.

24.

Milz

Putz

. Quantitative morphology of the subchondral plate of the tibial plateau. J Anat. 1994;185(pt 1):103-110.

25.

Muehleman

Berzins

Koepp

. Bone density of the human talus does not increase with the cartilage degeneration score. Anat Rec. 2002;266:81-86.

26.

Muller-Gerbl

Schulte

Putz

. The thickness of the calcified layer in different joints of a single individual. Acta Morphol Neerl Scand. 1987;25:41-49.

27.

Muller-Gerbl

Schulte

Putz

. The thickness of the calcified layer of articular cartilage: a function of the load supported? J Anat. 1987;154:103-111.

28.

O’Loughlin

Heyworth

Kennedy

. Current concepts in the diagnosis and treatment of osteochondral lesions of the ankle. Am J Sports Med. 2010;38:392-404.

29.

Outerbridge RE: The etiology of chondromalacia patellae. J Bone Joint Surg Br. 1961;43B:752-757.

30.

Pastoureau

Chomel

. Methods for cartilage and subchondral bone histomorphometry. Methods Mol Med. 2004;101:79-91.

31.

Peterson

Minas

Brittberg

. Two- to 9-year outcome after autologous chondrocyte transplantation of the knee. Clin Orthop Relat Res. 2000;374:212-234.

32.

Pritzker

Gay

Jimenez

. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage. 2006;14:13-29.

33.

Revell

Pirie

Amir

. Metabolic activity in the calcified zone of cartilage: observations on tetracycline labelled articular cartilage in human osteoarthritic hips. Rheumatol Int. 1990;10:143-147.

34.

Saltzman

Salamon

Blanchard

. Epidemiology of ankle arthritis: report of a consecutive series of 639 patients from a tertiary orthopaedic center. Iowa Orthop J. 2005;25:44-46.

35.

Shepherd

Seedhom

. The “instantaneous” compressive modulus of human articular cartilage in joints of the lower limb. Rheumatology (Oxford). 1999;38:124-132.

36.

Shepherd

Seedhom

. Thickness of human articular cartilage in joints of the lower limb. Ann Rheum Dis. 1999;58:27-34.

37.

Steadman

Rodkey

Rodrigo

. Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop Relat Res. 2001;391:S362-S369.

38.

Sugimoto

Takakura

Tohno

. Cartilage thickness of the talar dome. Arthroscopy. 2005;21:401-404.

39.

Swann

Seedhom

. Improved techniques for measuring the indentation and thickness of articular cartilage. Proc Inst Mech Eng H. 1989;203:143-150.

40.

Swann

Seedhom

. The stiffness of normal articular cartilage and the predominant acting stress levels: implications for the aetiology of osteoarthrosis. Br J Rheumatol. 1993;32:16-25.

41.

Treppo

Koepp

Quan

. Comparison of biomechanical and biochemical properties of cartilage from human knee and ankle pairs. J Orthop Res. 2000;18:739-748.

42.

Valderrabano

Leumann

Rasch

. Knee-to-ankle mosaicplasty for the treatment of osteochondral lesions of the ankle joint. Am J Sports Med. 2009;37(suppl 1):105S-111S.

43.

van Dijk

Reilingh

Zengerink

. Osteochondral defects in the ankle: why painful? Knee Surg Sports Traumatol Arthrosc. 2010;18:570-580.

44.

Wang

Ying

Duan

. Histomorphometric analysis of adult articular calcified cartilage zone. J Struct Biol. 2009;168:359-365.

45.

Weileder

. Die “Physiologische Inkongruenz” des oberen Sprunggelenkes—ein optimiertes biologisches Bauprinzip auch in nicht-sphärischen Gelenken? Anatomische Anstalt Lehrstuhl I Munich, Ludwigs-Maximilians-Universität München, 67.