accuracy of mri technique in measuring tendon cross-sectiona area

8/11/2019 Accuracy of MRI Technique in Measuring Tendon Cross-sectiona Area

http://slidepdf.com/reader/full/accuracy-of-mri-technique-in-measuring-tendon-cross-sectiona-area 1/5

SHORT COMMUNICATION

Accuracy of MRI technique in measuring tendoncross-sectional areaC. Couppe1,2, R. B. Svensson1, V. Sødring-Elbrønd3, P. Hansen4, M. Kjær1 and S. P. Magnusson1,2

1Faculty of Health Sciences, Institute of Sports Medicine, Bispebjerg Hospital and Center for Healthy Aging, University of Copenhagen, Copenhagen NV,Denmark, 2Department of Physical Therapy, Bispebjerg Hospital, University of Copenhagen, Copenhagen NV, Denmark, 3Department of Basic Animal andVeterinary Sciences/Anatomy & Cell Biology, University of Copenhagen, Copenhagen NV, Denmark, and 4Department of Radiology, Bispebjerg Hospital,University of Copenhagen, Copenhagen NV, Denmark

Summary

CorrespondenceChristian Couppe, Institute of Sports Medicine

Copenhagen, Bispebjerg Hospital, Building 8, 1st.

floor. Bispebjerg Bakke 23 2400 Copenhagen NV,Denmark

E-mail: [email protected]

Accepted for publicationReceived 01 May 2013;accepted 29 August 2013

Key wordsaccuracy; cross-sectional area; mould; MRI;

tendon

Magnetic resonance imaging (MRI) has commonly been applied to determine ten-don cross-sectional area (CSA) and length either to measure structural changes or

to normalize mechanical measurements to stress and strain. The ability to repro-duce CSA measurements on MRI images has been reported, but the accuracy inrelation to actual tendon dimensions has never been investigated. The purpose of this study was to compare tendon CSA measured by MRI with that measured invitro with the mould casting technique. The knee of a horse was MRI-scanned with1.5 and 3 tesla, and two examiners measured the patellar tendon CSA. Thereafter,the patellar tendon of the horse was completely dissected and embedded in analginate cast. The CSA of the embedded tendon was measured directly by opticalimaging of the cast impression. 1.5 tesla grey tendon CSA and 3 tesla grey tendonCSA were 16.5% and 13.2% lower than the mould tendon CSA, respectively. Also,3 tesla tendon CSA, based on the red-green border on the National Institute of Health (NIH) colour scale, was lower than the mould tendon CSA by 2.8%. The

typical error between examiners was below 2% for all the measured CSA. The typi-cal error between examiners was below 2% for all the measured CSA. These datashow that measuring tendon CSA on the grey-scale MRI images is associated withan underestimation, but by optimizing the measurement using a 3 tesla MRI andthe appropriate NIH colour scale, this underestimation could be reduced to 2.8%compared with the direct measurements on the mould.

Introduction

Force generated by muscle is transferred to bones viatendons to produce movement (Elliott, 1965; Alexander

& Bennet-Clark, 1977; Butler et al., 1978; Biewener &Baudinette, 1995; Magnusson et al., 2008). Tendons have tra-ditionally been considered relatively inert structures, butseveral recent reports demonstrate that human tendons responddirectly to physical activity by increased metabolism (Hannu-kainen et al., 2005; Kalliokoski et al., 2005; Bojsen-Moller et al.,2006) and increased collagen synthesis (Langberg et al., 1999,2001; Christensen et al., 2011). Furthermore, strength trainingand habitual loading of tendons appear to be associated withan increase in tendon size (Arampatzis et al., 2007; Kongsgaardet al., 2007; Couppe et al., 2008), confirming that the

aforementioned responses to elevated loading result in a netincrease in tendon tissue. Studies that have reported increasedtendon cross-sectional area (CSA) used magnetic resonanceimaging (MRI) (Arampatzis et al., 2007; Kongsgaard et al.,

2007; Couppe et al., 2008; Seynnes et al., 2009). Because of itshigh resolution and seemingly good contrast between differenttissues compared with other available imaging modalities(Roberts et al., 1999; Reeves et al., 2003; de Boer et al., 2007),it is the preferable assessment tool to detect modest changes intendon CSA. The MRI technique is able to distinguish betweendifferent structures, but how well the contrast in the imagecorresponds with the actual borders of the tendon remainsunknown, and as a result, the MRI-based measurement mayeither under- or overestimate tendon CSA. Previous attempts todetermine tendon CSA in vitro have resulted in damage to the

Clin Physiol Funct Imaging (2014) 34, pp237–241 doi: 10.1111/cpf.12086

237© 2013 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd 34, 3, 237–241



structure, inaccurate values for non-uniform shapes, labour-intensive techniques or the requirement of rather expensiveequipment (Walker et al., 1964; Lee & Woo, 1988; Race &Amis, 1996). However, recently, one study reported accuratemeasurements of the cross-sectional area of tendon, in vitro,using a simple non-destructive mould casting technique com-monly utilized in dental medical practice (Goodship & Birch,

2005). The purpose of this pilot study was to compare tendonCSA measured by MRI with that measured in vitro using themould casting technique.

Materials and methods

Specimen procedure

A horse cadaver knee was obtained from a 15-year-old horsedonor within 30 min postmortem. The horse knee was placedin a refrigerator at 4°C for 24 h, and then, it was stored at20°C. The knee was allowed to thaw at 4°C for 24 h before

preparation.

MRI procedure

The horse patellar tendon CSA was determined by MRI 1.5tesla (General Electric, Sigma Horizon LX 1.5 Tesla,T1-weighted Spin Echo (SE), Millwaukee, WI, USA) and MRI3 tesla (Siemens Verio, 3 Tesla, T1-weighted SE, Erlangen,Germany). Axial scans were performed perpendicular tothe tendon using the following parameters for 1.5 tesla

(Kongsgaard et al., 2007; Couppe et al., 2008): relaxation time(TR)/echo time (TE) 400/14 ms, field of view (FOV) 20,matrix 256 9 256, slice thickness 5.0 mm and spacing0 mm. For 3 tesla, the following parameters were used: TR/TE 400/14 ms, FOV 20, matrix 512 9 512, slice thickness1.0 mm and spacing 0 mm. Tendon CSA was measured alongits length as previously described (Kongsgaard et al., 2007;

Couppe et al., 2008) at three positions, the central slice usedfor aiming the MRI and two slices 1 cm to either side of thecentral slice (Fig. 1a,d). A pill containing fish oil was attachedin front of the patellar tendon prior to MRI examination inorder to measure MRI and mould examinations in the samelocation. The patellar tendon CSA was manually outlined usingthe software program Osiris 4.19 (http://www.sim.hcuge.ch/osiris/). A phantom (plastic tube) containing 1.0% CuSO4,which was also scanned in the MRI, was placed in FOV tonormalize the tendon signal intensity (Carroll et al., 2008).The colour intensity of each image was adjusted using theNational Institute of Health (NIH) colour scale mode of the

software by setting the intensity of the phantom as the maxi-mum value. Tendon CSA was measured using the grey scalefor 1.5 tesla and 3 tesla. To optimize the measuring protocol,the NIH colour scale was also used to measure tendon CSAfor 3 tesla. Here, the red-green border was used as the borderfor the tendon (Fig. 1f). The details of the measurement,including the reliability of the method in our laboratory (Kon-gsgaard et al., 2007, 2009; Couppe et al., 2008) and elsewhere(Carroll et al., 2008; Seynnes et al., 2009), has been reportedpreviously. Two different examiners measured tendon CSA.

(a) (d)

(b) (e)

(c) (f)

Figure 1 Tendon cross-sectional area (CSA)was measured using the grey scale for 1.5tesla and 3 tesla (b+e). To optimize themeasuring protocol, the National Institute of Health (NIH) colour scale was also used tomeasure tendon CSA for 3 tesla (f). Here, thered-green border was used as the border forthe tendon (f).

© 2013 Scandinavian Society of Clinical Physiology and Nuclear Medicine. Published by John Wiley & Sons Ltd 34, 3, 237–241

Accuracy of MRI in measuring tendon size, C. Couppe et al.238



Mould procedure

The patella and tibial tubercle were removed from the kneewith a saw. The horse patellar tendon was then embedded ina mould made of an alginate dental impression material (Blue-print Cremi, DENTPLY De trey, Germany) as described byGoodship & Birch (2005) (Fig. 2). Using a glass tube of well-

defined CSA, we found that the mould shrinks by 3.6%. Thiswas accounted for in the reported moulds’ CSA.

Mould tendon CSA

The mould was cut in the transverse plane at the three posi-tions corresponding to the MRI sections, and the tendon wasremoved. A small piece of graph paper was placed on top of the mould sections to aid in focusing and to function as aninternal standard to account for small differences in focus(Fig. 2). Digital images were taken using microscope(SMZ1000, Nikon, Tokyo, Japan) to measure the tendon CSA

by image analysis (Scion image, NIH). Two examiners mea-sured the CSA.

Statistical analysis

Typical error percentage was used to analyse the reliability of measures between 2 examiners. The typical error percentage iscalculated as ðSDdiff =

ffiffiffi

2p

MeanoverallÞ 100 and provides ameasure of the relative measurement error (Hopkins, 2000).Results are reported as means (SD).

Results

The values of the measurements of the moulding techniqueand MRI are shown in Table 1. 1.5 tesla grey tendon CSA and3 tesla grey tendon CSA were 16.5% and 13.2% lower thanthe mould tendon CSA, respectively. Also, 3 tesla tendon CSA,

based on the red – green border on the NIH colour scale, waslower than the mould tendon CSA by 2.8%. The typical errorbetween examiners was below 2% for all the measured CSA(Table 2).

Discussion

To the best of our knowledge, this is the first pilot study thathas examined how well MRI-measured CSA corresponds to theactual tendon CSA. We found an underestimation of 2.8% of the tendon CSA using 3 tesla red-green MRI compared with thedirect measurements from the mould, which indicates that withthis optimized CSA measurement procedure, the contrast of MRI represents the tissue uniquely. By comparison, measure-ments on the grey-scale images resulted in a significantly greaterunderestimation of tendon CSA by 16.5% (1.5 tesla grey MRI)and 13.2% (3 tesla grey MRI). The reason for this underestima-tion is likely that the high-intensity signal of the surroundingtissue overlaps the low-intensity signal of the tendon.

While tendon CSA may seem relatively easy to measure,previous studies have shown that it may be a challenge toaccurately determine tendon dimension due to dehydration,compression or damage of tendon (Lee & Woo, 1988; Race &Amis, 1996). Furthermore, inaccurate values for non-uniformshapes, labour-intensive techniques and requirement of expen-sive equipment are also difficulties that have been associatedwith measuring the tendon in vitro (Walker et al., 1964; Lee &Woo, 1988; Race & Amis, 1996). In the present study, weused a simple non-destructive mould casting techniquethat have reported accurate measurements of tendon size(Goodship & Birch, 2005). However, using a glass tube with

Figure 2 The tendon was dissected out and embedded in a mould-ing material. The mould was then cut into sections equivalent to MRIscans and cross-sectional areas compared.

Table 1 The values of the mould and MRI measurements.

CSA mm2

Difference frommould (mm2 )

Mould 88.4 (1.1)1.5 tesla Grey 73.6 (0.7) 14.6 [16.5%]3 tesla Grey 76.5 (0.8) 11.7 [13.2%]3 tesla Red-green 85.8 (0.6) 2.5 [2.8%]

Values are mean (SD) between two examiners for mould and for MRI.

Table 2 The values of the mould and MRI measurements betweenthe two examiners.

Examiner 1(mm2 )

Examiner 2(mm2 )

Inter examiner typical error (mm2 )

Inter examiner typicalerror %

Mould 88.9 88.0 0.39 0.441.5 tesla

Grey75.2 72.0 1.30 1.76

3 tesla Grey 75.9 77.2 0.76 1.003 tesla

Red-green84.1 87.5 1.35 1.58


Accuracy of MRI in measuring tendon size, C. Couppe et al. 239



a well-defined CSA, we found that the mould consistentlyshrunk by 3.6%, which was accounted for in the reported ten-don CSA values based on mould measurement. This shrinkingof the mould has not been reported before. Although themould casting technique may not necessarily be a gold stan-dard to use as reference because shrinkage was detected, itmay still be a useful technique to validate other tendon struc-

tures in future studies.Therefore, only the mould was used for determining the ten-

don CSA by the optical imaging, because the correspondingtendon pieces were affected by flaring and dehydration(Goodship & Birch, 2005). Therefore, we assumed that themould would best represent the tendon CSA compared withMRI scanning. As shown in Fig. 1f, the contrast of the sur-rounding tissue is greater on 3 tesla MRI compared with 1.5tesla (Fig. 1c) (the transition from blue to red is narrower).The higher contrast enables an examiner to better trace the out-line of the tendon and thereby reduce the error in measuringtendon CSA, in vivo. The typical percentage error of repeated

measures of site-specific tendon CSA of MRI images for oneexaminer has previously been reported to be 2.0 – 2.5%(Couppe et al., 2008), and in the present study, the typical errorpercentage of measures between two examiners was below 2%.These data highlight that a well-defined protocol must be usedto ensure low variability, especially if the aim is to detect thosemodest changes (5 – 6%) that can be expected to accompanyshort-term resistance training interventions (Arampatzis et al.,2007; Kongsgaard et al., 2007; Seynnes et al., 2009).

It should be noted that more inexpensive imaging tech-niques, such as ultrasound imaging, have not been able todetect changes in tendon CSA in prospective studies (Robertset al., 1999; Reeves et al., 2003; de Boer et al., 2007; Malliaraset al., 2013). The reason for this is maybe due to lower con-trast between different tissues, which becomes inherentlyassociated with measurement inaccuracy. In addition, it is

necessary to standardize the image contrast (here using aCuSO4 phantom) to accurately define the tendon outline,which is not possible with ultrasound. Taken together, 3 teslared-green MRI provides seemingly good contrast between dif-ferent tissues compared with other available imaging modali-ties and is therefore the preferable assessment tool to detectmodest changes in tendon CSA.

For this experiment, a tendon of roughly the same size asthat of humans was used and it had to be freshly harvested toensure normal hydration and thus contrast in the MRI. Forthis purpose, horse tendon is suitable, but because of the lowavailability, it precludes a greater sample size. To reduce therisk of systematic error caused by the reduced contrast, weused two examiners.

In conclusion, these data show that measuring CSA on thegrey-scale MRI images is associated with an underestimation,but by optimizing the measurement using a 3 tesla MRI andthe appropriate NIH colour scale, this underestimation couldbe reduced to 2.8% compared with the direct measurements

on the mould.

Acknowledgments

We thank Professor Dr.med. Preben Dybdahl-Thomsen,Department of Basic Animal and Veterinary Sciences/Anatomy& Cell Biology, University of Copenhagen, Denmark, and MRItechnician, Berit Sorensen, Department of Radiology, Bispeb-jerg Hospital, University of Copenhagen, Denmark, for theirexemplary technical assistance. The Danish Medical ResearchCouncil and the Danish Rheumatism Association supportedthis work.

Conflict of interest

The authors have no conflict of interests.

References

Alexander RM, Bennet-Clark HC. Storage of elastic strain energy in muscle and other tis-sues. Nature, (1977); 265: 114 – 117.

Arampatzis A, Karamanidis K, Albracht K.Adaptational responses of the human Achil-les tendon by modulation of the applied

cyclic strain magnitude. J Exp Biol (2007);210: 2743 – 2753.

Biewener A, Baudinette R. In vivo muscle forceand elastic energy storage during steady-speed hopping of tammar wallabies (Macropuseugenii). J Exp Biol (1995); 198: 1829 – 1841.

de Boer MD, Maganaris CN, Seynnes OR,Rennie MJ, Narici MV. Time course of mus-cular, neural and tendinous adaptations to23 day unilateral lower-limb suspension inyoung men. J Physiol (2007); 583:1079 – 1091.

Bojsen-Moller J, Kalliokoski KK, Seppanen M,Kjaer M, Magnusson SP. Low-intensity ten-sile loading increases intratendinous glucoseuptake in the Achilles tendon. J Appl Physiol(2006); 101: 196 – 201.

Butler DL, Grood ES, Noyes FR, Zernicke RF.

Biomechanics of ligaments and tendons.Exerc Sport Sci Rev (1978); 6: 125 – 181.

Carroll CC, Dickinson JM, Haus JM, Lee GA,Hollon CJ, Aagaard P, Magnusson SP,Trappe TA. Influence of aging on the invivo properties of human patellar tendon.

J Appl Physiol (2008); 105: 1907 – 1915.Christensen B, Dandanell S, Kjaer M,

Langberg H. Effect of anti-inflammatorymedication on the running-induced rise inpatella tendon collagen synthesis in humans.

J Appl Physiol (2011); 110: 137 – 141.

Couppe C, Kongsgaard M, Aagaard P, HansenP, Bojsen-Moller J, Kjaer M, Magnusson SP.Habitual loading results in tendon hypertro-phy and increased stiffness of the humanpatellar tendon. J Appl Physiol (2008); 105:805 – 810.

Elliott DH. Structure and function of mamma-lian tendon. Biol Rev Camb Philos Soc (1965);40: 392 – 421.

Goodship AE, Birch HL. Cross sectional areameasurement of tendon and ligament invitro: a simple, rapid, non-destructive tech-nique. J Biomech (2005); 38: 605 – 608.

Hannukainen J, Kalliokoski KK, Nuutila P,Fujimoto T, Kemppainen J, Viljanen T,Laaksonen MS, Parkkola R, Knuuti J, KjaerM. In vivo measurements of glucose uptakein human Achilles tendon during different


Accuracy of MRI in measuring tendon size, C. Couppe et al.240



exercise intensities. Int J Sports Med (2005);26: 727 – 731.

Hopkins WG. Measures of reliability in sportsmedicine and science. Sports Med (2000); 30:1 – 15.

Kalliokoski KK, Langberg H, Ryberg AK,Scheede-Bergdahl C, Doessing S, Kjaer A,Boushel R, Kjaer M. The effect of dynamic

knee-extension exercise on patellar tendonand quadriceps femoris muscle glucoseuptake in humans studied by positron emis-sion tomography. J Appl Physiol (2005); 99:1189 – 1192.

Kongsgaard M, Reitelseder S, Pedersen TG,Holm L, Aagaard P, Kjaer M, Magnusson SP.Region specific patellar tendon hypertrophyin humans following resistance training. ActaPhysiol (Oxf) (2007); 191: 111 – 121.

Kongsgaard M, Kovanen V, Aagaard P,Doessing S, Hansen P, Laursen AH, KaldauNC, Kjaer M, Magnusson SP. Corticosteroidinjections, eccentric decline squat training

and heavy slow resistance training in

patellar tendinopathy. Scand J Med Sci Sports(2009); 19: 790 – 802.

Langberg H, Skovgaard D, Petersen LJ, Bulow J, Kjaer M. Type I collagen synthesis and deg-radation in peritendinous tissue after exercisedetermined by microdialysis in humans.

J Physiol (1999); 521(Pt 1): 299 – 306.Langberg H, Rosendal L, Kjaer M. Training-

induced changes in peritendinous type I col-lagen turnover determined by microdialysisin humans. J Physiol (2001); 534: 297 – 302.

Lee TQ, Woo SL. A new method for determin-ing cross-sectional shape and area of soft tis-sues. J Biomech Eng (1988); 110: 110 – 114.

Magnusson SP, Narici MV, Maganaris CN,Kjaer M. Human tendon behaviour and adap-tation, in vivo. J Physiol (2008); 586: 71 – 81.

Malliaras P, Kamal B, Nowell A, Farley T,Dhamu H, Simpson V, Morrissey D,Langberg H, Maffulli N, Reeves ND. Patellartendon adaptation in relation to load-intensity and contraction type. J Biomech,

(2013); 46: 1893 –

1899.

Race A, Amis AA. Cross-sectional areameasurement of soft tissue. A new castingmethod. J Biomech (1996); 29: 1207 – 1212.

Reeves ND, Maganaris CN, Narici MV.Effect of strength training on humanpatella tendon mechanical properties of older individuals. J Physiol (2003); 548:971 – 981.

Roberts CS, King DH, Goldsmith LJ. A statisti-cal analysis of the accuracy of sonographyof the patellar tendon. Arthroscopy (1999);15: 388 – 391.

Seynnes OR, Erskine RM, Maganaris CN,Longo S, Simoneau EM, Grosset JF, NariciMV. Training-induced changes in structuraland mechanical properties of the patellartendon are related to muscle hypertrophy,but not to strength gains. J Appl Physiol,(2009); 107 : 523 – 530.

Walker LB, Harris EH, Benedict JV. Stress-strain in human cadaveric plantaris tendon:a preliminary study. Med Electron Biol Eng,

(1964); 2 : 31 –

38.


Accuracy of MRI in measuring tendon size, C. Couppe et al. 241

accuracy of mri technique in measuring tendon cross-sectiona area

Documents