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Note: This copy is for your personal, non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights. ORIGINAL RESEARCH n MUSCULOSKELETAL IMAGING 502 radiology.rsna.org n Radiology: Volume 259: Number 2—May 2011 Sonoelastography of the Plantar Fascia 1 Chueh-Hung Wu, MD Ke-Vin Chang, MD Sun Mio, MD Wen-Shiang Chen, MD, PhD Tyng-Guey Wang, MD Purpose: To compare the stiffness of the plantar fascia by using sonoelastography in healthy subjects of different ages, as well as patients with plantar fasciitis. Materials and Methods: The study protocol was approved by the Research Ethics Committee of the hospital, and all of the subjects gave their informed consent. Bilateral feet of 40 healthy sub- jects and 13 subjects with plantar fasciitis (fasciitis group) were examined by using color-coded sonoelastography. Healthy subjects were divided into younger (18–50 years) and older ( . 50 years) groups. The color scheme was red (hard), green (medium stiffness), and blue (soft). The color histogram was subsequently analyzed. Each pixel of the image was separated into red, green, and blue compo- nents (color intensity range, 0–255). The color histogram then computed the mean intensity of each color compo- nent of the pixels within a standardized area. Mixed model for repeated measurements was used for comparison of the plantar fascia thickness and the intensity of the color components on sonoelastogram. Results: Quantitative analysis of the color histogram revealed a sig- nificantly greater intensity of blue in older healthy subjects than in younger (94.5 6 5.6 [ 6 standard deviation] vs 90.0 6 4.6, P = .002) subjects. The intensity of red and green was the same between younger and older healthy subjects ( P = .68 and 0.12). The intensity of red was sig- nificantly greater in older healthy subjects than in the fas- ciitis group (147.8 6 10.3 vs 133.7 6 13.4, P , .001). The intensity of green and blue was the same between older healthy subjects and those in the fasciitis group ( P = .33 and .71). Conclusion: Sonoelastography revealed that the plantar fascia softens with age and in subjects with plantar fasciitis. q RSNA, 2011 1 From the Department of Physical Medicine & Rehabilita- tion, National Taiwan University Hospital Yun-Lin Branch, Yunlin, Taiwan, ROC (C.H.W.); and Department of Physical Medicine & Rehabilitation, National Taiwan University Hospital, 7 Chan-Shan South Road, 100 Taipei, Taiwan, Republic of China (K.V.C., S.M., W.S.C., T.G.W.). Received August 18, 2010; revision requested September 20; revi- sion received November 7; accepted November 26; final version accepted December 9. Address correspondence to T.G.W. (e-mail: [email protected] ). q RSNA, 2011
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Page 1: MUSCULOSKELETAL IMAGING Sonoelastography of the Plantar … · At conventional US ex-amination, all healthy subjects had plan-tar fascia with normal echogenicity. The thickness of

Note: This copy is for your personal, non-commercial use only. To order presentation-ready copies for distribution to your colleagues or clients, contact us at www.rsna.org/rsnarights.

ORIG

INAL

RES

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MUS

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502 radiology.rsna.org n Radiology: Volume 259: Number 2—May 2011

Sonoelastography of the Plantar Fascia 1

Chueh-Hung Wu , MD Ke-Vin Chang , MD Sun Mio , MD Wen-Shiang Chen , MD , PhD Tyng-Guey Wang , MD

Purpose: To compare the stiffness of the plantar fascia by using sonoelastography in healthy subjects of different ages, as well as patients with plantar fasciitis.

Materials and Methods:

The study protocol was approved by the Research Ethics Committee of the hospital, and all of the subjects gave their informed consent. Bilateral feet of 40 healthy sub-jects and 13 subjects with plantar fasciitis (fasciitis group) were examined by using color-coded sonoelastography. Healthy subjects were divided into younger (18–50 years) and older ( . 50 years) groups. The color scheme was red (hard), green (medium stiffness), and blue (soft). The color histogram was subsequently analyzed. Each pixel of the image was separated into red, green, and blue compo-nents (color intensity range, 0–255). The color histogram then computed the mean intensity of each color compo-nent of the pixels within a standardized area. Mixed model for repeated measurements was used for comparison of the plantar fascia thickness and the intensity of the color components on sonoelastogram.

Results: Quantitative analysis of the color histogram revealed a sig-nifi cantly greater intensity of blue in older healthy subjects than in younger (94.5 6 5.6 [ 6 standard deviation] vs 90.0 6 4.6, P = .002) subjects. The intensity of red and green was the same between younger and older healthy subjects ( P = .68 and 0.12). The intensity of red was sig-nifi cantly greater in older healthy subjects than in the fas-ciitis group (147.8 6 10.3 vs 133.7 6 13.4, P , .001). The intensity of green and blue was the same between older healthy subjects and those in the fasciitis group ( P = .33 and .71).

Conclusion: Sonoelastography revealed that the plantar fascia softens with age and in subjects with plantar fasciitis.

q RSNA, 2011

1 From the Department of Physical Medicine & Rehabilita-tion, National Taiwan University Hospital Yun-Lin Branch, Yunlin, Taiwan, ROC (C.H.W.); and Department of Physical Medicine & Rehabilitation, National Taiwan University Hospital, 7 Chan-Shan South Road, 100 Taipei, Taiwan, Republic of China (K.V.C., S.M., W.S.C., T.G.W.). Received August 18, 2010; revision requested September 20; revi-sion received November 7; accepted November 26; fi nal version accepted December 9. Address correspondence to T.G.W. (e-mail: [email protected] ).

q RSNA, 2011

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Radiology: Volume 259: Number 2—May 2011 n radiology.rsna.org 503

MUSCULOSKELETAL IMAGING: Sonoelastography of the Plantar Fascia Wu et al

an Acuson S2000 US system (Siemens, Munich, Germany) with a 6–12-MHz linear transducer (14L5; Siemens). All examinations were conducted by a phy-siatrist (C.H.W.), who had 3 years ex-perience in US. Each subject was exam-ined lying prone with 90° of knee fl exion in the neutral ankle position ( 15 ). In a longitudinal view, the thickness of the plantar fascia was measured from the anterior edge of the inferior calcaneal border vertically to the inferior border of the plantar fascia ( 16 ) ( Fig 1 ).

Sonoelastography was performed by applying gentle compression with the hand-held transducer on the heel. The force applied to the plantar fascia was adjusted according to the quality factor set on the machine and it was displayed on the screen. A quality factor equal to or greater than 60 indicated the optimal compression force. During the examina-tions, the B-mode image and the elasto-gram were displayed concurrently side by side on the screen. The elastogram appeared within a rectangular region of interest as a color-coded image super-imposed over the B-mode image. The color represented the relative stiffness of the tissues within the region of inter-est and ranged from red (hard) to blue (soft) in a continuous spectrum. Thus, green indicated medium stiffness. Dur-ing the examination, the right half of the screen, which showed the elastogram, was covered to avoid intentional in-fluence by the examiner. Elastogram

part, we used quantitative analysis of sonoelastography to compare differing stiffness of the plantar fascia between different age groups. In the second part, we used quantitative analysis of sono-elastography to compare the stiffness of the plantar fascia between healthy sub-jects and patients with plantar fasciitis.

Materials and Methods

Study Population The study was approved by the Re-search Ethics Committee of our hospi-tal. All of the volunteers and patients gave their informed consent.

Bilateral feet of 40 healthy volunteers were examined. The volunteers were di-vided into younger (18–50 years) and older ( . 50 years) groups. None of the volunteers had ever participated in any professional sports or longstanding physi-cal activities. Each volunteer was asked to avoid longer-than-usual standing, walking, or running for a week prior to imaging. Any volunteer who had a his-tory of heel or connective tissue pain, metabolic or endocrine diseases, or cor-ticosteroid injection was excluded from the study.

Thirteen patients with clinical diag-nosis of plantar fasciitis were also ex-amined. Inclusion criteria were (a) heel pain at the plantar fascia insertion of the medial tubercle of the calcaneus, (b) worsening pain when waking up in the morning or after a period of rest ( 14 ), (c) pain duration longer than 6 months, and (d) a visual analog score of more than 4 on a scale of 10. Patients who had received steroid injections or had under-gone shock wave therapy or surgery to the heel were excluded from the study.

Imaging The examination of each plantar fascia included B-mode scanning and sonoelas-tography and was performed by using

P lantar fasciitis is the most com-mon cause of heel pain ( 1 ). De-spite its self-limiting nature, it has

substantial impact on patients’ quality of life ( 2 ). Although the etiology of plan-tar fasciitis is multifactorial, mechanical overload and degeneration have been re-garded as the main factors ( 3 ). A prior systemic review revealed that increased age was one of the factors associated with chronic plantar heel pain ( 4 ). Age-related changes in tendons, as well as specifi c changes to the elastic modulus with degeneration, have been reported in prior studies ( 5–7 ). In some but not all ways, plantar fascia is similar to ten-dons ( 8 ); therefore, age-related changes of elastic modulus may also occur in the plantar fascia.

Sonoelastography is an ultrasono-graphic (US) imaging technique that al-lows a noninvasive estimation of tissue stiffness ( 9 ). It is based on the fact that soft tissue has greater tissue displace-ment than hard tissue when externally compressed. Sonoelastography allows calculation and comparison of tissue dis-placement before and after tissue com-pression with conventional US equip-ment but modifi ed software ( 10 ).

Sonoelastography has been applied to assess the stiffness of various tissues. It has been used to detect tendinopathy in the common extensor tendon of the elbow and to describe the pattern of a normal Achilles tendon ( 11–13 ). Thus, sonoelastography may add information about the mechanical properties of plan-tar fascia in addition to morphology. However, most work with sonoelastog-raphy has been based on visual inspection.

The intention of this study was to gain a more accurate picture of the nexus between age and stiffness and be-tween plantar fasciitis and stiffness. This study consisted of two parts. In the fi rst

Implication for Patient Care

Sonoelastography with quantita- n

tive analysis may provide an ancillary tool for evaluating plan-tar fasciitis.

Advances in Knowledge

Sonoelastography can be used to n

evaluate the stiffness of plantar fascia.

Plantar fascia is softened in the n

elderly and in patients with plan-tar fasciitis.

Published online before print 10.1148/radiol.10101665

Radiology 2011; 259:502–507

Abbreviation: ICC = intraclass correlation coeffi cient

Author contributions: Guarantors of integrity of entire study, C.H.W., W.S.C., T.G.W.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; approval of fi nal version of submitted manuscript, all authors; literature research, C.H.W., K.V.C., S.M., T.G.W.; clinical studies, all authors; experimental studies, K.V.C., W.S.C.; statistical analysis, C.H.W.; and manuscript editing, C.H.W., W.S.C., T.G.W.

Potential confl icts of interest are listed at the end of this article.

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difference in the sex ratio, weight, and body mass index between younger and older subjects. At conventional US ex-amination, all healthy subjects had plan-tar fascia with normal echogenicity. The thickness of the plantar fascia between younger and older healthy subjects was the same (2.4 mm 6 0.3 vs 2.7 mm 6 0.5, P = .19) ( Table ). The interrater reli-ability was found to be an ICC of 0.792 (95% confi dence interval: 0.532, 0.908). Twenty symptomatic plantar fasciae of 13 patients with plantar fasciitis (six men, mean age of 47.8 years 6 16.1; seven women, mean age 50.9 years 6 16.4) were included in the analysis. There was no difference in age, sex ratio, weight, and body mass index between older healthy subjects and those in the fascii-tis group. The thickness of the plantar fascia was signifi cantly thicker in the fasciitis group than in the older healthy subjects at conventional US examina-tion (3.7 mm 6 0.9 vs 2.7 mm 6 0.5, P , .001) ( Table ).

Sonoelastography demonstrated that the plantar fasciae of all the healthy sub-jects generally were hard structures that corresponded to the red color coding. However, whereas in younger subjects a homogeneously red-color coded plantar fascia could be seen on the elastogram ( Fig 2a ), in older subjects some small

the t test to compare weight and body mass index, and the results were ex-pressed as the mean 6 standard devia-tion. The x 2 test was used to test the dif-ference of the qualitative description of the elastogram. The mixed model for re-peated measurements was used to com-pare the thickness of the plantar fasciae and the mean intensity of each color in the elastogram. Fixed effect of the age was applied in this model. Results were expressed as the mean 6 standard de-viation. Intraclass correlation coeffi cient (ICC) was calculated to determine the interrater and intrarater reliability of measurements of the color intensities of the plantar fasciae. The ICC classifi -cations were rated as poor (ICC, 0.00–0.20), fair (ICC, 0.20–0.40), good (ICC, 0.40–0.75), and excellent (ICC . 0.75) ( 17 ). A P value of less than .05 was con-sidered to indicate a statistically sig-nifi cant difference.

Results

Twenty younger healthy subjects (10 men, mean age of 30.6 years 6 3.0; 10 women, mean age of 29.9 years 6 2.7) and 20 older healthy subjects (10 men, mean age of 54.7 years 6 6.3; 10 women, mean age of 56.1 years 6 6.9) were included. Except for age, there was no

images chosen for the analysis were those obtained with B-mode sonography that were of good quality (plantar fascia was horizontal and with clear upper and lower borders) and with the quality factor greater than 60. Three images of each plantar fascia were recorded and all of them were sent to picture archiving and communication system for imaging analysis.

Twelve plantar fasciae of six non-selected volunteers were re-evaluated within 3 days of testing by the original physiatrist and another physiatrist (S.M.). These data were then used to analyze intrarater and interrater reliability for imaging analysis of sonoelastography.

Imaging Analysis For qualitative and quantitative imaging analysis, we selected a standardized rect-angular area, of which the shorter side was 2 mm toward the heel from the point of the inferior border of the calcaneus plantar fascia inserted and the long side was 1 cm distal to the insertion ( Fig 2 ).

For the qualitative description, we used the following visual grading system: grade 1, area of red greater than half of the selected rectangular area mentioned above; grade 2, area of green greater than half of the region of interest, or the area of each color is smaller than half of the selected area; and grade 3, area of blue greater than half of the selected area.

We used Image J software (version 1.42q; National Institutes of Health, Bethesda, Md) for the color histogram of the elastogram of the plantar fascia. Each pixel of the image was separated by the program into red, green, and blue components (color intensity range, 0–255). The higher value defi ned a greater intensity of the color. The color histo-gram then computed the mean intensity of each component of the pixels within the standardized area. For each plantar fascia, the mean values of the red, green, and blue components in the three pic-tures were used for statistical analysis.

Statistical Analysis All statistical analyses were performed by using SPSS version 12.0 for Windows software (SPSS, Chicago, Ill). We used

Figure 1

Figure 1: B-mode US scan shows measurement of the plantar fascia thickness at its insertion of the calcaneus in longitudinal view (+).

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scattered yellow or green areas (that is, intermediate stiffness) were identi-fi ed within the red-coded plantar fascia ( Fig 2b ). In younger subjects, 97.5% of the plantar fasciae were classifi ed with the visual grading system as grade 1 and 2.5%, as grade 2. In older subjects, 85% of the plantar fasciae were classifi ed as grade 1 and 15%, as grade 2 ( P = .048).

Quantitative analysis of the color histogram revealed that the respective mean values for the intensity of red, green, and blue on the elastogram were 148.9, 111.9, and 90.0 for younger subjects and 147.8, 116.5, and 94.5 for older subjects. There was a signifi cantly greater intensity of blue in older subjects than in younger subjects ( P = .002). The intensity of red and green was the same between older and younger healthy subjects ( Table ).

In sonoelastography, generally speak-ing, the plantar fascia in subjects with plantar fasciitis revealed a lesser red-coded area and a greater green-coded area ( Fig 2c ). With the qualitative de-scription, 60% of the plantar fasciae of the fasciitis group were classifi ed as grade 1 and 40%, as grade 2. They were signifi cantly different from those of older healthy subjects ( P = .018). With the quantitative analysis, the mean values for the intensity of red, green, and blue on the elastogram were 133.7, 119.6, and 94.2, respectively, in the fasciitis group. The intensity of red was signifi cantly greater in older healthy subjects than in those in the fasciitis group ( P = .002). The intensity of green and blue was the same between older healthy subjects and those in the fasciitis group ( Table ).

As for reliability of the imaging anal-ysis of sonoelastography, the interrater reliability was found to be an ICC of 0.765 (95% confi dence interval: 0.505, 0.888), and the intrarater reliability was found to be an ICC of 0.818 (95% con-fi dence interval: 0.617, 0.913).

Figure 2

Figure 2: B-mode US scans (left) and elastograms (right) of plantar fascia. Blue rectangle depicts standardized area of qualitative and quantitative analysis of plantar fascia. Images in (a) asymptomatic 26-year-old woman, (b) asymptomatic 58-year-old man, and (c) 51-year-old woman with plantar fasciitis. There was a greater area of green and a smaller area of red within the proximal plantar fascia.

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structures, we did fi nd a similar change of the mechanical properties in their diseased state, that is, softening.

Sonoelastography may provide valu-able information about the characteris-tics of stiffness of the plantar fascia. As for age-related degeneration, age is not signifi cant as a predictor factor in plan-tar fascia thickness ( 15 ). It seemed that, in healthy subjects, age does not play a signifi cant role in plantar fascia thick-ness. Our results that thickness of the plantar fascia was no different between younger and older healthy subjects con-curred with this observation. However, sonoelastography demonstrated that the characteristics of the stiffness differed between younger and older healthy sub-jects. Findings of conventional US exami-nations show that plantar fasciitis may appear as thickening of the plantar fascia, reduced echogenicity within the proximal plantar fascia, and probable fl uid collection ( 19 ). In this study, the thickness of the plantar fascia was shown to be signifi cantly thicker in the fasciitis group than in healthy subjects. There was also a difference in the stiffness of the plantar fascia between healthy subjects and the fasciitis group. Although conventional US examinations have provided valuable information about the morphology of plantar fascia, sonoelas-tography can add information about the mechanical properties of the tissue and can broaden understanding about the disorders of the plantar fascia.

Although the US examination is a highly operator-dependent technique, fi ndings of this study nevertheless showed excellent interpretive reliability for the sonoelastography measurements and color histogram analysis. The set-ting of the quality factor at more than 60 to indicate optimal compression force of the transducer on the heel was used as an internal standard of sonoelastogra-phy, as well as an aid to avoid artifacts caused by too heavy or too gentle pres-sure. Furthermore, by standardizing the region of interest of sonoelastography and the specifi c area for imaging analy-sis, we were able to minimize the vari-ability of analysis with color histogram between different examiners. The ex-cellent reliability of this self-designed

of the plantar fascia. Young’s modulus and strain ratio measurements were not obtained in this study. Analyzing the color histogram of the sonoelastograms allowed us not only to calculate quanti-tatively the intensity of different colors, but also to achieve a more objective com-parison than that with qualitative anal-ysis alone. Moreover, the method was able to be used readily in conjunction with commercially available sonoelastog-raphy. This approach may therefore be useful in providing additional informa-tion and a more objective interpretation than qualitative analysis of color-coded sonoelastography.

As for the comparison between healthy subjects and the fasciitis group, sonoelastography revealed that the per-centage of the plantar fasciae rated as grade 1 was lower for the plantar fascii-tis subjects than for similar-aged healthy subjects. With quantitative analysis, while the intensity of the green and blue com-ponents was the same for the fasciitis group and similar-aged healthy subjects, the intensity of the red component of the fasciitis group was significantly smaller than that of similar-aged healthy subjects, thus indicating that plantar fas-ciitis subjects had a softer plantar fas-cia. In a prior study, sonoelastography has revealed softening of the common extensor tendon in patients with lateral epicondylitis ( 11 ). Although plantar fas-ciae and tendons were different in their

Discussion

Sonoelastography depicted homogeneous red coloring of the plantar fascia in younger healthy subjects and scattered yellow or green areas within the red-colored plantar fascia in older healthy subjects. The percentage of the plantar fasciae rated as grade 1 was also lower in those older than 50 years. This sug-gests that, with aging, the plantar fas-cia of healthy subjects becomes softer. These results suggest that age-related phenomenon of the plantar fascia is, at least partially, associated with softening. In prior studies, age-related softening of tendon was reported ( 3,18 ). Although the plantar fascia is not structurally identical to tendons, these fi ndings indi-cated age-related softening of the plan-tar fascia, a similar condition noted in tendons.

With quantitative analysis, we found a signifi cantly greater intensity of blue in the plantar fascia of those older than 50 years than those younger than 50 years. This greater intensity of blue for the older subjects, indicative of more pixels within the plantar fascia located farther away from the red color in a con-tinuous spectrum, was a notable distinc-tion given that the red and green com-ponents showed as the same in younger and older healthy subjects. Our results were also consistent with the qualita-tive description of age-related softening

Characteristics and US and Sonoelastography Findings

VariableYounger Healthy Subjects

Older Healthy Subjects Fasciitis Group

P Value (Younger vs Older)

P Value (Older vs Fasciitis)

Age (y) 30.3 6 2.8 55.4 6 6.5 49.5 6 15.7 , .001 .11M/F ratio 10:10 10:10 6:7No. of plantar fasciae 40 40 20Weight (kg) 63.0 6 12.8 60.9 6 10.1 62.3 6 11.2 .74 .68BMI (kg/m 2 ) 21.8 6 3.0 23.1 6 2.4 23.5 6 3.8 .098 .78Plantar fascia thickness 2.4 6 0.3 2.7 6 0.5 3.7 6 0.9 .19 , .001Plantar fascia red * 148.9 6 8.5 147.8 6 10.3 133.7 6 13.4 .68 .002Plantar fascia green * 111.9 6 9.9 116.5 6 11.5 119.6 6 12.5 .12 .33Plantar fascia blue * 90.0 6 4.6 94.5 6 5.6 94.2 6 9.6 .002 .71

Note.—Data are means 6 standard deviation. BMI = body mass index.

* Statistical method was a mixed model for repeated measurements.

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MUSCULOSKELETAL IMAGING: Sonoelastography of the Plantar Fascia Wu et al

analysis was indicated by the high value of interrater and intrarater ICC.

This study had several limitations. First, a small area analyzed on the color histogram does not represent the en-tire plantar fascia. However, since the abnormality in plantar fasciitis occurred mostly near the site of the origin of plantar fascia at the medial tuberosity of the calcaneus ( 1 ), we chose that site as the standardized area that represents the greater part of the lesion. We chose a height of 2 mm (short side of the rect-angular area) to avoid including the area outside the plantar fascia, because most normal plantar fasciae were thicker than 2 mm ( 14,19 ). Furthermore, because of the not parallel course of the fascia in that area, it might be problematic to perform sonoelastography. When performing so-noelastography, we adjusted the posi-tion and the tilting angle of the trans-ducer to avoid anisotropy on a B-mode sonogram, to minimize the effect of the not parallel course of the fascia. Second, no histologic testing was performed in this study. Further histopathologic and biomechanical examinations are needed to confi rm our results. Nonetheless, our study has demonstrated sonoelastogra-phy to be a reliable, in vivo noninvasive technique for examining the stiffness of the plantar fascia. Third, since this study was a cross-sectional design, it was not possible to confi rm whether a softened plantar fascia was the cause or the effect of plantar fasciitis. A longi-tudinal, prospective study is warranted to verify this. Fourth, observers in this study were not blinded and the produc-tion of images in elastography may be biased. Because it was diffi cult to con-ceal the subjects’ age and the thickness and echogenecity of plantar fascia on sonograms during the examination, we tried to minimize intentional infl uence on the elastography from the examiner by covering the right half of the screen.

Fifth, reliability of the image production, which was the most operator-dependent step in sonoelastography, was not mea-sured in this study. Since the primary aim of this study was not to examine the reliability of performing sonoelas-tography, we only tested the reliability of quantitative analysis, and excellent in-terpretive reliability was obtained.

In conclusion, sonoelastography with quantitative image analysis demonstrates age-related softening of the plantar fas-cia and also softening of the plantar fas-cia in subjects with plantar fasciitis.

Disclosures of Potential Confl icts of Interest: C.H.W. No potential confl icts of interest to dis-close. K.V.C. No potential confl icts of interest to disclose. S.M. No potential confl icts of interest to disclose. W.S.C. No potential confl icts of in-terest to disclose. T.G.W. No potential confl icts of interest to disclose.

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