Clinical Study Clinical Features Associated with Frozen

Clinical StudyClinical Features Associated with Frozen ShoulderSyndrome in Parkinsonrsquos Disease

Ya-Ting Chang12 Wen-Neng Chang2 Nai-Wen Tsai2 Kuei-Yueh Cheng2

Chih-Cheng Huang2 Chia-Te Kung3 Yu-Jih Su14 Wei-Che Lin5 Ben-Chung Cheng14

Chih-Min Su13 Yi-Fang Chiang2 and Cheng-Hsien Lu126

1Department of Biological Science National Sun Yat-sen University Kaohsiung Taiwan2Department of Neurology Chang Gung Memorial Hospital Kaohsiung Medical Center Chang Gung University College of MedicineKaohsiung 833 Taiwan3Department of Emergency Medicine Chang Gung Memorial Hospital Kaohsiung Medical Center Chang Gung UniversityCollege of Medicine Kaohsiung 833 Taiwan4Department of Medicine Chang Gung Memorial Hospital Kaohsiung Medical Center Chang Gung University College of MedicineKaohsiung 833 Taiwan5Department of Radiology Chang Gung Memorial Hospital Kaohsiung Medical Center Chang Gung University College of MedicineKaohsiung 833 Taiwan6Department of Neurology Xiamen Chang Gung Memorial Hospital Xiamen Fujian China

Correspondence should be addressed to Cheng-Hsien Lu chlu99ms44urlcomtw

Received 8 January 2015 Accepted 17 May 2015

Academic Editor Jan O Aasly

Copyright copy 2015 Ya-Ting Chang et alThis is an open access article distributed under the Creative Commons Attribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Background Frozen shoulder syndrome is a common musculoskeletal disease of idiopathic Parkinsonrsquos disease (PD) that causeslong-term pain and physical disability A better understanding of the associated factors can help identify PD patients who willrequire prevention to improve their quality of lifeMethodology This prospective study evaluated 60 shoulders of 30 PD patientsCorrelation analysis was used to evaluate the relationships between clinical factors and shoulder sonography findings ResultsFrozen shoulder syndrome was found in 14 of 30 PD patients affecting 19 shoulders including bilateral involvement in fiveand unilateral involvement in nine There was a significant positive correlation between the parameters of sonography findingsand frozen shoulder syndrome (ie thickness of bicipital effusion and tendon thickness of the subscapularis and supraspinatus)and mean ipsilateral Unified Parkinsonrsquos Disease Rating Scale (UPDRS) III and its subscores (tremor rigidity and bradykinesiascores) Conclusions Higher ipsilateral UPDRS and subscores are associated with increased effusion around the biceps tendonwith increased tendon thickness of subscapularis and supraspinatus Preventing frozen shoulder syndrome in the high-risk PDgroup is an important safety issue and highly relevant for their quality of life

1 Introduction

After Alzheimerrsquos disease Parkinsonrsquos disease (PD) is thesecond most common neurodegenerative disorder [1ndash4]Associatedmusculoskeletal conditions seen in as high as 70of PD patients are the most common cause of long-termpain and physical disability [5] Frozen shoulder syndromealso known as adhesive capsulitis is characterized by stiffnessand pain and is associated with increased fluid in the tendonsheath of the long head of the biceps [6] It is one of its

most disabling musculoskeletal problems severely affectingthe quality of life of patients with PD

To date very few clinical researches have focused specif-ically on PD patients with frozen shoulder syndrome [7ndash10] Most of these studies are case reports [11] or ret-rospective studies [7] with less strict selection criteria(eg enrolled in combination with PD and multiple sys-tem atrophy or frozen shoulder and other shoulder dis-turbances) [12 13] or depend solely on clinical diagnosis[14]

Hindawi Publishing CorporationParkinsonrsquos DiseaseVolume 2015 Article ID 232958 7 pageshttpdxdoiorg1011552015232958

2 Parkinsonrsquos Disease

Sonography enables the visualization of the internalstructure of the shoulder tendons and has become an impor-tant diagnostic adjunct in the evaluation of shoulder condi-tions [15 16] Although sonography and magnetic resonanceimaging have comparable high sensitivity and specificity fordiagnosing rotator pathologies [15 16] ultrasonography isnoninvasivemorewidely accessible portable and less expen-sive for assessing soft tissue involvement in musculoskeletaldiseases [17]

Because of its possible benefits an appropriate rehabil-itation program should be routinely recommended withemphasis on regular physical activity to reduce the risk offrozen shoulder syndrome Nonetheless a better delineationof potential prognostic factors in PD patients who shouldreceive preventive intervention is warranted At the sametime it is imperative to obtain accurate information onthe relative frequency and severity of frozen shoulder syn-drome the severity and duration of PD the daily dose ofantiparkinsonian agents and functional outcome Thus thishospital-based study aimed to analyze the clinical featuresimaging findings scientific clinical scores andmeasurementsto determine potential risk factors associated with frozenshoulder syndrome in PD patients

2 Patients and Methods

21 Study Design This single-center prospective case-control study was conducted at Chang Gung MemorialHospital Kaohsiung a tertiary medical center and the mainreferral hospital serving a population of 3million in southernTaiwan

22 Inclusion Criteria This study evaluated 60 shoulders of30 patients with clinical diagnosis of idiopathic Parkinsonrsquosdisease with a good levodopa response [18] who werefollowed up at the Neurology Out-Patient Clinic for morethan six months after titration of their daily antiparkinsonianagents to a steady dose in accordance with their clinicalsymptoms There were 34 patients initially enrolled in thisstudy Four patients including rotator cuff tear in 2 andshoulder joints dislocation in 2 were excluded Finally only30 cases were enrolled in this study Seventeen shoulders ofnine healthy age-matched patients who did not have PDwerestudied as the control group All of the subjects in the controlgroup were asymptomatic for shoulder pathologies and werepain-free

The hospitalrsquos Institutional Review Committees onHuman Research approved the study protocol and all of thepatients or their relatives provided written informed consent

23 Exclusion Criteria Patients with preexisting shoulderpathology or other medical history of stroke rheumatoidarthritis trauma dislocation fracture or surgery or cervicalspine disease were excluded

24 Clinical Assessment An experienced neurology nursespecialist who was blinded to the patientsrsquo clinical andbiochemical data was trained to measure the functional

scores upon enrollment The clinical features recorded wereage at disease onset (or age at the time of the first reportedsymptom attributable to the disease) and disease duration(time from onset until follow-up) The severity of PD wasgraded according to the scores of the Unified ParkinsonrsquosDisease Rating Scale (UPDRS) III and the Hoehn and Yahrstaging [19 20]

The daily dose of antiparkinsonian agents was convertedinto the equivalent dose of levodopa [21] In patients withfluctuating PD the UPDRS III and Hoehn and Yahr scaleswere administered during the ldquooffrdquo situation (8ndash10 hours afterthe patient stopped the usual antiparkinsonian treatment) toevaluate the possible influence of disease severity The Mini-Mental State Examination (MMSE)was used to assess generalintellectual function while cognitive outcomes were assessedusing the Clinical Dementia Rating (CDR) scale All of thesubjects were assigned a CDR rating score as follows 0 for nodementia and 05 1 2 and 3 for questionablemildmoderateand severe dementia respectively

All of the patients underwent 99mTc-TRODAT-1 SPECTCT study according to previously published methods [22]TheHoehn andYahr disability scale andUPDRS IIIwere usedto determine the severity of the disease Both shoulders wereused separately for data analysis

25 Diagnostic Criteria of Adhesive Capsulitis In this studythe diagnostic criteria for adhesive capsulitis were the follow-ing [23] (1) insidious onset of pain associated with passiveglenohumeral motion (2) restricted range of glenohumeralmotion both actively and passively with external rotationlt50 of the normal side and (3) normal radiography anda shoulder ultrasound demonstrating no significant rotatorcuff tear Patients were excluded if they had secondary causesof adhesive capsulitis such as a fracture recent shouldersurgery calcific tendonitis or rotator cuff tears declinedto participate or were younger than 18 years of age Fourpatients were excluded for shoulder dislocation in onerotator cuff tear in two and another shoulder disorder in oneOnly 30 cases were finally included in this study

26 99119898Tc-TRODAT-SPECTCT and Region of InterestAnalysis The participants were intravenously injected with asingle bolus dose of 99mTc-TRODAT-1([2[[2-[[[3-(4-chlo-rophenyl)-8-methyl-8-azabicyclo[321]-oct-2-yl]-methyl](2-mercaptoethyl)amino]ethyl]amino]ethanethiolato(3-)-N2N21015840S2S2]oxo-[1R-(exo-exo)]-99mTc-technetium) Four hoursafter the injection images were obtained using a dual-headSPECTCT equipped with low-energy high-resolutioncollimators (Symbia T Siemens Medical Solutions ErlangenGermany) With the help of anatomic coregistration CTimages the regions of interest (ROIs) of the bilateral striata(including their subregions of caudate and putamen) weredefined on composite images of the six highest striatumactivity slices The occipital cortex was drawn in the sameway and served as background area The radioactivity of theregions of interest was then calculated

Striatal dopamine transporter uptake ratios (TRODATratio) were calculated as the quotient of the mean counts

Parkinsonrsquos Disease 3

per pixel in each striatum divided by the mean counts perpixel in the occipital cortex All images were reviewed byan experienced nuclear physician who was blinded to thepatientsrsquo data

27 Sonographic Examination An experienced neurologistwho was skilled in shoulder sonography examinations andblinded to the patientsrsquo clinical and biochemical data wastrained tomeasure shoulder sonography studies at the time ofenrollment Ultrasonography of the shoulder was performedusing a scanner with a 125MHz linear array transducer(Philips HDI 5000 Philips Medical Systems Bothell WA)During the examination the patient sat on a stool in acomfortable position and the long head of the biceps wasexamined with the patientrsquos hands placed on the ipsilateralknee The subscapularis tendon and biceps tendon grooveswere examined with the patient seated and the arm held inneutral position the elbow flexed to 90∘ and the forearmresting supine on the ipsilateral thigh dynamic with internaland external rotation [24ndash27] The supraspinatus tendon wasevaluated in full internal rotation and hyperextension withthe forearm behind the back and the palm facing posteriorly[24ndash27] The infraspinatus tendon was evaluated with thebent arm placed in front of the patientrsquos own chest while theipsilateral hand was on the contralateral arm [24ndash27]

All of the tendons were examined in transverse andlongitudinal scans and after adjusting the angle of measure-ment the brightest echogenic tendon was obtained Tendonthickness was measured in sonograms at the point of thelargest diameter An increased hypoechoic area (thicknessgt 2mm) around the long head of the biceps tendon in thetransverse view was interpreted as effusion in the biceps ten-don sheath [27] Nonvisualization of the tendon or completefiber discontinuity of the subscapularis supraspinatus andinfraspinatus tendons was interpreted as full thickness tear[25] Partial fiber discontinuity andmixed hypo- and hypere-choic focus in the critical zone of the tendon suggested partialthickness tear [26] Tendonitis was defined as hypoechoicand swelling changes with a difference in tendon thickness(gt2mm) compared to the healthy side [25]

28 Statistical Analyses Datawere expressed asmeanplusmn SDormedian (interquartile range) for continuous variables Thosewith skewed deviation were logarithmically transformed toimprove normality before comparison Two separate statisti-cal analyses were performed First parameters of sonographyfindings among three groups were compared using one-way ANOVA followed by post hoc multiple comparisonComparisons between two groups weremade using indepen-dent 119905-test Second correlation analysis was used to explorethe relationship between parameters of shoulder sonographyfindings and clinical severity in PD patients All statisticalanalyses were conducted using the SPSS software packageversion 12 (SPSS Inc Chicago IL)

3 Results

The 30 patients with idiopathic PD included 14 males (agerange 47ndash78 years mean age 666 years) and 16 females

Table 1 Demographic data of patients with Parkinsonrsquos disease

PD (119899 = 30)Age 6477 plusmn 103Male (119899 ) 14 467Disease duration years 507 plusmn 32Hoehn and Yahr staging 212 plusmn 10Unified Parkinsonrsquos Disease Rating Scale(UPDRS) III 1477 plusmn 84

Tremor score 363 plusmn 36Rigidity score 447 plusmn 31Bradykinesia score 787 plusmn 42

Levodopa equivalent dose (mg) 41148 plusmn 3443Mini-Mental State Examination 2457 plusmn 61Clinical Dementia Rating0 (119899 ) 16 53305 (119899 ) 13 4331 (119899 ) 1 33

Underlying conditionsHypertension (119899 ) 12 400Diabetes mellitus (119899 ) 6 20Knee osteoarthritis 4 13

Values are expressed in mean plusmn SD unless otherwise indicated

(age range 47ndash81 years mean age 632 years) (Table 1)Frozen shoulder syndrome was found in 19 shoulders of 14patients including bilateral involvement in five and unilateralinvolvement in nine Furthermore the mean age betweenpatients with and without frozen shoulder was 649 plusmn 109and 647 plusmn 102 respectively (119901 = 0965) and the meaneducational levels between patients with and without frozenshoulder were 64plusmn31 and 46plusmn32 respectively (119901 = 0130)

The underlying diseases of the 30 patients includedhypertension in 12 diabetes mellitus (DM) in six and kneeosteoarthritis in four (Table 1) Their percentage of cognitiveimpairment was 466 including CDR 05 in 13 and CDR 1in one By theHoehn and Yahr staging 11 were of stage I ninewere of stage II eight were of stage III and two were of stageIV Their mean UPDRS III score was 2773 plusmn 139 (range 5ndash62)

The mean thickness of the tendon in the 19 shoulderswith adhesive capsulitis was as follows subscapularis 510 plusmn12mm supraspinatus 545plusmn12mm and infraspinatus 552plusmn13mmThemean thickness of the bicipital effusion in the 19frozen shoulders was 272plusmn05mmThe ipsilateral UPDRS ofPD patients with and without frozen shoulder syndrome was1700 plusmn 71 and 1407 plusmn 88 (119901 = 0210) respectively whiletheir other ipsilateral motor severities were listed in Table 2Patientswith frozen shoulder had ameanMMSEof 2543plusmn33points whereas patients without frozen shoulder had a meanMMSE of 2381 plusmn 77 points

Correlation analysis was used to test the influence ofMMSE and ipsilateral motor state (ipsilateral UPDRS IIIipsilateral tremor score ipsilateral rigidity score and ipsi-lateral bradykinesia score) on mean effusion around thebiceps tendon The significant statistical results (correlation


Table 2 Clinical data and shoulder sonography findings among healthy controls andPDpatientswith andwithout frozen shoulder syndrome

Control (119873 = 17) PD (119873 = 30)119901 value

With frozen shoulder (119899 = 41) Without frozen shoulder (119899 = 19)Age 6371 plusmn 96 6477 plusmn 103Sex (malefemale) 611 1416Tendon thickness (mm)

Subscapularis 438 plusmn 10 495 plusmn 11 510 plusmn 12 0630a

Supraspinatus 442 plusmn 10 506 plusmn 11 545 plusmn 13 0184a

Infraspinatus 358 plusmn 06 380 plusmn 07 324 plusmn 04 lt0001a

Thickness of bicipital effusion (mm) 139 plusmn 03 208 plusmn 08 272 plusmn 05 0002a

Ipsilateral motorIpsilateral UPDRS III 1407 plusmn 88 1700 plusmn 71 0210b

Ipsilateral tremor score (median [IQR]) 1 (0 2) 2 (05 35) 0065b

Ipsilateral rigidity score 198 plusmn 17 279 plusmn 16 0083b

Ipsilateral bradykinesia score 373 plusmn 24 437 plusmn 21 0333b

Contralateral TRODAT ratio 149 plusmn 01 128 plusmn 01 lt0001b

Values are expressed in mean plusmn SD unless otherwise indicatedaStatistical comparison by ANOVAbStatistical comparison by independent 119905-testPD Parkinsonrsquos disease IQR interquartile range MMSE Mini-Mental State Examination UPDRS Unified Parkinsonrsquos Disease Rating Scale

coefficient p value) revealed a mean MMSE score (119903 =minus0341 119901 = 0035) mean ipsilateral UPDRS III score (119903 =0618 119901 lt 0001) mean ipsilateral tremor score (119903 = 0521119901 lt 0001) mean ipsilateral rigidity score (119903 = 0574119901 lt 0001) and mean ipsilateral bradykinesia score (119903 =0613 119901 lt 0001)

Furthermore themean ipsilateral UPDRS III scoremeanipsilateral tremor score mean ipsilateral rigidity score andmean ipsilateral bradykinesia score were positively correlatedwith the thickness of the subscapularis tendon (average) (119903 =0386 119901 = 0003 119903 = 0465 119901 lt 0001 119903 = 0281 119901 = 0031and 119903 = 0399 119901 = 0002 resp) while the mean ipsilateralUPDRS III score (119903 = 0421 119901 = 0001) mean ipsilateraltremor score (119903 = 0341 119901 = 0004) and mean ipsilateralbradykinesia score (119903 = 0385 119901 = 0001) were positivelycorrelated with the thickness of the supraspinatus tendon(average) (Table 3)

4 Discussion

Differences in the relative prevalence of frozen shouldersyndrome in patients with idiopathic PD vary with casedetermination and inclusion criteria disease severity lengthof follow-up underlying diseases and diagnostic methodsThe frequency of frozen shoulder syndrome in PD patientsin other studies varies and is estimated to be as high as 226in one study [7] In the present study the frequency is 467(14 out of 30)

The present study examines risk factors associated withfrozen shoulder syndrome in 30 patients with idiopathic PDand has two major findings First both the mean thicknessof the subscapularis tendon and the supraspinatus andinfraspinatus muscles and the thickness of bicipital effusionin the shoulders are largest in the frozen shoulders of PD

patients followed by the nonfrozen shoulders of PD patientsand the shoulders of healthy controls Second both the meanthickness of the subscapularis and supraspinatus tendons andthe thickness of bicipital effusion in the shoulders positivelycorrelated with the mean ipsilateral UPDRS III and itssubscores (ie tremor rigidity and bradykinesia scores)

Frozen shoulder syndrome also known as adhesive cap-sulitis is the spontaneous onset of painful and progressivelysevere restriction of shoulder joint mobility in the absence ofany demonstrable intrinsic joint abnormality [28] Althoughthere are no specific ultrasound findings findings associatedwith frozen shoulder syndrome may be correlated withincreased fluid in the tendon sheath of the long head ofthe biceps [6] Two reports have mentioned an associationbetween chronic tendinopathy and the increase in thicknessof the rotator cuff through indirect or direct measurements[24 29] Regarding the sonography findings there is asignificantly thicker bicipital effusion in PD patients withasymptomatic shoulders than in the shoulders of the controlsFurthermore bicipital effusion is significantly thicker in PDpatients with symptomatic shoulders than in those withasymptomatic shoulders

A thicker mean bicipital effusion is observed in patientswith significantly higher mean ipsilateral UPDRS III andits subscores for tremor rigidity and bradykinesia (scoresindicated in advanced PD) This study also demonstrates theeffects of ipsilateral UPDRS III and its subscores on the thick-ness of the supraspinatus and subscapularis tendons and thesignificantly higher tendon thickness of both the supraspina-tus and the subscapularis in asymptomatic PD shoulderscompared to those of the controls The supraspinatus tendonis considered to be the most commonly affected site bydegeneration and among rotator cuff age-related increases inthickness [24] The present study demonstrates that not onlythe supraspinatus tendon but also the subscapularis tendon


Table 3 Correlation between parameters of shoulder sonography findings and clinical severity in PD patients

Variable Thickness ofbicipital effusion

Subscapularisthickness

Supraspinatusthickness

Infraspinatusthickness

Age years 0175 0138 0254 minus0057Body mass index kgm2 0124 0115 0145 minus0094Disease duration years 0105 0143 0166 minus0102Mini-Mental State Examination minus0341lowast minus0123 minus0028 0030Striatal dopamine transporter uptake ratios

Contralateral TRODAT ratio minus0319 minus0081 minus0367lowast 0122Ipsilateral TRODAT ratio 0030 0139 minus0100 0105

Levodopa equivalent dose (mg) 0027 minus0139 minus0003 minus0092Hoehn and Yahr staging 0321lowast 0162 0055 0289lowast

Clinical motor stateIpsilateral motor stateIpsilateral UPDRS III 0618lowastlowast 0386lowast 0421lowastlowast 0110Ipsilateral tremor score 0521lowastlowast 0456lowastlowast 0341lowast minus0073Ipsilateral rigidity score 0574lowastlowast 0277lowast 0207 minus0132Ipsilateral bradykinesia score 0613lowastlowast 0400lowast 0385lowast 0135

Contralateral motor stateContralateral UPDRS III 0255 0089 0225 0066Contralateral tremor score 0095 0140 0164 0120Contralateral rigidity score 0222 0022 0035 0047Contralateral bradykinesia score 0169 0044 0174 0011

Values indicate correlation coefficientlowast119901 lt 005 lowastlowast119901 lt 001

PD Parkinsonrsquos disease UPDRS Unified Parkinsonrsquos Disease Rating Scale

has changes associated with the clinical severity of PD whichis represented by ipsilateral UPDRS III and its subscores

One study indicates that the supraspinatus and subscapu-laris tendons are especially commonly affected and cause ananterosuperior subluxation of the shoulder joint in patientswith PD [30] Another study shows positive correlationsbetween supraspinatus tendon tear and ipsilateral tremor andrigidity scores [9] Consistent with such findings results ofthe present study also reveal a positive correlation betweenthe thickness of the supraspinatus tendon and ipsilateralUPDRS III and its subscores for tremor rigidity and bradyki-nesia The mean infraspinatus tendon thickness is the onlyparameter that does not show any significant correlationwith clinical motor scores because the thickness of theinfraspinatus tendon is relatively difficult to measure due tothe lack of anatomic landmarks

Several articles report risk factors for frozen shoulder syn-drome including prolonged illness rigidity immobilizationand akinesia [7 8 31] One study demonstrates that akinesiais common as a first manifestation and is correlated with thelaterality of the frozen shoulder [7] Another study demon-strates that rigidity and bradykinesia in PD patients are sup-posed to lead to limited joint range of motion and predisposethe patient to developing frozen shoulder syndrome [7 31]The present study demonstrated the relationship betweenclinical severity and thickness of bicipital effusion Patientswith lower mean MMSE score which may imply cognitive

decline have thicker bicipital effusion Several important riskfactors for frozen shoulders (eg age sex occupation diseaseduration and PD phenotypes) should be further discussedIn the present study lower educational level and diseaseduration were found in patients without frozen shoulderHowever the difference is not significant within our patientsOur study is limited to small patientsrsquo number and patientswith lower educational level and thus the occupation and PDphenotypes difference were not studied in the present study

Although this study demonstrates that the mean ipsilat-eral tremor score in UPDRS III is independently associatedwith frozen shoulder syndrome in patients with idiopathicPD it has several limitations First PD is a slowly progressiveneurodegenerative disorder Hence it is not possible to assessthe effects of disease progression on the duration and severityof frozen shoulder in a cross-sectional study Second as aprospective observation study it may be subject to bias ofunmeasured factors The frozen shoulders of some patientsmay be related to accidents or immobilization Furthermoreunderlying cognitive decline may cause potential frozenshoulder during follow-up Third PD patients with frozenshoulder syndrome associated with rotator cuff tear havebeen excluded and this may be subject to bias in statisticalanalysis Lastly the case numbers are small Large-scaleprospective studies to clarify the relationship are warranted

Considering the morbidity and mortality associatedwith frozen shoulder syndrome prevention and evaluation


of shoulder through sonography should be considered inhigh-risk patients with PD especially in those with higherUPDRS III These are important issues for patient safety andare highly relevant for improving their quality of life

Ethical Approval

The study was approved by Chang GungMemorial HospitalrsquosInstitutional Review Committee on Human Research

Conflict of Interests

The authors indicate no potential conflict of interests regard-ing the publication of this paper

Acknowledgments

This study was supported by grants from NHRI-EX101-10142EIThe authors wish to thankDr Gene AlzonaNisperosfor editing and reviewing the paper for English languageconsiderations

References

[1] A D Woolf ldquoHow to assess musculoskeletal conditionsHistory and physical examinationrdquo Best Practice amp ResearchClinical Rheumatology vol 17 no 3 pp 381ndash402 2003

[2] S Fahn ldquoDescription of Parkinsonrsquos disease as a clinical syn-dromerdquo Annals of the New York Academy of Sciences vol 991pp 1ndash14 2003

[3] L M de Lau and M M Breteler ldquoEpidemiology of ParkinsonrsquosdiseaserdquoThe Lancet Neurology vol 5 no 6 pp 525ndash535 2006

[4] R Ashour and J Jankovic ldquoJoint and skeletal deformities inParkinsonrsquos disease multiple system atrophy and progressivesupranuclear palsyrdquo Movement Disorders vol 21 no 11 pp1856ndash1863 2006

[5] A G Beiske J H Loge A Roslashnningen and E Svensson ldquoPainin Parkinsonrsquos disease prevalence and characteristicsrdquo Pain vol141 no 1-2 pp 173ndash177 2009

[6] S Bianchi and C Martinoli Ultrasound of the MusculoskeletalSystem Medical Radiology Springer 2007

[7] D Riley A E Lang R D G Blair A Birnbaum and BReid ldquoFrozen shoulder and other shoulder disturbances inParkinsonrsquos diseaserdquo Journal of Neurology Neurosurgery andPsychiatry vol 52 no 1 pp 63ndash66 1989

[8] Y E Kim and B S Jeon ldquoMusculoskeletal problems in Parkin-sonrsquos diseaserdquo Journal of Neural Transmission vol 120 no 4 pp537ndash542 2013

[9] A Yucel and O Y Kusbeci ldquoMagnetic resonance imaging find-ings of shoulders in Parkinsonrsquos diseaserdquo Movement Disordersvol 25 no 15 pp 2524ndash2530 2010

[10] M Rafii H Firooznia O Sherman et al ldquoRotator cuff lesionssignal patterns at MR imagingrdquo Radiology vol 177 no 3 pp817ndash823 1990

[11] R H C Bisschops C J M Klijn L J Kappelle A Cvan Huffelen and J van der Grond ldquoCollateral flow andischemic brain lesions in patients with unilateral carotid arteryocclusionrdquo Neurology vol 60 no 9 pp 1435ndash1441 2003

[12] C JM Klijn L J Kappelle A C vanHuffelen et al ldquoRecurrentischemia in symptomatic carotid occlusion prognostic value of

hemodynamic factorsrdquoNeurology vol 55 no 12 pp 1806ndash18122000

[13] R L Grubb Jr C PDerdeyn SM Fritsch et al ldquoImportance ofhemodynamic factors in the prognosis of symptomatic carotidocclusionrdquo Journal of the American Medical Association vol280 no 12 pp 1055ndash1060 1998

[14] M J Burke M D I Vergouwen J Fang et al ldquoShort-termoutcomes after symptomatic internal carotid artery occlusionrdquoStroke vol 42 no 9 pp 2419ndash2424 2011

[15] WGrassi E Filippucci A Farina andCCervini ldquoSonographicimaging of tendonsrdquo Arthritis amp Rheumatism vol 43 no 5 pp969ndash976 2000

[16] W Grassi E Filippucci and P Busilacchi ldquoMusculoskeletalultrasoundrdquo Best Practice and Research Clinical Rheumatologyvol 18 no 6 pp 813ndash826 2004

[17] M Zanetti and J Hodler ldquoImaging of degenerative andposttraumatic disease in the shoulder joint with ultrasoundrdquoEuropean Journal of Radiology vol 35 no 2 pp 119ndash125 2000

[18] A J Hughes S E Daniel L Kilford and A J Lees ldquoAccuracyof clinical diagnosis of idiopathic Parkinsonrsquos disease a clinico-pathological study of 100 casesrdquo Journal of Neurology Neuro-surgery and Psychiatry vol 55 no 3 pp 181ndash184 1992

[19] P Martinez-Martin A Gil-Nagel L M Gracia J B Gomez JMartınez-Sarries and F Bermejo ldquoUnified Parkinsonrsquos DiseaseRating Scale characteristics and structure The CooperativeMulticentric GrouprdquoMovement Disorders vol 9 no 1 pp 76ndash83 1994

[20] M M Hoehn and M D Yahr ldquoParkinsonism onset progres-sion and mortalityrdquo Neurology vol 17 no 5 pp 427ndash442 1967

[21] P Krack P Pollak P Limousin et al ldquoSubthalamic nucleus orinternal pallidal stimulation in young onset Parkinsonrsquos diseaserdquoBrain vol 121 no 3 pp 451ndash457 1998

[22] Y H Weng T C Yen M C Chen et al ldquoSensitivity andspecificity of 99mTc-TRODAT-1 SPECT imaging in differenti-ating patients with idiopathic Parkinsonrsquos disease from healthysubjectsrdquo Journal of NuclearMedicine vol 45 no 3 pp 393ndash4012004

[23] K Wang V Ho D J Hunter-Smith P S Beh K M Smith andA B Weber ldquoRisk factors in idiopathic adhesive capsulitis acase control studyrdquo Journal of Shoulder and Elbow Surgery vol22 no 7 pp e24ndashe29 2013

[24] T-Y Yu W-C Tsai J-W Cheng Y-M Yang F-C Liang andC-H Chen ldquoThe effects of aging on quantitative sonographicfeatures of rotator cuff tendonsrdquo Journal of Clinical Ultrasoundvol 40 no 8 pp 471ndash478 2012

[25] Y-P Pong L-Y Wang Y-C Huang C-P Leong M-Y Liawand H-Y Chen ldquoSonography and physical findings in strokepatients with hemiplegic shoulders a longitudinal studyrdquo Jour-nal of Rehabilitation Medicine vol 44 no 7 pp 553ndash557 2012

[26] T Wallny U A Wagner S Prange O Schmitt and H ReichldquoEvaluation of chronic tears of the rotator cuff by ultrasoundA new indexrdquo The Journal of Bone amp Joint SurgerymdashBritishVolume vol 81 no 4 pp 675ndash678 1999

[27] E Naredo P Aguado E De Miguel et al ldquoPainful shouldercomparison of physical examination and ultrasonographicfindingsrdquo Annals of the Rheumatic Diseases vol 61 no 2 pp132ndash136 2002

[28] B Reeves ldquoThe natural history of the frozen shoulder syn-dromerdquo Scandinavian Journal of Rheumatology vol 4 no 4 pp193ndash196 1975


[29] C Milgrom M Schaffler S Gilbert and M Van HolsbeeckldquoRotator-cuff changes in asymptomatic adultsThe effect of agehand dominance and genderrdquo The Journal of Bone and JointSurgerymdashBritish Volume vol 77 no 2 pp 296ndash298 1995

[30] T Matsuzaki T Kokubu I Nagura et al ldquoAnterosuperiordislocation of the shoulder joint in an older patient withParkinsonrsquos diseaserdquo Kobe Journal of Medical Sciences vol 54no 5 pp E237ndashE240 2008

[31] S-B Koh J-H Roh J H Kim et al ldquoUltrasonographic findingsof shoulder disorders in patients with Parkinsonrsquos diseaserdquoMovement Disorders vol 23 no 12 pp 1772ndash1776 2008

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014


MEDIATORSINFLAMMATION

of


Behavioural Neurology

EndocrinologyInternational Journal of



Disease Markers


BioMed Research International

OncologyJournal of



Oxidative Medicine and Cellular Longevity


PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of



Computational and Mathematical Methods in Medicine

OphthalmologyJournal of


Diabetes ResearchJournal of



Research and TreatmentAIDS


Gastroenterology Research and Practice


Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom


Sonography enables the visualization of the internalstructure of the shoulder tendons and has become an impor-tant diagnostic adjunct in the evaluation of shoulder condi-tions [15 16] Although sonography and magnetic resonanceimaging have comparable high sensitivity and specificity fordiagnosing rotator pathologies [15 16] ultrasonography isnoninvasivemorewidely accessible portable and less expen-sive for assessing soft tissue involvement in musculoskeletaldiseases [17]

Because of its possible benefits an appropriate rehabil-itation program should be routinely recommended withemphasis on regular physical activity to reduce the risk offrozen shoulder syndrome Nonetheless a better delineationof potential prognostic factors in PD patients who shouldreceive preventive intervention is warranted At the sametime it is imperative to obtain accurate information onthe relative frequency and severity of frozen shoulder syn-drome the severity and duration of PD the daily dose ofantiparkinsonian agents and functional outcome Thus thishospital-based study aimed to analyze the clinical featuresimaging findings scientific clinical scores andmeasurementsto determine potential risk factors associated with frozenshoulder syndrome in PD patients

2 Patients and Methods

21 Study Design This single-center prospective case-control study was conducted at Chang Gung MemorialHospital Kaohsiung a tertiary medical center and the mainreferral hospital serving a population of 3million in southernTaiwan

22 Inclusion Criteria This study evaluated 60 shoulders of30 patients with clinical diagnosis of idiopathic Parkinsonrsquosdisease with a good levodopa response [18] who werefollowed up at the Neurology Out-Patient Clinic for morethan six months after titration of their daily antiparkinsonianagents to a steady dose in accordance with their clinicalsymptoms There were 34 patients initially enrolled in thisstudy Four patients including rotator cuff tear in 2 andshoulder joints dislocation in 2 were excluded Finally only30 cases were enrolled in this study Seventeen shoulders ofnine healthy age-matched patients who did not have PDwerestudied as the control group All of the subjects in the controlgroup were asymptomatic for shoulder pathologies and werepain-free

The hospitalrsquos Institutional Review Committees onHuman Research approved the study protocol and all of thepatients or their relatives provided written informed consent

23 Exclusion Criteria Patients with preexisting shoulderpathology or other medical history of stroke rheumatoidarthritis trauma dislocation fracture or surgery or cervicalspine disease were excluded

24 Clinical Assessment An experienced neurology nursespecialist who was blinded to the patientsrsquo clinical andbiochemical data was trained to measure the functional

scores upon enrollment The clinical features recorded wereage at disease onset (or age at the time of the first reportedsymptom attributable to the disease) and disease duration(time from onset until follow-up) The severity of PD wasgraded according to the scores of the Unified ParkinsonrsquosDisease Rating Scale (UPDRS) III and the Hoehn and Yahrstaging [19 20]

The daily dose of antiparkinsonian agents was convertedinto the equivalent dose of levodopa [21] In patients withfluctuating PD the UPDRS III and Hoehn and Yahr scaleswere administered during the ldquooffrdquo situation (8ndash10 hours afterthe patient stopped the usual antiparkinsonian treatment) toevaluate the possible influence of disease severity The Mini-Mental State Examination (MMSE)was used to assess generalintellectual function while cognitive outcomes were assessedusing the Clinical Dementia Rating (CDR) scale All of thesubjects were assigned a CDR rating score as follows 0 for nodementia and 05 1 2 and 3 for questionablemildmoderateand severe dementia respectively

All of the patients underwent 99mTc-TRODAT-1 SPECTCT study according to previously published methods [22]TheHoehn andYahr disability scale andUPDRS IIIwere usedto determine the severity of the disease Both shoulders wereused separately for data analysis

25 Diagnostic Criteria of Adhesive Capsulitis In this studythe diagnostic criteria for adhesive capsulitis were the follow-ing [23] (1) insidious onset of pain associated with passiveglenohumeral motion (2) restricted range of glenohumeralmotion both actively and passively with external rotationlt50 of the normal side and (3) normal radiography anda shoulder ultrasound demonstrating no significant rotatorcuff tear Patients were excluded if they had secondary causesof adhesive capsulitis such as a fracture recent shouldersurgery calcific tendonitis or rotator cuff tears declinedto participate or were younger than 18 years of age Fourpatients were excluded for shoulder dislocation in onerotator cuff tear in two and another shoulder disorder in oneOnly 30 cases were finally included in this study

26 99119898Tc-TRODAT-SPECTCT and Region of InterestAnalysis The participants were intravenously injected with asingle bolus dose of 99mTc-TRODAT-1([2[[2-[[[3-(4-chlo-rophenyl)-8-methyl-8-azabicyclo[321]-oct-2-yl]-methyl](2-mercaptoethyl)amino]ethyl]amino]ethanethiolato(3-)-N2N21015840S2S2]oxo-[1R-(exo-exo)]-99mTc-technetium) Four hoursafter the injection images were obtained using a dual-headSPECTCT equipped with low-energy high-resolutioncollimators (Symbia T Siemens Medical Solutions ErlangenGermany) With the help of anatomic coregistration CTimages the regions of interest (ROIs) of the bilateral striata(including their subregions of caudate and putamen) weredefined on composite images of the six highest striatumactivity slices The occipital cortex was drawn in the sameway and served as background area The radioactivity of theregions of interest was then calculated

Striatal dopamine transporter uptake ratios (TRODATratio) were calculated as the quotient of the mean counts






3 Results














Control (119873 = 17) PD (119873 = 30)119901 value














4 Discussion



























Ethical Approval




Acknowledgments


References







































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of





















3 Results














Control (119873 = 17) PD (119873 = 30)119901 value














4 Discussion



























Ethical Approval




Acknowledgments


References







































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of


















Control (119873 = 17) PD (119873 = 30)119901 value














4 Discussion



























Ethical Approval




Acknowledgments


References







































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of





































Ethical Approval




Acknowledgments


References







































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of


















Ethical Approval




Acknowledgments


References







































of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of

























of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of





















of






Disease Markers



OncologyJournal of





PPAR Research



Journal of

ObesityJournal of
















Documents

Clinical Study Clinical Features Associated with Frozen