Neurourology and Urodynamics

Receiver Operating Characteristic Analysis of SphincterElectromyography for Parkinsonian Syndrome

Tatsuya Yamamoto,1* Ryuji Sakakibara,1,5 Tomoyuki Uchiyama,1 Chiharu Yamaguchi,3 Fumio Nomura,3

Takashi Ito,1 Mitsuru Yanagisawa,2 Masashi Yano,2 Yusuke Awa,2 Tomonori Yamanishi,4

Takamichi Hattori,1 and Satoshi Kuwabara11Department of Neurology, Graduate School of Medicine, Chiba University, Chiba, Japan2Department of Urology, Graduate School of Medicine Chiba University, Chiba, Japan

3Department of Molecular Diagnosis, Graduate School of Medicine, Chiba University, Chiba, Japan4Department of Urology, Dokkyo Medical College, Tochigi, Japan

5Neurology Division, Department of Internal Medicine, Sakura Medical Center, Toho University, Sakura, Japan

Aims: We performed receiver operating characteristic (ROC) analysis to determine the ability of sphincter electromy-ography (EMG) to distinguish multiple system atrophy (MSA) from other parkinsonisms. The following was deter-mined: (1) the appropriate motor unit potential (MUP) parameter among duration, phase, and amplitude; (2) thedesirable parameter of our duration criteria; that is, more than 20% MUPs having >10 ms duration (criteria a) ormean duration >10 ms (criteria b). Methods: We retrospectively reviewed 441 case records where sphincter EMGwere performed in patients with parkinsonian syndromes: MSA, n ¼ 263; Parkinson’s disease, n ¼ 129; dementia withLewy bodies, n ¼ 25; and progressive supranuclear palsy, n ¼ 24. We performed ROC analysis of the data sets.Results: The area under the curve used to differentiate MSA from other parkinsonian syndromes was 0.68 in dura-tion, 0.57 in phase, and 0.51 in amplitude, respectively; these values were statistically significant. With regard to ourduration criteria, area under the curve was 0.69 for the average duration of MUPs (criteria b) and 0.67 for percentageof MUPs of duration >10 ms (criteria a); these values were also statistically significant. Conclusions: This studysuggests that duration is appropriate parameter for the differentiation of MSA. However, the area under the curve ofthe mean duration was insufficient to confirm the diagnosis; sphincter EMG should be used as a supportive diagnostictool for the diagnosis of MSA. Neurourol. Urodynam. � 2012 Wiley Periodicals, Inc.

Key words: external anal sphincter electromyography; multiple system atrophy; receiver operating characteristicanalysis; parkinsonian syndrome

INTRODUCTION

External anal sphincter electromyography (EAS-EMG) is anestablished method to detect neurogenic change of thesphincter muscle.1 Neurogenic change detected by EAS-EMGsuggests either neuropathic change in the pudendal nerve,which innervates the EAS muscle,2 or Onuf’s nucleus involve-ment. Neurodegeneration of Onuf’s nucleus is common inmultiple system atrophy (MSA).3,4

However, neurogenic change in EAS-EMG was reported infew subjects with other parkinsonian syndromes, for example,Parkinson’s disease (PD),5 progressive supranuclear palsy(PSP),6 dementia with Lewy bodies (DLB),7 and Machado–Jo-seph disease.8 Although EAS-EMG is commonly performed todiagnose MSA,9 its ability in differentiating MSA from otherparkinsonian syndromes, which is often difficult in earlystages,10 remains unconfirmed.

Diagnostic criteria defining ‘‘neurogenic change’’ in EAS-EMG are controversial.9 EAS-EMG usually analyses quantita-tive motor unit potentials (MUPs), including their amplitude,duration, and number of phases.11 Duration is frequently usedin detecting neurogenic change in EAS-EMG11; however, crite-ria differ between laboratories, and optimal criteria are notdefined. We adopted the criteria12 that states ‘‘>20% of MUPshave a duration >10 ms’’ or ‘‘the mean duration of MUPs>10 ms, particularly including the late components.’’

This study aims to determine the appropriate MUP parame-ter to differentiate MSA from other parkinsonian syndromes,

particularly PD, using receiver operating characteristic (ROC)analysis, and to determine the desirable criteria.

MATERIALS AND METHODS

Patients

We retrospectively reviewed 445 patients with parkinso-nian syndromes referred to our hospital (Chiba University) forfurther confirmation of diagnosis. Patient statistics were asfollows: MSA, n ¼ 263 [mean age 64 years (range 47–82),male n ¼ 154, female n ¼ 109]; PD, n ¼ 129 [mean age66 years (range 43–85), male n ¼ 86, female n ¼ 43]; DLB,n ¼ 25 [mean age 73 years (range 61–84), male n ¼ 12, femalen ¼ 13]; and PSP, n ¼ 24 [mean age 72 years (range 53–79),male n ¼ 20, female n ¼ 4]. The mean disease duration of PDand MSA was 3.2 years; the rest varied between 3 and 5 years.

Dirk De Ridder led the review process.Conflict of interest: none.These authors contributed equally to this study.*Correspondence to: Tatsuya Yamamoto, M.D., Ph.D., 1-8-1 Inohana Chuo-ku,Chiba 260-8670, Japan. E-mail: tatsuya-yamamoto@mbc.nifty.comReceived 1 November 2011; Accepted 11 January 2012Published online in Wiley Online Library

(wileyonlinelibrary.com).

DOI 10.1002/nau.22208

� 2012 Wiley Periodicals, Inc.

All patients with PD met the clinical diagnostic criteria ofidiopathic PD and responded well to treatment with levodo-pa.13 All patients with MSA satisfied the second consensuscriteria for the diagnosis of possible or probable MSA.14 Allpatients with DLB met the consensus guidelines for the clini-cal diagnosis of probable or possible DLB.15 Some patientswith PSP (also called Steele–Richardson–Olszewski syndrome)met the clinical criteria given by the National Institute of Neu-rological Disorders and Stroke, and Society for PSP, Inc16; theremaining were diagnosed as having PSP-parkinsonism.17 Thepatients with the past history of anal or perineal surgery(such as hemorrhoidectomy) were excluded from this study.The patients with the past history of other pelvic floor prob-lems, such as vaginal childbirth with or without episiotomyanal fissures, lumbosacral radiculopathies, and direct localtrauma from falls were also excluded from this study. In-formed consent was obtained from all participants. The ethicscommittee of Chiba University School of Medicine reviewedthe protocol.

Methods

We performed standard EMG cystometry with pressureflow studies and single MUP analysis using an EMG computer(Neuropack Sigma MEB5504; Nihon Kohden, Tokyo, Japan).EAS-EMG was performed by one of our authors (C.Y.) who istechnical staff in performing urodynamic studies and EAS-EMG. A disposable concentric needle electrode (needle diame-ter 0.46 mm; Alpine Biomed, Skovlunde, Denmark) wasinserted into the most superficial layer of the anal sphinctermuscle under audio guidance. The needle was inserted intothe right (5 O’clock position) and the left (7 O’clock position)sphincter muscle and MUP analysis was performed separate-ly. Five MUPs were recorded in each side. The position of theneedle electrode was usually adjusted until continuous firingactivities of 3–5 MUPs were visually observed. The rise time ofthe MUP was 300–500 ms. The range of sites from which MUPwas recorded was about 1 cm from the anal orifice, to a depthof 3–6 mm. A gain of 100 mV and 5 ms/div was used. Theamplifier filter was set at 5–10 kHz.

The MUPs were stored into the input buffer of the computerwhen the amplitude reached the threshold determined by theexaminer. After visually confirmed 3–5 MUPs were continu-ously firing, the examiner manually set the threshold by mov-ing the cursor to detect visually confirmed 3–5 MUPs andthen a total of 64 MUPs were stored into the input buffer ofthe computer. The stored 64 MUPs were classified into thefour most similar MUPs by ‘‘Auto MUP Analysis software’’equipped with the EMG computer. The ‘‘Auto MUP Analysissoftware’’ identified the ‘‘four most similar MUPs’’ by follow-ing procedures. The stored 64 MUPs were numbered, such asMUP1, MUP2,. . .,MUP64. The Auto MUP Analysis software ini-tially registered MUP1 as template wave and calculated thecorrelational coefficient between MUP1 and MUP2. If the cor-relational coefficient exceeded 0.94, the software regardedthat MUP2 was identical to MUP1. Otherwise, MUP2 wasregarded as different wave from MUP1. The software repeatedthis procedure to the rest of the MUPs and finally identifiedthe four most similar MUPs. Our automated system couldidentify up to four MUPs which were visually confirmed. Theonset of the MUP was automatically determined when boththe slope and the voltage exceeded the predefined threshold(onset slope: 5 mV/ms, onset level: 20 mV above or below thebaseline voltage in this study). The termination was also de-termined by the same procedure. As a result, the duration wasautomatically determined. Since, this program cannot identify

‘‘late components (separate satellite potentials),’’ the examin-er checked the wave form and manually set the cursor to in-clude ‘‘late component.’’ Late components were included inthis ‘‘total MUP duration.’’We repeated above procedures to obtain 10 different MUPs

by moving the position of the electrode. The EMG computercalculated the mean duration, number of phases, and theamplitude of the 10 obtained different MUPs.Neurogenic change was diagnosed according to our dura-

tion criteria on observing at least one of the followingabnormalities:

(a) More than 20% of MUPs have a duration >10 ms.(b) The mean duration of MUPs >10 ms, particularly includ-

ing the late components.

The method of performing EAS-EMG and the diagnosticcriteria of neurogenic change in EAS-EMG was concurrentwith previous study.12,18 All of the EMG recordings were per-formed only in Chiba University and all of the results in thisstudy were examined under the same criteria. All of ourauthors have experience of working in Chiba Universityand therefore all authors understand our duration criteriacompletely.

Statistical Analysis

Means and SDs of the MUP parameters; that is, duration,phase, and amplitude were calculated for each disease. Analy-sis of variance (ANOVA) tests were performed to compare thedifference between each parameter among patients withparkinsonian syndrome. The Mann–Whitney U-test was per-formed to compare the difference between each parameter forpatients with MSA and PD.We performed ROC analysis to determine the appropriate

MUP parameter from duration, phase, and amplitude for thedifferentiation of MSA from other parkinsonian syndromes,especially PD, and to determine the desirable parameter of ourduration criteria; that is, mean duration of MUPs >10 ms ormore than 20% of MUPs with duration >10 ms.A detailed ROC analysis was performed as follows. We first

generated ROC curves by calculating the sensitivity and speci-ficity of each MUP parameter, followed by plotting specificityagainst sensitivity by varying the threshold value. We auto-matically performed ROC analysis on a PC with Windows 7operating system using ROCKIT version 0.9.1 beta andPLOTROC version 1.0.0, which were developed at the Depart-ment of Radiology, University of Chicago (http://www-radiology.uchicago.edu/krl/index.htm).

RESULTS

MUP parameters such as duration, phase, and amplitudewere measured for each case of parkinsonian syndrome.ANOVA analysis showed significant differences in mean dura-tion (P < 0.001), mean number of MUPs >10 ms (P < 0.001),and mean number of phases (P < 0.001) for each case of par-kinsonian syndrome (Table I). Furthermore, these parameterswere significantly higher in MSA than in PD (P < 0.01;Table I).We identified 203 patients with neurogenic changes in

EAS-EMG using our duration criteria. Among these, positivecriteria (a) were noted in 203 patients, whereas positivecriteria (b) were noted in 102 patients. All patients satisfyingcriteria (b) also satisfied criteria (a) except for one patient withDLB. The distributions of the mean duration of MUPs for each

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Neurourology and Urodynamics DOI 10.1002/nau

disease are presented in Figure 1. Duration of MUP longerthan 14.2 ms was only detected in patients with MSA.

The sensitivity and specificity of our duration criteria indifferentiating MSA from other parkinsonian syndromes anddifferentiating from PD is demonstrated in Table II.

Area under ROC curves (AUC) for MSA versus parkinsoniansyndrome and for MSA versus PD are depicted in Figure 2aand b, respectively. The AUC in duration was significantly thehighest amongst the three parameters for MSA and parkinso-nian syndrome (P < 0.01) and for MSA and PD (P < 0.01;Fig. 2c).

Taking our duration criteria into account, AUC for MSAversus parkinsonian syndrome and for MSA versus PD aredepicted in Figure 3a and b, respectively. The AUC in criteria(b) was significantly higher than in criteria (a) (Fig. 3c).

DISCUSSION

EAS-EMG analysis is thought to be useful to identify MSAbecause the degeneration of Onuf’s nucleus is a pathologicalhallmark of MSA.4,19 However, the criteria for the detection ofneurogenic changes in EAS-EMG differ among neurophysiolo-gy laboratories.11 This poses as a problem for neurologists indistinguishing MSA from other parkinsonian syndromes. Wewould like to focus on the differentiation of MSA from otherparkinsonian diseases, especially from PD.

Although, there are number of reports performing EAS-EMGto differentiate MSA from other parkinsonism20 and manylaboratories concluded that EAS-EMG is useful for the differen-tiation of MSA,3,11,21 some laboratories concluded that EAS-EMG is not useful for the differentiation of MSA,22,23 and,therefore, the reliability of EAS-EMG remains unknown. Thereasons for the difference depend on whether they include‘‘late components’’ or not. Late components are defined aslate spikes which are distinct from the main component. Theappearance of late components usually suggests neurogenicchange in the examined muscle.24 The neurogenic pathome-chanism is based on decreased impulse propagation alongnerve terminals after primary nerve damage or after collateralreinnervation of denervated muscle fibers. These neurogenicchanges result in differences in the arrival time of the spikesat various muscle fibers, which could lead to the appearanceof late components in EMG.24 We think that including latecomponents might increase the reliability of EAS-EMG in thediagnosis of MSA.4,11,25 Other possibilities for the differentresults might include that some automated analysis techni-ques, resident in software in many modern EMG machineswhich ‘‘cut-up’’ the motor units into components particularlyif the unit has an iso-electric phase, thus underestimating theduration. However, the sample size or the severity of MSA andPD might also contribute to the different results. This studymight be able to validate the results of EAS-EMG due to thelarge number of patients, the inclusion of late components,and the ROC analysis of MUP parameter.The mean duration of MUPs is the most frequently used

parameter followed by the mean number of phases.25 In con-trast, the mean amplitude of MUPs is rarely used. However,the most appropriate MUP parameter to differentiate MSAfrom other parkinsonian syndromes remains unknown. Thecut-off value of the mean duration of MUPs differs significant-ly among laboratories.11 Although we used our duration crite-ria,12 we were unable to determine the more suitable criteriafor detecting neurogenic change in EAS-EMG. The availability

TABLE I. MUP Data in Each Disease

MSA PD DLB PSP P-value

Mean duration (ms) 9.33 � 2.38� 7.43 � 1.77 8.26 � 2.21�� 8.45 � 2.11��� <0.001

Mean phase 4.55 � 1.14� 4.13 � 0.86 4.62 � 1.04 4.40 � 0.75 <0.001

Mean amplitude (mV) 516.14 � 824.58 462.28 � 234.29 543.52 � 247.23 503.39 � 281.71 0.8055

Number of MUPs >10 ms 3.63 � 2.26� 1.96 � 1.71 2.80 � 2.04 2.92 � 2.21 <0.001

Each MUP data are represented in mean � SD.

ANOVA analysis showed significant differences in mean duration, mean number of MUPs >10 ms, and mean number of phases among each case of

parkinsonian syndrome.�MSA versus PD: P < 0.01.��DLB versus PD: P < 0.01.���PSP versus PD: P < 0.01.

Fig. 1. Distribution of the mean duration of MUPs in each disease. The

mean duration of MUPs in each disease. The mean duration of MUPs longer

than 10 ms is detected as neurogenic change in EAS-EMG (criteria b).

TABLE II. Sensitivity and Specificity of Our Duration Criteria

Sensitivity Specificity

(1) Differentiating MSA from other parkinsonian syndrome

Criteria (a) 0.66 0.52

Criteria (b) 0.35 0.84

(2) Differentiating MSA from PD

Criteria (a) 0.66 0.62

Criteria (b) 0.35 0.90

ROC Analysis of Sphincter EMG 3

Neurourology and Urodynamics DOI 10.1002/nau

of a relatively large number of patients with parkinsoniansyndromes, including many with MSA, facilitated the deter-mination of the most appropriate MUP parameter to differen-tiate MSA from other parkinsonian diseases, particularly PD,and also evaluation of the cut-off value of MUP parameters,using the ROC analysis.

The results of ROC analysis suggested that mean durationmay be the most appropriate parameter to differentiate MSAfrom other parkinsonian syndromes, followed by the meannumber of phases. However, the AUC in mean duration andmean number of phases were not sufficiently high to well-dif-ferentiate MSA from other parkinsonian syndromes. Similarly,the AUC for mean duration in distinguishing MSA from PDwas slightly higher than that in differentiation of MSA from

other parkinsonian syndromes. The higher AUC value in dis-tinguishing MSA from PD was probably attributed to the factthat the mean duration of MUP in PSP and DLB was signifi-cantly longer than that in PD (Table I). This result is consistentwith previous studies showing that some patients with PSPalso revealed neurogenic change in EAS-EMG.6

Next, we determined which of the above-mentioned our du-ration criteria are more appropriate in the diagnosis of MSA.The ROC analysis revealed that criteria (b) are significantlymore appropriate than criteria (a) in both differentiation ofMSA from other parkinsonian syndromes and in differentia-tion of MSA from PD.Previously, a wide range of cut-off values for MUP duration

(6–20 ms) was used in different laboratories. In 1997, Fowler

Fig. 2. Comparison of MUP parameters. a: ROC curves for MUP parameters between MSA and other parkinson-

isms. b: ROC curves for MUP parameters between MSA and PD. c: AUC values of MUP parameters.

4 Yamamoto et al.

Neurourology and Urodynamics DOI 10.1002/nau

Fig. 3. Comparison of criteria (a) and criteria (b) with our duration criteria. a: ROC curves according to our criteria

to distinguish between MSA and other parkinsonisms. b: ROC curves according to our criteria to distinguish

between MSA and PD. c: AUC values of our duration criteria.

ROC Analysis of Sphincter EMG 5

Neurourology and Urodynamics DOI 10.1002/nau

and colleagues12 proposed a cut-off value of ‘‘10 ms,’’ becausethe mean duration of MUPs in 156 MSA patients showed bi-modal distribution with a trough at 10 ms. Since then, the10 ms criterion has become prevalent. However, the sensitivi-ty of the cut-off value of 10 ms was 0.35 in our study, which ismarkedly low as compared to several previous studies. Thefeasible reason for this low sensitivity is that our MSApatients had shorter disease duration than those in otherstudies.1 We have previously reported that nearly half of thepatients with MSA whose duration was less than 2 years didnot show neurogenic change in EAS-EMG, and even the 17% ofthe patients MSA whose duration was longer than 5 years didnot show neurogenic change in EAS-EMG.18 On the otherhand, the specificity of the cut-off value; that is, 10 ms, in dif-ferentiating MSA from other parkinsonian syndromes andfrom PD was 0.85 and 0.90, respectively; this finding was con-current with other studies.1 Since the sensitivity of the cut-offvalue of 10 ms is low and there is much overlap in the dura-tions of MSA with the other three disorders with both longerand shorter durations in MSA, it is reasonable to change thecut-off value or to combine the number of polyphasic MUPwith the duration. For example, the sensitivity and the speci-ficity for cut-off value of 12 ms was 0.15 and 0.98, respective-ly. We also examined the feasibility of a cut-off of 12.0 mscombined with the number of polyphasic (mean number ofphase >6.0) MUPs and the sensitivity and the specificity was0.19 and 0.93, respectively. Since sphincter EMG test had highspecificity value in our study, it also seems reasonable to rede-fine a cut-off value as 12 ms. Combining the number of poly-phasic MUPs with a duration criteria may be anothercandidate for the new criteria. On the other hand, the cut-offvalue of 10 ms is the most widely used duration criteria andis considered abnormal when compared to normal values.26

Specificity of the cut-off value of 10 ms showed acceptableresults in this study. However, it should be noted that the sen-sitivity and the specificity value of this criterion is variableamong laboratories and can be confirmed only by furtherinvestigation.

There are some limitations in evaluating the data sets gath-ered from EAS-EMG studies. First, we do not have age-matched normal control data. Second, we do not know towhat extent the mean duration of MUPs >10 ms is abnormalas compared to age-matched normal data. This lack of normaldata might also be common in other laboratories. Gilad et al.26

performed EAS-EMG for 100 healthy adults (67 women and 33men) aged between 17 and 89 years. MUP amplitude, dura-tion, and polyphasicity tended to increase with age; however,age did not significantly affect MUP parameters. Furthermore,mean duration of MUPs ranged from 6.1 to 6.9 ms (SD, 1.1–1.5 ms), indicating that the mean duration of MUPs >10 mswas abnormal.26 However, considerable normal control dataobtained from various laboratories is necessary to validatenormal data pertaining to MUP parameters. Third, the meth-ods used to analyze MUPs vary among laboratories, whichmake data comparison difficult 27; for example, inclusion orexclusion of the late component in measuring the duration ofMUPs significantly influences the results of EAS-EMG analysis.In addition, the differences in EMG systems may also affectresults of EAS-EMG analysis. These technical issues remain un-resolved. Fourth, the definite diagnosis of the neurological dis-orders was not pathologically confirmed in this study. Since, itis not uncommon that pathological diagnosis is different fromclinical diagnosis, it could not be denied that the uncertain-ness in the clinical diagnosis might affect the results in thestudy. However, almost all of the patients were hospitalizedand carefully examined by many neurologists for a couple of

weeks to make a correct clinical diagnosis. Unfortunately, wecould not follow-up patients for many years and we did notknow the changes in the diagnosis over the years.In spite of the above-mentioned unresolved issues, this

study succeeded in including a large number of patients withparkinsonian syndromes who underwent EAS-EMG, whichassisted in confirming the ability of EAS-EMG in differentiat-ing MSA from other parkinsonian syndromes. ROC analysis ofMUP parameters confirms the possibility that the mean dura-tion of MUPs is the appropriate parameter and this finding isconcurrent with the results of previous studies.1

CONCLUSIONS

The results of this study suggest that the mean duration ofMUPs in EAS-EMG is the most appropriate parameter in differ-entiating MSA from other parkinsonian syndromes. However,EAS-EMG should be used as a supportive diagnostic tool forthe diagnosis of MSA.

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