Upload
tobias-loddenkemper
View
213
Download
0
Embed Size (px)
Citation preview
Brief Communication
Ictal Urinary Urge: Further Evidence for Lateralization to theNondominant Hemisphere
*Tobias Loddenkemper, *Nancy Foldvary, †Shanker Raja, *Silvia Neme, and *Hans O. Lüders
Departments of *Neurology and †Nuclear Medicine, Cleveland Clinic Foundation, Cleveland, Ohio, U.S.A.
Summary: Purpose: To determine the lateralizing value ofictal urinary urgency.
Methods: A retrospective database search was performed forpatients with ictal urinary urgency admitted to the EpilepsyMonitoring Unit at the Cleveland Clinic between 1994 and2001.
Results: Six patients were identified; intracarotid amytal testdemonstrated left hemispheric speech dominance in five cases.
The sixth patient continued to speak during right temporal sei-zures. EEG and imaging data supported right temporal or fron-totemporal epilepsy in all six cases. Two patients were seizurefree after focal right hemispheric resection.
Conclusions: Ictal urinary urge appears to be a lateralizingsign for nondominant temporal lobe epilepsy. Key Words: Ic-tal urinary urge—Temporal—Lateralizing sign—Nondominant.
Ictal “desire to void” was first described by Feindeland Penfield in 1954 (1). The frequency of this auto-nomic manifestation in temporal lobe epilepsy (TLE)ranges from 0.3 to 8% (1–3). Recently a series of sixpatients with an aura of ictal urinary urge was described(4). Four of these patients underwent intracarotid amytaltesting (IAT) and were found to have seizures arisingfrom the either right or left, but always nondominanttemporal lobe.
METHODS
Medical records of 3,446 patients who underwentvideo-EEG monitoring at the Cleveland Clinic between1994 and 2001 were reviewed for the presence of ictalurinary urge. The patient population consisted of 75%with focal epilepsy (temporal, 48%; extratemporal, 19%;nonclassifiable focal, 8%), 5% with generalized epilepsy,1% with multifocal epilepsy, and 19% with nonepilepticseizures.
Clinical history, interictal and ictal video-EEG record-ings with scalp and sphenoidal electrodes, and imagingstudies were reviewed. Trained EEG/epilepsy technolo-
gists and nurses tested the patients during and after sei-zures to determine level of consciousness and reactivity.Only patients with repeated seizures with ictal urinaryurge were included.
RESULTS
Six patients were identified (0.4% of all patients withTLE). The results are summarized in Table 1. In allcases, patients reported an urge to void at the onset ofclinical seizures, usually accompanied by other types ofauras. None of these patients had urinary incontinence.In one patient (case 5), urinary urgency was the firstsymptom of impending seizures. The IAT revealed lefthemispheric speech dominance in five patients studied.The sixth patient was right-handed and had ictal speechduring right-hemispheric EEG seizures. In all cases, ictaland interictal EEG suggested localization of the seizureonset to the nondominant, right temporal region. In twopatients, seizures originated independently from the leftand right temporal regions; however, only the right tem-poral seizures were associated with ictal urinary urge. Inall cases with documented left hemisphere speech domi-nance, neuroimaging revealed abnormalities involvingthe temporal lobe, often extending to the insula or infe-rior frontal regions. In two cases, right anterior temporalresection led to seizure freedom.
Accepted August 25, 2002.Address correspondence and reprint requests to Dr. T.
Loddenkemper at Section of Epilepsy and Sleep Disorders, The Cleve-land Clinic Foundation, 9500 Euclid Ave, S-51 Cleveland, 44195 OH,U.S.A. E-mail: [email protected]
Epilepsia, 44(1):124–126, 2003Blackwell Publishing, Inc.© International League Against Epilepsy
124
DISCUSSION
Auras of a “desire to void” and increased intravesicalpressure are infrequent manifestations of focal seizures(1,2). We report six patients with ictal urinary urgencyduring seizures arising from the right hemisphere. Ourdata support and further extend a recent report in whichsix (2.2%) of 227 patients with TLE reported ictal uri-nary urge, all of whom had seizures arising from thenondominant temporal lobe based on IAT (4). In twocases, ictal single-photon emission tomography (SPECT)demonstrated hyperperfusion involving the right tempo-ral lobe, including the superior temporal gyrus and theinsular cortex (4).
Urinary urge and incontinence has been described inpatients with right frontal tumors (5,6) and right hemi-spheric strokes (7). Maurice-Williams et al. (5) reportedimpaired micturition control in seven of 50 patients withfrontal tumors, six of whom had lesions involving theright hemisphere. Kuroiwa et al. (7) studied micturitionin 134 chronic hemiplegic patients and found that thosewith right hemispheric lesions were significantly morelikely to report urinary urgency and frequency. Addition-ally, 43% of elderly patients with urge incontinence anddecreased sensation to void, as demonstrated by urody-
namics, were found to have right frontal hypoperfusionon SPECT as compared with 4% in a control group with-out bladder complaints (8).
A positron emission tomography (PET) study involv-ing 17 healthy, right-handed volunteers demonstrated hy-permetabolism in the right medial temporal gyrus andright anterior cingulate gyrus during voluntary urinaryretention (10). During micturation, hypermetabolism wasnoted in the right medial temporal gyrus, right inferiorfrontal gyrus, right frontal operculum, dorsomedial pon-tine tegmentum, periaqueductal grey and rostral hypo-thalamus (9). A more recent PET study involving 11 menduring different degrees of passive bladder filling alsosuggested right-sided activation of the hypothalamusduring micturition (10). During passive bladder filling,no lateralized PET findings were appreciated (10). How-ever, this study included right- as well as left-handedsubjects. Additionally, differences in methods may havecontributed to these findings [e.g., active voiding (9) vs.passive bladder filling (10)].
Evidence for a symptomatogenic region of urinaryurge in the frontal lobe derives from SPECT studies inelderly patients with an uninhibited overactive bladderand a reduced sensation of urinary urge. Reduced frontalmetabolism was found in these patients as compared
TABLE 1. Case descriptions of six patients with ictal urinary urge
CaseRisk
factorsInterictal
EEGIctalEEG Semiology
Seizures withdocumented
UU/totalrecorded
Speech(IAT) Imaging
Surgery/follow-up
37 y/o F FS, familyhistory
RT temp RT Hem, maxFT
Intraoral tingling, UU,nausea → OA, MA(1/mo)
4/7 LT MRI: NLPET: ↓ RT superior
tempMRS: ↓ NAA/Cho RT
anterior tempIctal SPECT: ↑ RT
superior temp, insula
Evaluation inprogress
12 y/o F None Generalizeda (99%);RT temp (1%)
RT temp Fear, chest tingling,UU → LOC, OA,MA (12/mo)
4/6 LT MRI: RT temp tumorPET: ↓ RT tempIctal SPECT: ↑ RT
insula, inferior frontal
RT TL; GG,Engel 1A(seizure free)
39 y/o M FS, CHI RT temp RT temp Abd sens, UU → OA,MA (10/mo)
2/4 LT MRI: RT MTSPET: ↓ RT tempMRS: ↓ NAA/Cho RT
temp
RT TL; MTS;Engel 1A(seizure free)
37 y/o M CHI RT temp (30%) RT temp Dizziness, UU (1/mo) 3/3 LT MRI: BL FTencephalomalacia
LT TL within lastmonth; MTS
LT temp (70%) LT temp Nonspecific aura →OA → RT version→ GMS (2/mo)
0/9
55 y/o F None RT temp (90%); RTparietal (10%)
RT Hem, maxFT
UU, fear, Abd sens,chills → LT facetonic → GMS(1/mo)
3/6 LT MRI: RT FT tumorPET: ↓ RT Hem
RT FT resection;GG; lost tofollow-up after8 wk
24 y/o F Familyhistory
RT temp (40%) RT temp UU → OA, MA, ictalspeech (3/mo)
4/5 NA MRI: LT & RT MTS Evaluation inprogress
LT temp (60%) LT temp Feels cold → OA,MA, RT handposturing (7/mo)
0/17
Abd sens, abdominal sensation; BL, bilateral; Cho, choline; CHI, closed head injury; F, female; FS, febrile seizures; FT, frontotemporal; GG, ganglioglioma; GMS,generalized motor seizure; Hem, hemisphere; IAT, intracarotid amobarbital test; Lt, left; LOC, loss of consciousness; M, male; MA, manual automatisms; MRS, magneticresonance spectroscopy; MTS, mesial temporal sclerosis; mo, month; NA, not accomplished; NAA, N-acetylaspartate; NL, normal; OA, oral automatisms; Rt, right; temp,temporal; SPECT, single-photon emission computed tomography; TL, temporal lobectomy; UU, urinary urge; y/o, years old.
a After resection of a ganglioglioma in case 2, generalized interictal epileptiform discharges disappeared, supporting the presence of tumor-induced generalizedepileptogenicity.
ICTAL URINARY URGE 125
Epilepsia, Vol. 44, No. 1, 2003
with a normal control group (13). In a series on 38 pa-tients with disturbances of micturition, all had lesionsin the anterior mesial frontal lobe including leucotomy(n � 22), intracranial tumors (n � 10), penetrating brainwounds (n � 4), and ruptured aneurysms (n � 2) (14).
Functional (8,9) and lesional (5–7) studies support thelocation of the symptomatogenic zone for urinary urge tobe in the medial temporal gyrus, opercular, and mesialfrontal regions. However, the epileptogenic zone mayinvolve entirely different areas than the symptomato-genic zone. If the patient is seizure free after surgery, itis assumed that the epileptogenic zone was included inthe resection (11). Two of our patients remained seizurefree after temporal lobe resection and therefore had aproven epileptogenic zone in the right temporal lobe.Whereas a prior series of patients with ictal urinary urgestrongly suggested TLE based on EEG and imaging (4),we report the first two cases of ictal urinary urge with aproven right temporal epileptogenic zone based on sei-zure freedom after resection. Propagation from a silentepileptogenic region may produce urinary urge as thedischarge spreads to the symptomatic zone.
The frontal lobe and in particular, the right anteriorcingulate gyrus and the right inferior frontal gyrus, havebeen suggested to play a major role in suprapontine blad-der control (9). Blok et al. (9) hypothesized that de-creased cerebral blood flow during withholding of urinein the anterior cingulate gyrus, which usually facilitatescertain behavioral patterns, may be related to an inhibi-tion of the urge to void. Seizure propagation from atemporal lobe focus into the frontal lobe cannot be ruledout in our cases and in the previous series (4).
To our knowledge, ictal urinary urge has never beenreported in patients with epilepsy arising from the dom-inant hemisphere. Such an aura could be easily missedbecause seizures arising from the dominant hemisphere,particularly the temporal lobe, more frequently producealtered levels of awareness (15) and amnesia (16), ascompared with seizures arising from the nondominanttemporal lobe.
CONCLUSION
Ictal urinary urge appears to occur in patients withnondominant hemispheric focal epilepsy, most notably,TLE. Urinary urge should be considered a useful later-
alizing and localizing sign in the evaluation of candidatesfor epilepsy surgery.
Acknowledgment: Author T.L. was supported by Innova-tive Medizinische Forschung, WWU Münster (FoeKz. LO610101) and NRW-Nachwuchsgruppe Kn2000, Federal Min-istry of Education and Research (Foe.1KS9604/0), Interdisci-plinary Center of Clinical Research Münster, Germany (IZKFProject NWG2). The data were partially presented at theAmerican Epilepsy Society meeting, Philadelphia, December2001. This study was approved by the Institutional ReviewBoard of the Cleveland Clinic Foundation.
REFERENCES
1. Feindel W, Penfield W. Localization of discharge in temporal lobeautomatism [Abstract]. Arch Neurol Psychiatry 1954;72:605–730.
2. Gupta AK, Jeavons PM, Hughes RC. Aura in temporal lobe epi-lepsy: clinical and electroencephalographic correlation. J NeurolNeurosurg Psychiatry 1983;46:1079–83.
3. O’Donnovan CA, Burgess RC, Lüders HO. Autonomic auras. In:Lüders HO, Noachtar S, eds. Epileptic seizures: pathophysiologyand clinical semiology. 1st ed. New York: Churchill Livingstone,2000:320–8.
4. Baumgärtner C, Groppel G, Leutmezer F, et al. Ictal urinary urgeindicates seizure onset in the nondominant temporal lobe. Neurol-ogy 2000;55:432–4.
5. Maurice-Williams RS. Micturition symptoms in frontal tumours. JNeurol Neurosurg Psychiatry 1974;37:431–6.
6. Andrew J, Nathan PW. Lesions of the anterior frontal lobes anddisturbances of micturition and defaecation. Brain 1964;87:233–62.
7. Kuroiwa Y, Tohgi H, Ono S, et al. Frequency and urgency ofmicturition in hemiplegic patients: relationship to hemisphere lat-erality of lesions. J Neurol 1987;234:100–2.
8. Griffiths D. Clinical studies of cerebral and urinary tract functionin elderly people with urinary incontinence. Behav Brain Res 1998;92:151–6.
9. Blok BF, Willemsen AT, Holstege G. A PET study on brain con-trol of micturition in humans. Brain 1997;120:111–21.
10. Athwal BS, Berkley KJ, Hussain I, et al. Brain responses tochanges in bladder volume and urge to void in healthy men. Brain2001;124:369–77.
11. Rosenow F, Lüders H. Presurgical evaluation of epilepsy. Brain2001;124:1683–700.
12. Blok BF, Willemsen AT, Holstege G. A PET study on brain con-trol of micturition in humans. Brain 1997;120:111–21.
13. Griffiths DJ, McCracken PN, Harrison GM, et al. Cerebral aetiol-ogy of urinary urge incontinence in elderly people. Age Ageing1994;23:246–50.
14. Andrew J, Nathan PW. Lesions of the anterior frontal lobes anddisturbances of micturition and defaecation. Brain 1964;87:233–62.
15. Ebner A, Dinner DS, Noachtar S, et al. Automatisms with pre-served responsiveness: a lateralizing sign in psychomotor seizures.Neurology 1995;45:61–4.
16. Jokeit H, Daamen M, Zang H, et al. Seizures accelerate forgettingin patients with left-sided temporal lobe epilepsy. Neurology 2001;57:125–6.
T. LODDENKEMPER ET AL.126
Epilepsia, Vol. 44, No. 1, 2003