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TERENCE J. O'BRIEN, M.D., FREDRIC B. MEYER, M.D., AND W. RICHARD MARSH, M.D.. Departments of Neurosurgery and Neurology; and Division of ...
J Neurosurg 105:71–76, 2006

Subtraction ictal single-photon emission computed tomography coregistered to magnetic resonance imaging in evaluating the need for repeated epilepsy surgery NICHOLAS M. WETJEN, M.D., GREGORY D. CASCINO, M.D., A. JAMES FESSLER, M.D., ELSON L. SO, M.D., JEFFREY R. BUCHHALTER, M.D., PH.D., BRIAN P. MULLAN, M.D., TERENCE J. O’BRIEN, M.D., FREDRIC B. MEYER, M.D., AND W. RICHARD MARSH, M.D. Departments of Neurosurgery and Neurology; and Division of Nuclear Medicine, Department of Diagnostic Radiology, Mayo Clinic, Rochester, Minnesota Object. The aim of this study was to determine whether ictal single-photon emission computed tomography (SPECT) is useful in localizing the site of seizure onset in patients in whom surgery for intractable epilepsy failed and who are being considered for repeated surgery. Methods. Subtraction ictal SPECT coregistered to magnetic resonance imaging (SISCOM) studies were retrospectively analyzed in 58 patients who were being evaluated for possible repeated resection for intractable partial epilepsy between January 1, 1996, and October 31, 1999. All patients had persistent seizures subsequent to an initial resection and underwent another excision. The SISCOM-demonstrated abnormalities were classified as concordant, discordant, or indeterminate, compared with the localization of the epileptogenic zone revealed on video electroencephalography monitoring. The ability of SISCOM to predict operative outcome was also determined in patients who had undergone repeated surgical procedures. The SISCOM studies revealed a localized hyperperfused alteration in 46 (79%) of 58 patients. Forty-one (89%) of these 46 patients had a SISCOM-demonstrated alteration in the hemisphere of the previous epilepsy surgery. Imaging changes in 33 (72%) of the 46 patients were at the site of the previous focal cortical resection. Eight (17%) of the 46 had SISCOM-demonstrated abnormalities remote from the lobe in which surgery had been performed but in the ipsilateral hemisphere. The hyperperfusion focus was in the contralateral hemisphere in the remaining five patients (11%). The site of the epileptogenic zone was concordant with the SISCOM focus in 32 (70%) of 46 patients. Twenty-six patients underwent repeated resection and were followed up for a mean of 44 months thereafter; 11 of these patients (42%) had a significant reduction in seizure tendency. Only five patients (19%) were seizure free. Ten (50%) of 20 patients with a concordant SISCOM focus compared with none (0%) of three patients with a discordant focus had a favorable surgical outcome (p = 0.23). Conclusions. The SISCOM method might be useful in the evaluation of, and the surgical planning for, patients with intractable partial epilepsy in whom previous resective treatment has failed and who are being considered for reoperation.

KEY WORDS • partial epilepsy • surgical treatment • repeated surgery

XCISION of the epileptogenic zone, that is, the site of seizure onset and initial seizure propagation, has been shown to be an effective alternative treatment in persons with intractable epilepsy.19 The most common surgical strategy for partial or localization-related epilepsy is focal resection of the anterior temporal lobe and mesial temporal structures. In a previous evidence-based study, authors revealed that approximately 70% of patients undergoing epilepsy surgery become seizure free after temporal lo-

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Abbreviations used in this paper: AED = antiepilepsy drug; ATL = anterior temporal lobectomy; EEG = electroencephalography; MR = magnetic resonance; SISCOM = subtraction ictal singlephoton emission computed tomography coregistered to MR imaging; SPECT = single-photon emission computed tomography.

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bectomy. Patients with extratemporal seizures may be less favorable operative candidates.8 Factors predictive of a less satisfactory surgical outcome include a nondiagnostic preoperative MR imaging study and the absence of a specific histopathological entity in the excised cortex.8,13 Approximately 20% of persons who undergo surgical treatment for a partial seizure disorder do not experience a significant reduction in seizure tendency, and thus the surgery is considered a failure.13 Potential reasons for an unfavorable surgical outcome include subtotal resection of the epileptogenic zone or incomplete excision of the pathological lesion.8,13,19 Treatment options in these patients include AED therapy, vagus nerve stimulation, and enrollment in an investigational study for epilepsy.3 Less than 10% of patients with intractable epilepsy will be seizure free with AED therapy or vagus nerve stimulation.3,7 Persons with 71

N. M. Wetjen, et al. partial epilepsy whose initial surgical procedure failed may be good candidates for a repeated operation.1,2,4–6,14–17,20 After repeated surgery, selected patients may experience no seizures or a significant reduction in their tendency. Ictal SPECT is used to identify a localized region of cerebral hyperperfusion and is a reliable indicator of the epileptogenic zone in patients with intractable partial epilepsy.9–12, 18,21 For revealing the site of seizure onset, SISCOM is a diagnostic innovation superior to visual interpretation of ictal and interictal SPECT. Furthermore, SISCOM has been shown to be of prognostic importance in patients undergoing epilepsy surgery.9–12 The purpose of the present study was to investigate the potential role of SISCOM when repeated surgery is being considered in patients in whom an initial resective epilepsy procedure failed. Clinical Material and Methods Patient Selection

The Mayo Foundation Institutional Review Board approved this study. The patients included in the present analysis were part of a series of 464 consecutive patients who had undergone an ictal SPECT injection during a presurgical evaluation at the Mayo Clinic, Rochester, Minnesota, between January 1, 1996, and October 31, 1999. During this period were identified 58 patients in whom previous surgical treatment for intractable partial epilepsy had failed, and these patients were being considered for another resection. These 58 patients were comprised of 33 females (57%) and 25 males (43%), whose mean age at the time of evaluation for the repeated surgery was 31 6 13.5 years (standard deviation, range 2–56 years). All underwent comprehensive evaluation, including routine asleep and awake EEG recordings with standard activating procedures, MR imaging of the head, neuropsychological studies, visual perimetry, and long-term video-EEG monitoring. Initial Epilepsy Surgery

Localization of epileptic brain tissue resected during the initial procedure is summarized in Table 1. In the present study, patients with MR imaging–demonstrated hippocampal atrophy were considered to have nonlesional partial epilepsy. The most common indication for surgical management was temporal lobe epilepsy. Twenty-one (36%) of the 58 patients underwent an ATL for pathologically verified hippocampal neuronal loss together with gliosis. Thirty-one (53%) of the 58 patients had a pathological substrate associated with an intraaxial lesion. Structural abnormalities included primary brain tumor (18 patients), malformed cortex (seven patients), arachnoid or porencephalic cyst (four patients), and focal encephalomalacia (two patients). Single-Photon Emission Computed Tomography Studies

Ictal SPECT studies were performed as described previously.9–12 The SISCOM method was used to analyze the imaging studies in all 58 patients. An SISCOM-demonstrated hyperperfused region of altered tissue was evaluated in 72

TABLE 1 Initial focal cortical resection for intractable epilepsy in 58 patients Lesion on MRI (no.) Surgery

temporal extratemporal frontal parietal occipital multilobar total

No. of Patients

Present*

Absent†

36 22 12 4 1 5 58

15 16 9 3 0 4 31

21 6 3 1 1 1 27

* Identified pathological lesion associated with epileptic brain tissue (see Initial Epilepsy Surgery for specific findings). † Includes patients with nonspecific findings or hippocampal atrophy.

these individuals. Localized imaging findings were classified both according to the relationship with the site of the initial epilepsy surgery, that is, ipsilateral (either adjacent to or far from the previous surgical site) or contralateral, and the results of the evaluation were performed before the repeated excision. Patients with discordant findings or without a localized electroclinical correlation underwent subsequent intracranial EEG monitoring. Any SISCOM-demonstrated abnormalities were also classified as concordant, discordant, or indeterminate, compared with the intracranial ictal EEG recording data. Repeated Surgery for Intractable Epilepsy

Thirty-one of the 58 patients underwent repeated resection after the SISCOM study and the comprehensive preoperative evaluation. Additional surgical treatment was deferred in 27 patients because the results of the comprehensive evaluation indicated that these persons were not favorable candidates for a focal cortical resection. All repeated resective procedures were performed at the Mayo Clinic. Details of the operation were analyzed to determine the prognostic importance of the SISCOM findings. Before the resection, intracranial EEG monitoring using depth electrodes or subdural strip or grid electrodes was performed in 15 patients for further localization. A modified Engel classification scheme was used to assess seizure outcome: Class I, seizure-free, auras only, single seizure with AED withdrawal; Class II, rare, nondisabling seizures (. 95% reduction in seizures); Class III, worthwhile improvement (80–94% reduction in seizures); Class IV, no worthwhile improvement (, 80% reduction in seizures).4 In the present study patients with a Class I or II outcome were considered to have a favorable surgical outcome. Statistical Methods

Statistical analysis was performed using the Fisher exact test (two-tailed) for categorical data and the Student t-test (two-tailed) for continuous data. Patients included in the statistical analyses to determine the prognostic importance of SISCOM consisted of those who had localizing ictal SPECT findings and had undergone both a repeated resection and a follow-up evaluation of at least 6 months. J. Neurosurg. / Volume 105 / July, 2006

Repeated excision and SISCOM in treating epilepsy

FIG. 1. An oblique coronal SISCOM image showing a localized region of hyperperfusion in the right frontal lobe. The patient had previously undergone a right ATL. Results of intracranial EEG monitoring confirmed the relationship between the ictal onset zone and the hyperperfusion focus. The patient was seizure free after a right frontal corticectomy.

Results Imaging Results

The SISCOM study revealed a hyperperfused localized alteration in 46 (79%) of 58 patients. Thirty-three (72%) of 46 imaging abnormalities were adjacent to the previous surgical site (for example, posterior to the resection margin), and eight (17%) of 46 were remote but in the ipsilateral cerebral hemisphere (Figs. 1 and 2). The hyperperfusion focus was in the contralateral hemisphere in five (11%) of 46 patients (Fig. 3). The SISCOM findings were indeterminate in 12 patients (21%). The onset zone revealed during the scalp-recorded ictal EEG monitoring was concordant with the SISCOM-demonstrated focus in 32 (70%) of 46 patients. The SISCOM findings were concordant with both the ictal EEG pattern and the MR imaging–demonstrated site of previous resection in 28 (61%) of 46 patients. The ictal SPECT data were correlated with the localization of epileptic brain tissue in the 15 patients who had undergone chronic intracranial EEG monitoring (Fig. 1). The SISCOM abnormality correctly lateralized the site of seizure onset in 12 (80%) of 15 patients. The localized imaging alteration was concordant with the ictal onset zone in seven (47%) of 15 patients. In five patients (33%) the SISCOM abnormality was ipsilateral to, but remote from, the site of seizure onset. In three patients (20%) the SISCOM data were either indeterminate (two patients) or revealed a localized abnormality contralateral to epileptic brain tissue (one patient; Fig. 3). Results of Repeated Surgery

Twenty-six (84%) of the 31 patients who had undergone J. Neurosurg. / Volume 105 / July, 2006

FIG. 2. An axial SISCOM image demonstrating a localized region of hyperperfusion in the left occipital lobe. The patient had previously undergone a left focal occipital corticectomy. Results of intracranial EEG monitoring confirmed the relationship between the ictal onset zone and the hyperperfusion focus. Seizures persisted after a left occipital cortical resection that included the SISCOMdemonstrated focus.

repeated resection were followed up for 6 months or longer thereafter (Table 2). The mean duration of the followup period in these 26 patients was 44 months (range 6–84 months). Seizure outcome at 1 year or longer postopera-

FIG. 3. An oblique coronal SISCOM image revealing a localized region of hyperperfusion in the right temporal lobe. The patient had previously undergone a left ATL. Results of intracranial EEG monitoring indicated a left temporal lobe neocortical origin for the seizures (remote from the SISCOM focus). The patient continued to have habitual seizures after a focal cortical resection in the left temporal lobe.

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N. M. Wetjen, et al. TABLE 2 Repeated surgery for intractable epilepsy in 26 patients Lesion on MRI (no.) Surgery

No. of Patients

Present*

Absent†

temporal extratemporal frontal parietal occipital multilobar total

15 11 7 3 1 0 26

0 3 2 1 0 0 3

15 8 5 2 1 0 23

* Identified pathological lesion associated with epileptic brain tissue (three primary brain tumors). † Includes patients with nonspecific findings or hippocampal atrophy.

tively could be determined in 24 of the 26 patients. Only one (4%) of the 26 patients had an MR imaging–demonstrated pathological substrate before the repeated surgery. Eleven (42%) of the 26 patients had a favorable surgical outcome and five persons (19%) became seizure free. Ten (38%) of 26 patients had a Class IV outcome. The site of focal cortical resection—in particular, extratemporal compared with temporal lobe—was not predictive of surgical outcome in this series (p = 1.0). Six (40%) of 15 patients who had undergone temporal lobe resections and five (45%) of 11 who had undergone extratemporal excisions had a favorable outcome. Chronic intracranial EEG monitoring before the repeated resection was of no prognostic importance (p = 0.69). The effect of the surgical strategy was evaluated in persons who had undergone an ATL as the initial procedure. Six (55%) of 11 patients who had undergone resection of the residual hippocampus and none (0%) of the four patients who had undergone repeated excision of the temporal lobe neocortical region had a favorable surgical outcome (p = 0.10). Surgical Outcome and SISCOM Data

The predictive value of SISCOM was assessed in 23 of the 26 patients who had undergone repeated excision and whose imaging studies had demonstrated a localized hyperperfused alteration (Table 3). The SISCOM-revealed abnormality was concordant with the epileptogenic zone in 20 (87%) of 23 patients. Ten (50%) of 20 patients with a concordant SISCOM focus and none (0%) of three patients with a discordant SISCOM focus had a favorable outcome. Note, however, that the results of the ictal SPECT study in this group of patients did not reach statistical significance (p = 0.23). The effect of SISCOM findings on operative outcome was also not significant when patients with indeterminate findings were included with individuals with discordant findings (p = 0.19). Discussion Selected persons whose initial surgery has failed may be considered for repeated excision to manage a disabling seizure disorder.1,2,5,6 Note, however, that a repeated surgery may be less effective and associated with increased adverse 74

effects compared with the initial surgical procedure.1,2,5,6,14–17 Data from previous studies have indicated that between 19 and 63% of patients undergoing a repeated resection become seizure free.1,2,5,6,14–17 Recent findings at our institution in 64 consecutive patients undergoing repeated excision revealed that 39% were made seizure free, whereas one third had no significant reduction in seizure tendency.17 In another study only four (19%) of 21 patients who had undergone an “aggressive” evaluation and initial surgical removal became seizure free after a second focal cortical resection.15 Favorable prognostic factors for repeated surgery have varied, including recurrent or residual abnormal lesional features, temporal lobe epilepsy, previous insufficient hippocampal resections, abnormal imaging findings, and focal interictal epileptiform discharges.1,2,5,6,14–17 Our study is the first series in which the diagnostic yield of SISCOM has been evaluated in patients being considered for repeated surgery after a previous procedure had been unsuccessful in treating intractable partial epilepsy. The SISCOM data provided a high localization rate and were concordant with extracranial and intracranial EEG recording results. Note, however, that we were unable to confirm the prognostic importance of SISCOM in individuals undergoing a second surgery. In previous studies authors using the SISCOM technique have indicated a predictive value for ictal SPECT in patients with intractable partial epilepsy who had undergone focal cortical resections.10–12 Our inability to demonstrate a significant beneficial effect of SISCOM in predicting surgical outcome may have been related to the relatively small number of patients who underwent repeated excision, a seizure-free outcome in only 19% of patients, and the use of the ictal SPECT results to select surgical candidates. Potential reasons for the unfavorable outcome in 15 (52%) of 26 patients include the predominance of nonlesional epilepsy and extrahippocampal neocortical resections in this series.14,15 The difference in seizure-free outcome between the present series and an earlier study in which we assessed the efficacy of repeated surgery may have been related to patient population.17 Thirty-nine percent of the patients in that previous study became seizure free. Only 14 (22%) of 64 patients required SISCOM before the repeated operation, however. Ictal SPECT is performed only in selected operative candidates when there is a conflicting presurgical evaluation or when scalp video-EEG monitoring does not localize the epileptogenic zone. Conclusions The results of our study demonstrate that ictal SPECT studies analyzed using the SISCOM technique commonly reveal a localizing abnormality in patients with intractable partial epilepsy whose previous surgery has failed. The hyperperfusion focus is usually concordant with localization of the epileptogenic zone as determined on a comprehensive presurgical evaluation. The SISCOM technique may be useful in selecting and evaluating patients with medically refractory partial epilepsy in whom an additional resection is being considered. The rationale for obtaining the ictal SPECT studies lies in identifying a potential site of seizure onset, guiding the implantation of intracranial electrodes for extraoperative monitoring, and possibly tailoring the resecJ. Neurosurg. / Volume 105 / July, 2006

Repeated excision and SISCOM in treating epilepsy TABLE 3 Site of surgical removal, SISCOM-demonstrated localization, and seizure outcome in 26 patients who underwent resection* Case No.

Site of Initial Resection

Site of Repeated Resection†

Concordant w/ SISCOM Localization

Outcome After Repeated Surgery‡

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26

rt temporal lt occipital rt temporal lt temporal lt parietal rt parietal lt parietal rt temporal rt frontal lt frontal lt frontal lt temporal lt occipital lt temporal lt temporal lt frontal lt temporal lt parietal lt temporal lt temporal lt temporal lt frontal rt temporal lt frontal lt temporal lt temporal

rt temporoparietal lt temporal rt frontal lt temporal lt parietal, LES rt temporoparietal lt parietal rt temporal rt frontal lt frontal lt frontal, LES lt temporal lt occipital lt temporal lt temporal lt frontal lt temporal lt parietal, LES lt temporal lt temporal lt temporal lt frontal rt temporal lt frontal lt temporal lt temporal

yes (LOC) yes (HEMI) yes (LOC) no (LOC) yes (LOC) yes (LOC) yes (HEMI) no (HEMI) yes (LOC) yes (LOC) NL yes (LOC) yes (LOC) no yes (LOC) NL yes (LOC) NL yes (LOC) yes (LOC) yes (LOC) yes (LOC) yes (LOC) yes (LOC) yes (LOC) yes (LOC)

favorable unfavorable favorable (SF) unfavorable favorable (SF) unfavorable unfavorable unfavorable favorable unfavorable favorable favorable (SF) unfavorable unfavorable unfavorable unfavorable unfavorable unfavorable favorable favorable favorable (SF) favorable (SF) unfavorable unfavorable favorable unfavorable

* HEMI = unilateral multilobar or hemispheric abnormality; LES = pathological lesion; LOC = localized regional abnormality; NL = nonlocalizing; SF = seizure free. † Patients who underwent temporoparietal resections were classified as having temporal lobe epilepsy. ‡ Favorable, Class I and II outcomes; unfavorable, Class III and IV outcomes. See Repeated Surgery for Intractable Epilepsy for seizure classification.

tion.10–12,18,21 Additional studies with greater patient numbers will be necessary to confirm the predictive value of this neurodiagnostic technique in patients who undergo repeated resections. Unfortunately, data in the present series also provide additional evidence that most patients continue to experience seizures after a repeated excision, even when the initial surgical procedure involved an attempted total resection of the epileptogenic zone. References 1. Awad IA: Reoperation for intractable seizures. Clin Neurosurg 39:125–139, 1992 2. Awad IA, Nayel MH, Luders H: Second operation after the failure of previous resection for epilepsy. Neurosurgery 28:510–518, 1991 3. DeGiorgio CM, Schachter SC, Handforth A, Salinsky M, Thompson J, Uthman B, et al: Prospective long-term study of vagus nerve stimulation for the treatment of refractory seizures. Epilepsia 41:1195–1200, 2000 4. Engel J Jr, Van Ness P, Rasmussen TB, Ojemann LM: Outcome with respect to epileptic seizures, in Engel J Jr (ed): Surgical Treatment of the Epilepsies, ed 2. New York: Raven Press, 1993, pp 609–621 5. Germano IM, Poulin N, Olivier A: Reoperation for recurrent temporal lobe epilepsy. J Neurosurg 81:31–36, 1994 6. Hennessy MJ, Elwes RD, Binnie CD, Polkey CE: Failed surgery

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for epilepsy. A study of persistence and recurrence of seizures following temporal resection. Brain 123:2445–2466, 2000 Kwam P, Brodie MJ: Early identification of refractory epilepsy. N Engl J Med 342:314–319, 2000 Mosewich RK, So EL, O’Brien TJ, Cascino GD, Sharbrough FW, Marsh WR, et al: Factors predictive of the outcome of frontal lobe epilepsy surgery. Epilepsia 41:843–849, 2000 O’Brien TJ, O’Connor MK, Mullan BP, Brinkmann BH, Hanson D, Jack CR, et al: Subtraction ictal SPET co-registered to MRI in partial epilepsy: description and technical validation of the method with phantom and patient studies. Nucl Med Commun 19: 31–45, 1998 O’Brien TJ, So EL, Cascino GD, Hauser MF, Marsh WR, Meyer FB, et al: Subtraction SPECT coregistered to MRI in focal malformations of cortical development: localization of the epileptogenic zone in epilepsy surgery candidates. Epilepsia 45:367–376, 2004 O’Brien TJ, So EL, Mullan BP, Cascino GD, Hauser MF, Brinkmann BH, et al: Subtraction peri-ictal SPECT is predictive of extratemporal epilepsy surgery outcome. Neurology 55:1668–1677, 2000 O’Brien TJ, So EL, Mullan BP, Hauser MF, Brinkmann BH, Bohnen NI, et al: Subtraction ictal SPECT co-registered to MRI improves clinical usefulness of SPECT in localizing the surgical seizure focus. Neurology 50:445–454, 1998 Radhakrishnan K, So EL, Silbert PL, Jack CR Jr, Cascino GD, Sharbrough FW, et al: Predictors of outcome of anterior temporal lobectomy for intractable epilepsy: a multivariate study. Neurology 51:465–471, 1998

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N. M. Wetjen, et al. 14. Salanova V, Markand O, Worth R: Temporal lobe epilepsy: analysis of failures and the role of reoperation. Acta Neurol Scand 111:126–133, 2005 15. Schwartz TH, Spencer DD: Strategies for reoperation after comprehensive epilepsy surgery. J Neurosurg 95:615–623, 2001 16. Shaver EG, Harvey AS, Morrison G, Prats A, Jayakar P, Dean P, et al: Results and complications after reoperation for failed epilepsy surgery in children. Pediatr Neurosurg 27:194–202, 1997 17. Siegel AM, Cascino GD, Meyer FB, McClelland RL, So EL, Marsh WR, et al: Resective reoperation for failed epilepsy surgery: seizure outcome in 64 patients. Neurology 63:2298–2302, 2004 18. Spanaki MV, Spencer SS, Corsi M, MacMullan J, Seibyl J, Zubal IG: Sensitivity and specificity of quantitative difference SPECT analysis in seizure localization. J Nucl Med 40:730–736, 1999 19. Wiebe S, Blume WT, Girvin JP, Eliasziw M: Effectiveness and efficiency of surgery for temporal lobe epilepsy study group: a ran-

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domized, controlled trial of surgery for temporal-lobe epilepsy. N Engl J Med 345:311–318, 2001 20. Wyler AR, Hermann BP, Richey ET: Results of reoperation for failed epilepsy surgery. J Neurosurg 71:815–819, 1989 21. Zubal IG, Spencer SS, Imam K, Seibyl J, Smith EO, Wisniewski G, et al: Difference images calculated from ictal and interictal technetium-99m-HMPAO SPECT scans of epilepsy. J Nucl Med 36:684–689, 1995 Manuscript received March 3, 2005. Accepted in final form January 18, 2006. Address for Dr. Fessler: University of Rochester, New York. Address for Dr. O’Brien: The Royal Melbourne Hospital, University of Melbourne, Victoria, Australia. Address reprint requests to: Gregory D. Cascino, M.D., Department of Neurology, Mayo Clinic, 200 First Street SW, Rochester, Minnesota 55905. email: [email protected].

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