Professional Documents
Culture Documents
|
Revised: 3 August 2020
|
Accepted: 3 August 2020
DOI: 10.1111/epi.16664
1
Department of Neurosurgery, Icahn School
of Medicine at Mount Sinai, New York,
Abstract
NY, USA Objective: Despite national guidelines supporting surgical referral in drug-resistant
2
Department of Neurology, Icahn School of epilepsy, it is hypothesized that surgery is underutilized. We investigated the vol-
Medicine at Mount Sinai, New York, NY,
umes of lobectomy/amygdalohippocampectomy surgeries over time and examined
USA
3 differences in outcomes between (1) high-volume (HV), middle-volume (MV), and
Division of Health Outcomes &
Knowledge Translation Research, Icahn low-volume (LV) hospitals and (2) Level 4 Centers versus non–Level 4 Centers.
School of Medicine at Mount Sinai, New Methods: The 2003-2014 National Inpatient Sample (the largest all-payer hospi-
York, NY, USA
talization database, representative of the US population) was utilized. Epilepsy was
Correspondence identified using a previously validated International Classification of Diseases,
Churl-Su Kwon, Icahn School of Medicine Ninth Revision, Clinical Modification (ICD-9-CM) case definition and surgeries
at Mount Sinai, One Gustave L. Levy Place,
New York, NY 10029. using ICD-9-CM procedure codes. A hospital was considered a Level 4 Center if
Email: churlsu.kwon@mssm.edu it performed intracranial electroencephalographic (EEG) monitoring. Tumor sur-
geries were excluded. Linear regression was used to perform trend tests. Weighted
multivariate logistic regression was used to summarize association of surgery with
outcomes.
Results: A total of 4,487 lobectomy/amygdalohippocampectomy surgeries were per-
formed in children and adults with epilepsy. Lobectomy/amygdalohippocampectomy
surgeries significantly decreased over time (slope: −0.24, P < .001). This declin-
ing surgical trend was greater for all resective/disconnective surgery (slope: −0.45,
P < .001), and greatest when compared to all types of epilepsy surgery, for example,
resection/disconnection/radiosurgery/laser interstitial thermal therapy/vagus nerve
stimulation/deep brain stimulation/responsive neurostimulation/intracranial EEG
(slope: −0.95, P < .001). LV compared to HV hospitals had higher odds of transfer
to other facilities (13.60% vs 4.24%, odds ratio [OR] = 2.76, 95% confidence interval
[CI] = 1.11-6.82). LV hospitals had higher odds of surgical complications versus
MV (12.69% vs 6.80%, OR = 2.20, 95% CI = 1.01-5.09). HV hospitals incurred the
least total charges. There were no differences in discharge status, adverse events,
length of stay, or cost between Level 4 Centers versus non–Level 4 Centers.
Significance: Lobectomies/amygdalohippocampectomies are decreasing over
time, suggesting ongoing underutilization. LV centers are associated with greater
Epilepsia. 2020;00:1–10. |
wileyonlinelibrary.com/journal/epi 1
|
2 KWON et al.
complication and transfer rates. Future studies are required to understand the reason
for worse outcomes in LV centers and to determine whether a minimum number of
surgeries must be performed to meet necessary standards.
KEYWORDS
epilepsy surgery, hospital volume, Level 4 Center, lobectomy trends
1 | IN TRO D U C T ION
Key Points
Drug-resistant epilepsy patients often fail to receive a pre-
• Lobectomies/amygdalohippocampectomies
surgical evaluation, although level 1 evidence suggests that
are decreasing over time, suggesting ongoing
individuals who fail two antiseizure medications are not
underutilization
likely to respond to further medication trials.1,2 Since the piv-
• Low-volume centers are associated with greater
otal randomized-controlled trial (RCT) for epilepsy surgery
complication and transfer rates
showing its effectiveness in appropriately selected candidates
• No differences are seen in outcomes between
with drug-resistant epilepsy, temporal lobectomy has been a
Level 4 Centers and non–Level 4 Centers for
well-established, safe, and effective mode of treatment.3,4
lobectomies/amygdalohippocampectomies
Seizure freedom can be achieved for a significant proportion
• A minimum number of surgeries performed to
of these patients, with the number needed to treat with sur-
meet necessary standards may be considered
gery for an additional patient to become seizure-free being
two. This RCT showed seizure freedom in 73% of those who
underwent surgery at 2 years of follow-up versus 0% in those
treated with medicine alone.3 Ten-year follow-up studies also
report good results, with seizure freedom in 50%-60% of pa- sample of discharges from community hospitals (all nonfed-
tients undergoing temporal lobectomy and 30%-40% of those eral, short-term general and special hospitals, special chil-
undergoing frontal lobe resections.5–7 Despite national guide- dren's hospitals), whose facilities and services are available
lines supporting surgical referral in drug-resistant epilepsy, it to the public. Discharges from rehabilitation and long-term
is thought that surgery is underutilized.8 acute care hospitals are not included in this sample. From
In this study, we sought to examine the trends of epilepsy 1988 to 2011, the NIS database was created by including
surgery utilization since the publication of national guide- 100% of all discharges from 20% of US hospitals every year
lines and investigate whether there were any differences in and was restructured in 2012 as a 20% national patient-level
outcomes between high, middle, and low surgical volume sample; thus, for our hospital volume comparison analysis,
hospitals as well as Level 4 Centers versus non–Level 4 we used only up to 2011 data.9
Centers. We hypothesize that epilepsy surgery remains un- To create the NIS database, samples of discharges are ex-
derutilized, with the proportion of those drug-resistant not tracted from the SID hospitals that are stratified based on the
changing and with increasing numbers of active epilepsy pa- following hospital characteristics: census division, hospital
tients over time. teaching status, bed size, location, and ownership. The NIS
covers >95% of the US population, and its weighted design
enables calculation of precise national level estimates. The
2 | METHODS NIS includes data on patient demographics, hospital charac-
teristics, admission/discharge dispositions, location, primary
2.1 | Study design and data source payer status, diagnoses, procedures, patient diagnosis–related
group, charges, length of stay, and comorbidities.
The National Inpatient Sample (NIS) database for the years
2003-2014 was used to perform a retrospective population-
based observational study. The NIS is a component of the 2.2 | Cohort identification
Healthcare Cost and Utilization Project (HCUP), supported
by the Agency for Healthcare Research and Quality. Sampled Patients of any age were included if they had a primary or
from the State Inpatient Database (SID), the NIS comprises secondary diagnosis of epilepsy identified in the NIS data-
patient- and hospital-level factors from ~8 million yearly hos- base (2003-2014) using a previously validated case defini-
pital admissions. The NIS includes around a 20% stratified tion of the International Classification of Diseases, Ninth
KWON et al.
|
3
calculated for lobectomy/amygdalohippocampectomy for However, a declining surgical trend was even greater for all
each year from 2003 to 2011. Total annual primary epilepsy resective/disconnective surgery (slope: −0.45, P < .001),
discharges were used as the denominator for total epilepsy and greatest when comparing to all types of epilepsy sur-
surgical volumes. gery (slope: −0.95, P < .001). There was no significant trend
In all analyses, national level estimates were calculated over time when comparing across hospital volumes for per-
after accounting for survey (stratum and cluster) weights. centages of lobectomies/amygdalohippocampectomies per-
Statistical Analysis Software (SAS) version 9.4 was used to formed (Figure 2).
conduct all analyses (SAS Institute). As compared to HV hospitals, LV hospitals had signifi-
cantly higher odds of transfer to other facilities (13.60% vs
4.24%, odds ratio [OR] = 2.76, 95% confidence interval
3 | R ES U LTS [CI] = 1.11-6.82). No discharges against medical advice
were noted in this cohort. There were no inpatient mortal-
A total of 4487 elective lobectomy/amygdalohippocampec- ities across hospitals. The mean LOS was not significantly
tomy surgeries were performed in children and adults with different across different hospital volumes (HV: 7.35 days,
epilepsy from 2003 to 2011. HV and MV hospitals performed MV: 7.46 days, LV: 7.59 days); however, one would expect
more elective lobectomy/amygdalohippocampectomy sur- significantly higher LOS in LV hospitals if patients were not
geries in younger people (HV: 29.80 years, MV: 30.84 years, transferred to other types of facilities. HV hospitals incurred
LV: 37.79 years; P < .01). Hospitalizations in HV and MV the lowest total charge (HV: $89,914, MV: $103,244, LV:
hospitals were primarily in those who had private insurance $96,623). As compared to MV hospitals, LV hospitals had
(HV: 58.20%, MV: 58.08%, LV: 50.62%; P < .01), whereas higher odds of surgical complications (12.69% vs 6.80%, OR
LV hospitals had greater admissions in those who were on = 2.20, 95% CI = 1.01-5.09) (Tables 1-6). A significantly
Medicare (HV: 11.30%, MV: 14.19%, LV: 28.99%; P < .01). greater proportion of stroke, hematoma formation, and hy-
About half the population were female (54.72%). The majority drocephalus occurred in LV hospitals as compared to MV
of surgeries were performed in urban teaching hospitals (HV: and HV hospitals (Supplementary Table S3). There were no
96.55%, MV: 88.17%, LV: 86.03%; P < .01). No significant differences in medical complications across different hospital
differences in race, median household income, or Elixhauser volumes.
Comorbidity Index were noted across hospital volumes. There were no differences in discharge status, adverse
Lobectomy/amygdalohippocampectomy surgeries signifi- events, LOS, or cost between Level 4 Centers versus non–
cantly decreased over time (slope: −0.24, P < .001; Figure 1). Level 4 Centers (Supplementary Tables S5-S12).
To determine whether this trend was due to other types of
surgery being performed more frequently, all resective/dis-
connective surgeries as well as all epilepsy surgery types 4 | DISCUSSION
(resection/disconnection/radiosurgery/LITT/vagus nerve
stimulation/deep brain stimulation/responsive neurostimu- In this study, we show that rates of surgical lobectomies/
lation/intracranial electroencephalogram) were investigated. amygdalohippocampectomies decreased over the 2003-2014
F I G U R E 1 Trends of surgery
in elective admissions for epilepsy as
a percentage of all primary epilepsy
discharges comparing lobectomies/
amygdalohippocampectomies versus
resective/disconnective surgeries versus
all epilepsy surgery types (resection/
disconnection/radiosurgery/laser
interstitial thermal therapy/vagal nerve
stimulation/deep brain stimulation/
responsive neurostimulation/intracranial
electroencephalogram)
KWON et al.
|
5
F I G U R E 2 Percentage of lobectomies/
amygdalohippocampectomies performed by
hospital volume from 2003 to 2011
period. This decrease in trend was also seen when looking the proportion of drug-resistant epilepsy patients has not
at all epilepsy surgery types, that is, not just resective sur- changed.21 Thus, with the significantly increasing numbers
geries (Figure 1). This decrease is of concern, because it oc- eligible for surgery and decreasing (nonsignificant) trends of
curred in a period of increasingly publicized evidence of the actual surgery performed, we are seeing persistent underuti-
efficacy of temporal lobectomy including RCTs and society lization of epilepsy surgery in the USA. A nationwide study
guidelines recommending early referral for surgery in the using the American College of Surgeons National Surgical
treatment of drug-resistant epilepsy.3,4,8 The declining surgi- Quality Improvement Program database looked at trends of
cal rate is concerning and adds to prior studies showing that spinal and cranial surgeries from 2006 to 2013.22 The total
epilepsy surgery is underused.16–18 number of spinal and cranial cases increased throughout the
Regarding the overall number of surgeries, there is no study period.
change (nonsignificant decreasing trends) between 2003 and It is also notable that the number of Level 4 Centers in-
2009 and again between 2010 and 2014. However, there ap- creased during this time period, which suggests that the un-
pears to be an increase in overall numbers from 2009 to 2010. derutilization is less likely to be a capacity problem. It is
The number of LITT surgeries has been gradually increas- likely that the observed underutilization is multifactorial,
ing, but numbers do not compensate for the decrease in the with a combination of inappropriate or delayed referrals for
number of resective surgeries, let alone other surgeries. Other surgical evaluation in persons with drug-resistant epilepsy,
than very small increases seen for LITT, intracranial elec- and the associated patient/caregiver and provider-reported
troencephalography, and responsive neurostimulation since barriers to epilepsy surgery, for example, minority race/
2010, most other surgical modalities have been generally de- ethnicity, lower income and Medicaid insurance status, age
creasing from 2010. The 2008 economic recession would not (>60 years old), misconceptions about epilepsy surgery risks,
be expected to affect the true number of candidates for epi- and psychiatric comorbidities. That we are seeing decreasing
lepsy surgery, but across every surgical type there is a drop trends of epilepsy surgery over this same period may point to
in frequencies from 2008 to 2009, with a subsequent rise in a lack of referral and underutilization problem.
numbers in 2010. This may be because during the recession Importantly, our study differs in several key ways from
fewer people had insurance and sought elective medical care the previous examination of national rates of epilepsy sur-
in addition to the adoption of Obamacare in 2010. It is likely gery through 2008.16 Ideally, the denominator for surgical
that these two factors combine to explain the sudden rise in rates would be patients with drug-resistant epilepsy, who
surgeries performed between 2009 and 2010. Moreover, the are potential candidates for resective surgery. Prior stud-
overall number of potential candidates for surgery has been ies have attempted to use “intractable localization related
increasing over time (Supplementary Table S2). This reflects epilepsy codes” (ICD-9-CM 345.41 or 345.51)16; however,
what the Centers for Disease Control and Prevention has these are known to be generally unreliable.23 Our study
shown, with the number of active epilepsy cases increasing uses total epilepsy discharges as the denominator for sur-
over time in US adults and children.19 In the USA, 40% of per- gical volume. Epilepsy, unlike epilepsy syndrome, is gen-
sons with epilepsy are drug-resistant.20 Despite the introduc- erally accurately coded in administrative data, and despite
tion of 20+ new antiseizure medication over several decades, multiple new medications introduced in the past 20 years,
|
6 KWON et al.
Mid-volume hospital,
Low-volume hospital, number of 1st quartile < number of High-volume hospital, number of
surgeries ≤ 1st quartile surgeries ≤ 4th quartile surgeries > 4th quartile
Ref
stable.24
.90
.04
—
—
Note: Unadjusted model tests association between discharge disposition and hospital volume without controlling for any other factors. Adjusted model adjusts for the following factors: age, expected primary payer, location,
P
In addition, when looking at health care outcomes as-
sociated with epilepsy surgery, we found that LV centers
are associated with higher complication and transfer rates.
—
—
greater length of inpatient stay. This is consistent with prior
data from a nonrepresentative subset of the adult population
including Centers for Medicare and Medicaid Services and
Ref
.68
.02
—
—
P
—
—
performed annually.
A recent study demonstrated the benefits of specialist
High-volume hospital
0.00%
0.00%
93.18%
6.82%
0.00%
0.00%
0.00%
13.60%
0.00%
0.00%
T A B L E 5 Surgical complications
greater number of patients on Medicare (who are thus older additional limitation of this kind of study is that there is no in-
and more likely to have medical comorbidities) are operated formation on disease severity; thus, we do not know whether,
in LV hospitals, which may account for this as a proxy. An for example, LV centers have people with better-controlled
KWON et al. 9
|
comorbidities compared to HV centers. In addition, admin- DATA AVAILABILIT Y STATEMENT
istrative claims data are produced for billing purposes, and HCUP data are publicly accessible. The data user agree-
therefore do not allow for a detailed examination of socioeco- ment limits release of data, and any requests should be
nomic background, health care attitudes, medication adher- made directly to HCUP. Analyses comply with HCUP
ence, or functional status, all of which might impact decisions regulations.
as to whether/what type of surgery to perform and surgical
complications. In addition, we do not have data about long- ORCID
term outcomes, including seizure freedom, which is the ulti- Churl-Su Kwon https://orcid.org/0000-0001-9904-2240
mate goal of these procedures. We used validated ICD-9-CM Leah Blank https://orcid.org/0000-0001-8719-6752
codes for epilepsy, but despite being widely used, these codes
have not been specifically validated in this population. R E F E R E NC E S
We present data on declining epilepsy surgery rates over 1. Kwan P, Brodie MJ. Early identification of refractory epilepsy. N
an 11-year period in which there was robust and increasingly Engl J Med. 2000;342:314–9.
2. Haneef Z, Stern J, Dewar S, Engel J Jr. Referral pattern for epilepsy
publicized evidence for the efficacy of the surgical treatment
surgery after evidence-based recommendations: a retrospective
of epilepsy. This is a concerning finding that suggests that
study. Neurology. 2010;75:699–704.
drug-resistant epilepsy continues to be undertreated despite 3. Wiebe S, Blume WT, Girvin JP, Eliasziw M, Effectiveness and
evidence and recommendations by national societies includ- Efficiency of Surgery for Temporal Lobe Epilepsy Study Group. A
ing the American Academy of Neurology and the American randomized, controlled trial of surgery for temporal-lobe epilepsy.
Epilepsy Society. Our data also provide initial evidence N Engl J Med. 2001;345:311–8.
highlighting the potential importance of specialization for 4. Engel J Jr, McDermott MP, Wiebe S, et al. Early surgical ther-
epilepsy surgery with lower cost, and fewer complications apy for drug-resistant temporal lobe epilepsy: a randomized trial.
JAMA. 2012;307:922–30.
seen at HV centers. Our findings suggest that epilepsy sur-
5. Jeha LE, Najm IM, Bingaman WE, et al. Predictors of outcome
gery may benefit from further specialization and reinforce
after temporal lobectomy for the treatment of intractable epilepsy.
the need to direct significant resources to the identification Neurology. 2006;66:1938–40.
of potential epilepsy surgical candidates and to reduce the 6. de Tisi J, Bell GS, Peacock JL, et al. The long-term outcome of
existing gap between recommended and actual care. adult epilepsy surgery, patterns of seizure remission, and relapse: a
cohort study. Lancet. 2011;378:1388–95.
ACKNOWLEDGMENTS 7. Simasathien T, Vadera S, Najm I, Gupta A, Bingaman W, Jehi L.
C-S.K. holds a Leon Levy Foundation Fellowship. N.J. is the Improved outcomes with earlier surgery for intractable frontal lobe
epilepsy. Ann Neurol. 2013;73:646–54.
Bludhorn Professor of International Medicine at the Icahn
8. Engel J Jr, Wiebe S, French J, et al. Practice parameter: temporal
School of Medicine at Mount Sinai. lobe and localized neocortical resections for epilepsy: report of the
Quality Standards Subcommittee of the American Academy of
CONFLICT OF INTEREST Neurology, in association with the American Epilepsy Society and
N.J. receives grant funding paid to her institution for the American Association of Neurological Surgeons. Neurology.
grants unrelated to this work from the National Institute of 2003;60:538–47.
Neurological Disorders and Stroke (NIH U24NS107201, NIH 9. Houchens RL, Ross DN, Elixhauser A, Jiang J.Nationwide inpa-
tient sample redesign: final report. April 4, 2014. Available at:
IU54NS100064) and Patient-Centered Outcomes Research
https://www.hcup-us.ahrq.gov/db/nation/nis/reports/NISRedesig
Institute. She receives an honorarium for her work as an
nFinalReport040914.pdf Accessed April 20, 2020.
Associate Editor of Epilepsia. None of the other authors has any 10. Kee VR, Gilchrist B, Granner MA, Sarrazin NR, Carnahan RM.
conflict of interest to disclose. We confirm that we have read the A systematic review of validated methods for identifying seizures,
Journal's position on issues involved in ethical publication and convulsions, or epilepsy using administrative and claims data.
affirm that this report is consistent with those guidelines. Pharmacoepidemiol Drug Saf. 2012;21(Suppl 1):183–93.
11. St Germaine-Smith C, Metcalfe A, Pringsheim T, et al.
ETHICAL PUBLICATION STATEMENT Recommendations for optimal ICD codes to study neurologic con-
ditions: a systematic review. Neurology. 2012;79:1049–55.
We confirm that we have read the Journal's position on issues
12. Vadera S, Griffith SD, Rosenbaum BP, et al. National trends and
involved in ethical publication and affirm that this report is
in-hospital complication rates in more than 1600 hemispherecto-
consistent with those guidelines. mies from 1988 to 2010. Neurosurgery. 2015;77(2):185–91; dis-
cussion 191.
STANDARD PROTOCOL APPROVAL S, REG- 13. Sharma M, Sonig A, Ambekar S, Nanda A. Discharge dispo-
ISTRATIONS, AND PATIENT CONSENT sitions, complications, and costs of hospitalization in spinal
Our Icahn School of Medicine at Mount Sinai Institutional cord tumor surgery: analysis of data from the United States
Review Board has reviewed and approved this project and Nationwide Inpatient Sample, 2003–2010. J Neurosurg Spine.
2014;20:125–41.
waived the need for human consent.
|
10 KWON et al.
14. Elixhauser A, Steiner C, Harris DR, Coffey RM. Comorbidity mea- National Surgical Quality Improvement Program analysis. J Clin
sures for use with administrative data. Med Care. 1998;36:8–27. Neurosci. 2016;31:106–11.
15. Austin PC. An introduction to propensity score methods for reduc- 23. Jette N, Reid AY, Quan H, Hill MD, Wiebe S. How accurate is ICD
ing the effects of confounding in observational studies. Multivariate coding for epilepsy? Epilepsia. 2010;51:62–9.
Behav Res. 2011;46:399–424. 24. Kalilani L, Sun X, Pelgrims B, Noack-Rink M, Villanueva V. The
16. Englot DJ, Ouyang D, Wang DD, Rolston JD, Garcia PA, Chang epidemiology of drug-resistant epilepsy: a systematic review and
EF. Relationship between hospital surgical volume, lobectomy meta-analysis. Epilepsia. 2018;59:2179–93.
rates, and adverse perioperative events at US epilepsy centers. J 25. Lowerison MW, Josephson CB, Jette N, et al. Association of levels
Neurosurg. 2013;118:169–74. of specialized care with risk of premature mortality in patients with
17. Rolston JD, Englot DJ, Knowlton RC, Chang EF. Rate and com- epilepsy. JAMA Neurol. 2019;76(11):1352.
plications of adult epilepsy surgery in North America: analysis of
multiple databases. Epilepsy Res. 2016;124:55–62.
SUPPORTING INFORMATION
18. Kinney MO, Brigo F. What can Google Trends and Wikipedia-
Pageview analysis tell us about the landscape of epilepsy surgery Additional supporting information may be found online in
over time? Epilepsy Behav. 2020;103:106533. the Supporting Information section.
19. Centers for Disease Control and Prevention. More Americans have ep-
ilepsy than ever before. Available at: https://www.cdc.gov/media/relea
ses/2017/p0810-epilepsy-prevalence.html Accessed April 20, 2020. How to cite this article: Kwon C-S, Blank L, Mu L,
20. Kobau R, Zahran H, Thurman DJ, et al. Epilepsy surveillance Jetté N. Trends in lobectomy/
among adults—19 States, Behavioral Risk Factor Surveillance amygdalohippocampectomy over time and the impact
System, 2005. MMWR Surveill Summ. 2008;57:1–20. of hospital surgical volume on hospitalization
21. Engel J Jr. What can we do for people with drug-resistant epilepsy?
outcomes: A population-based study. Epilepsia.
The 2016 Wartenberg Lecture. Neurology. 2016;87:2483–9.
2020;00:1–10. https://doi.org/10.1111/epi.16664
22. Cote DJ, Karhade AV, Larsen AM, Burke WT, Castlen JP, Smith
TR. United States neurosurgery annual case type and complication
trends between 2006 and 2013: an American College of Surgeons