Comparative effectiveness of treatments for cerebral arteriovenous malformations: trends in nationwide outcomes from 2000 to 2009

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Object

The development of multimodality approaches for the treatment of cerebral arteriovenous malformations (AVMs), including microsurgery, endovascular therapy, and radiosurgery, has shifted modern treatment paradigms in the last 10 years. This study examines these changes in detail from a nationwide perspective.

Methods

The authors examined data from 2001 to 2009 in the Nationwide Inpatient Sample (NIS) database, and they assessed the safety, quality, and cost-effectiveness, including the total number of discharges, discharge proportion, length of stay, and hospital charges. The authors also examined patient demographics (including age, sex, income level, and insurance), hemorrhage status at presentation, and trends in open surgical and endovascular treatment.

Results

A total of 33,997 inpatient admissions for patients with a primary diagnosis of intracranial AVM were identified, with a mean of 4191 patients admitted annually. The mean hospital charges increased 2-fold over the study period without significant differences in outcomes. There were substantial differences between surgical, endovascular, radiosurgical, and multimodality treatments. The proportion of AVMs treated microsurgically remained stable over this period, while the proportion treated endovascularly dramatically increased in size, and the data demonstrate important patient-level distinctions among groups. Outcomes and complication profiles were significantly different between treatment modalities and were impacted by age and hemorrhage status.

Conclusions

Charges associated with treatment of cerebral AVMs to the payer and society have increased dramatically over the first decade of the 21st century without clear improvements in quality parameters. However, analysis of the 3 primary treatment modalities has demonstrated differences and warrants further investigation to understand which patient population would benefit maximally from each. Unfortunately, with only imprecise measurements of quality in health care delivery, it remains imperative to develop national databases in which parameters, such as survival, functional outcomes, quality of life, and complication rates, can be assessed to examine the value of care delivered in a more meaningful way. Demonstrating an ever-increasing value of delivered health care will be imperative in our evolving health care system.

Abbreviations used in this paper:AVM = arteriovenous malformation; LOS = length of stay; NIS = Nationwide Inpatient Sample.

Object

The development of multimodality approaches for the treatment of cerebral arteriovenous malformations (AVMs), including microsurgery, endovascular therapy, and radiosurgery, has shifted modern treatment paradigms in the last 10 years. This study examines these changes in detail from a nationwide perspective.

Methods

The authors examined data from 2001 to 2009 in the Nationwide Inpatient Sample (NIS) database, and they assessed the safety, quality, and cost-effectiveness, including the total number of discharges, discharge proportion, length of stay, and hospital charges. The authors also examined patient demographics (including age, sex, income level, and insurance), hemorrhage status at presentation, and trends in open surgical and endovascular treatment.

Results

A total of 33,997 inpatient admissions for patients with a primary diagnosis of intracranial AVM were identified, with a mean of 4191 patients admitted annually. The mean hospital charges increased 2-fold over the study period without significant differences in outcomes. There were substantial differences between surgical, endovascular, radiosurgical, and multimodality treatments. The proportion of AVMs treated microsurgically remained stable over this period, while the proportion treated endovascularly dramatically increased in size, and the data demonstrate important patient-level distinctions among groups. Outcomes and complication profiles were significantly different between treatment modalities and were impacted by age and hemorrhage status.

Conclusions

Charges associated with treatment of cerebral AVMs to the payer and society have increased dramatically over the first decade of the 21st century without clear improvements in quality parameters. However, analysis of the 3 primary treatment modalities has demonstrated differences and warrants further investigation to understand which patient population would benefit maximally from each. Unfortunately, with only imprecise measurements of quality in health care delivery, it remains imperative to develop national databases in which parameters, such as survival, functional outcomes, quality of life, and complication rates, can be assessed to examine the value of care delivered in a more meaningful way. Demonstrating an ever-increasing value of delivered health care will be imperative in our evolving health care system.

Abbreviations used in this paper:AVM = arteriovenous malformation; LOS = length of stay; NIS = Nationwide Inpatient Sample.

The diagnosis and treatment of cerebral AVMs is an important component of modern neurosurgical care.18 Goals of care focus on prevention of hemorrhage, seizures, and neurological deficits associated with AVMs.14 The treatment of AVMs has increased in complexity with the development of multimodal approaches1 that involve open microsurgical excision,4 endovascular therapy,21 and radiosurgery.2,13 Each of these procedures has associated complications, with approximately 7.1% of surgical candidates, 6.6% of endovascular candidates, and 5.1% of radiosurgical candidates facing permanent neurological deficits after treatment.20 With such a dynamic treatment approach wherein each modality is associated with significant complications, constant assessment of clinical outcomes is imperative in determining which treatment options afford consistently superior outcomes and under what circumstances.

Several AVM grading schemes currently in use have shown that certain patient-level characteristics correlate with outcome after intervention and are used to guide therapeutic decisions in clinical practice. The Spetzler-Martin grading system19 and Lawton supplementary grading system12 together assess for the following 6 factors: size, location, and eloquence for the former and age, hemorrhage, and nidal compactness for the latter. Both have been validated for their utility in predicting surgical morbidity and have proven useful in clinical practice; however, these factors have not been assessed on a broader scale.

Given the variation in institutional demographics, assessing the comparative effectiveness of care delivery across institutions is imperative in ensuring that the highest quality of care is delivered consistently. To date, studies in the neurosurgical literature have almost exclusively examined the experiences at a single institution.20 These results, while helpful in delineating some of the trends, are highly variable from institution to institution and are difficult to generalize. A meta-analysis published in 2011 summarizes the results from these studies.20 Unfortunately, comprehensive assessments on a truly national scale remain sparse. Examining patient outcomes and hospital charges allows us to look at the value of health care provided, defined as the ratio of outcomes to costs. As we begin to look at the comparative effectiveness of these different modalities in treating AVMs, the value of care delivered will be an essential parameter to examine. National patient databases offer an unparalleled tool for assessing the efficacy of rapidly evolving therapeutic modalities. Herein, we use the database to assess the diagnosis and management of cerebral AVMs between 2000 and 2009,5 examining demographics, outcomes, and value over this period. Nationwide Inpatient Sample analyses have become increasingly important by enabling rapid evaluation of national trends in neurosurgery,6–11,15–17 and our findings establish a baseline of care for cerebral AVMs against which future innovations in care can be compared and assessed for efficacy.

Methods

Database

We obtained data from the NIS, a database sponsored by the Agency for Healthcare Research and Quality of the US Department of Health and Human Services under the Healthcare Cost and Utilization Project. The NIS is the largest national inpatient care database, representing approximately 20% of inpatient admissions to nonfederal hospitals in the US, with approximately 8 million annual discharges from 1004 hospitals in 37 states. We specifically analyzed data collected within this database between 2000 and 2009 to determine trends in admissions and treatments for cerebral AVMs.

Analysis

The NIS was queried for all hospital admissions with a primary diagnosis of intracranial AVM using the ICD-9-CM diagnosis code 747.81. Primary outcome measures within the database included the total number of discharges, LOS, hospital charges, and discharge proportion. The NIS delineates discharge as either mortality or discharge to one of a number of types of facilities by acuity of care. We used “routine discharge,” meaning discharge to home without services, as a surrogate for functional status. We examined primary patient demographics, including age, sex, and median household income for zip code. We also examined the payer demographic (Medicare, Medicaid, private insurance, or uninsured). Correlations between these demographic variables and the primary outcome measures were assessed using JMP and SAS software (version 9.1, SAS Institute, Inc.). We also examined trends in treatment by endovascular (ICD-9-CM principal procedure code 39.72) and open excision (ICD-9-CM principal procedure code 01.59). Statistical significance was evaluated using the Student t-test, Wilcoxon rank-sum test, Spearman rank correlation, analysis of variance (ANOVA), or logistic regression analysis as appropriate. A p value < 0.05 was considered statistically significant.

To control for the effects of medical comorbidities, we used the method of Elixhauser et al.3 using software provided by the Agency for Healthcare Research and Quality (http://www.hcup-us.ahrq.gov/toolssoftware/comorbidity/comorbidity.jsp). A comorbidities index was created by summing each of the categories, with possible values between 0 and 28. We identified and tabulated markers of potential adverse events as follows: implant complications (ICD-9-CM codes 996.2, 996.63, 996.75, and 996.79), accidental laceration (ICD-9-CM code 99.82), neurological complication (ICD-9-CM codes 997.00–997.09), pulmonary complications (ICD-9-CM codes 518.5, 518.81, 518.84, and 997.3), deep venous thrombosis complications (ICD-9-CM codes 415.11, 453.40, 453.8, and 453.9), cardiac complications (ICD-9-CM codes 997.1 and 41.0), renal complications (ICD-9-CM codes 584.5, 584.9, and 997.5), gastrointestinal complications (ICD-9-CM codes 008.45, 56.01, and 997.4), infectious complications (ICD-9-CM codes 595.0, 595.9, and 599.0), pneumonia (ICD-9-CM codes 48.1, 48.2, and 48.6), wound infection complications (ICD-9-CM codes 998.32, 998.51, 998.59, 998.6, 998.81, and 998.83), and decubitus ulcer (ICD-9-CM codes 707.01–707.09).

Results

Annual Discharges

A mean of 4191 patients were admitted annually with a primary diagnosis of AVM over the 10-year period from 2000 to 2009. The trend in annual admission rates is shown in Fig. 1A. Admissions ranged from 3503 in 2005 to 5209 in 2003. There was no statistically significant variation over this period of time as assessed by a year-to-year comparison.

Fig. 1.
Fig. 1.

A: Overall AVM admissions between 2001 and 2009. B: Annual mean hospital charges for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009. C: Discharge proportion for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009. D: Average LOS for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009

Length of Stay

The LOS ranged between 3.8 and 5.1 days over the 10-year period, with a mean LOS of 4.6 days with no statistically significant variation over this period of time as assessed by a year-to-year comparison. The trend in annual average LOS is shown in Fig. 1D.

Discharge Proportion

Discharge functional status was measured by “routine discharges.” The discharge proportion ranged between 83% and 87% from 2000 to 2009, with a mean discharge proportion of 84% (Fig. 1C). There was no statistically significant variation over this period of time, as assessed by a year-to-year comparison.

Hospital Charges

Mean hospital charges ranged from $42,853 in 2001 to $83,807 in 2009, an average annual increase of 8.1% (Fig. 1B). When adjusted for inflation, this amounts to a 41% increase over the study period, or a 5.8% increase per year over the nominal rate of inflation. Charges per day of care similarly increased by 60% over that period, from $8000/day in 2001 to $13,000/day in 2006. When adjusted for inflation, this amounts to a 43% increase, again a 5.8% increase per year over the nominal rate of inflation. This represents a statistically significant year-over-year increase in mean charges over this period, even after inflation adjustment (p < 0.05).

Patient Demographics

We further analyzed the total number of discharges, mean LOS, mean total charges, mean charges per day, and routine discharge percentage with respect to patient age, income, and sex. Data aggregated from 2001, 2003, and 2005 are represented in Table 1. A near majority (45%) of patients were between 18 and 44 years of age. Patients between 45 and 64 years of age comprised 30% of the total population but had the longest LOS and highest charges in 2001 and had the most dramatic decrease in both LOS and overall charges during the time period between 2001 and 2005. There were no statistically significant differences between any of the groups when examining mean charges per day. There were also no statistically significant differences between any of the variables when stratified by patient income or sex.

TABLE 1:

Demographics of patients admitted with a primary diagnosis of AVM*

Demographic ParameterTotal No. of Discharges (%)Mean LOS (days)Mean Charges ($)Mean Charges/Day ($)Admission From ED (%)Routine Discharge (%)
all discharges12,585 (100)4.447,68411,0032086
age group (yrs)
 1–171,899 (16)4.544,05010,2131111
 18–445,511 (45)3.947,08812,1561990
 45–643,692 (30)4.950,98510,8901784
 65–841,072 (9)4.940,2568,4893476
insurance
 Medicare1,572 (12)4.844,6689,9292977
 Medicaid1,916 (15)5.552,3019,7761981
 private7,752 (62)4.248,61211,9731588
 uninsured454 (4)4.132,7027,9724291
patient income
 low1,869 (22)4.348,32211,5491988
 not low6,474 (78)4.151,13912,4982086
* Data are aggregated from 2001, 2003, and 2005. Abbreviation: ED = emergency department.

Payer Demographics

We analyzed the total number of discharges, mean LOS, mean total charges, mean charges per day, and routine discharge percentage with respect to payer (Medicare, Medicaid, private insurance, or uninsured). Data aggregated from 2001, 2003, and 2005 are presented in Table 1. Significant differences were noted among payer types for all of the primary outcome measures. The majority of cases represented private insurance payers (62%), with Medicaid representing 15%, Medicare representing 12%, and the uninsured representing 4%. By comparison, LOS for Medicare patients was 4.8 days, and that for Medicaid patients was 5.5 days (p < 0.05). The mean charges per day of stay were highest for the private insurance carriers and lowest for the uninsured population (p < 0.05). The Medicare and Medicaid population had the lowest discharge percentage, while the private insurance carriers and the uninsured had a statistically significant higher proportion of discharges (p < 0.05).

Treatment

A mean of 1232 patients with AVMs were treated annually with open excision. The trend in the proportion of AVMs treated by open excision is shown in Fig. 2A. There was an initial decline in the overall proportion treated with excision over the first half of the decade, with increased surgical management in the latter half. Concurrently, the proportion of endovascular interventions increased rapidly over the first half of the study period from 2.6% in 2000 to 36.6% in 2005 (p < 0.05), with modest decline toward the end of the decade.

Fig. 2.
Fig. 2.

A: Proportion of AVMs treated with open surgery, endovascular treatment, radiosurgery, or observation by year. B: Proportion of AVMs treated with open excision, endovascular treatment, radiosurgery, or observation stratified by age group. C: Median total charges by year for open surgery, endovascular, radiosurgery, or observation from 2000 to 2009.

We were further able to analyze treatment trends by stratifying on patient demographic, as shown in Fig. 2B. The distribution of treatments correlates closely with age with several clear trends observed when stratified as follows: younger than 18 years, 18–44 years, and 45 years or older. Both open surgery and radiosurgery had the highest rates among the young, at 40% and 4%, respectively. These proportions decrease linearly across age strata to 32% and 2%, respectively (p > 0.05). In contrast, endovascular treatments show a countercurrent trend, increasing in frequency as age increases, from 21% in the youngest strata to 26% in the oldest (p < 0.05). There was no statistically significant correlation between patient income or sex and treatment modality. Total hospital charges also showed distinct trends, overall increasing over the course of the decade for all treatment modalities (Fig. 2C). Open surgery increased the fastest with peak median charges occurring in 2007, with subsequent regression, yielding an overall yearly average growth rate of 9.18% (p < 0.05). Endovascular treatments likewise increased at 8.63% yearly, and radiosurgery remained relatively constant given inflation at a yearly growth of 3.31%.

Regional Variation

The NIS database also groups patient data according to 4 regions of the US: Northeast, Midwest, West, and South. Among these regions, there was no significant difference in LOS for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2006. However, there was a statistically significant difference in mean hospital charges, ranging from $38,000 in the Northeast to $78,000 in the West (p < 0.05).

Comparative Effectiveness of Treatments

We evaluated the comparative effectiveness of treatments by analyzing our primary outcomes measures, in-hospital mortality, LOS, routine discharge, and total charges, while controlling for both patient and hospital factors (Table 2). We stratified by presence of subarachnoid or intracerebral hemorrhage and by age according to the supplemental grading scheme for each treatment modality, including uni- and multimodal approaches. We assessed the impact of these factors by univariate and multivariate analysis and found that several patient-level factors were significant predictors of outcome (Table 3). Figure 3 illustrates the impact of age and hemorrhage status on each of the primary outcome measures.

TABLE 2:

Outcomes of patients treated with open surgery, endovascular therapy, radiosurgery, or combination therapy with a primary diagnosis of AVM from 2000 to 2009 stratified by presentation hemorrhage status*

OutcomeTreatmentp Value
OpEndoSRSOp + EndoEndo + SRSOp + SRSOp + Endo + SRSOp + AngioNone
unruptured
 in-hospital mortality (%)1.01.60.00.00.0NANA0.50.7<0.01
 mean LOS (days)5.45 ± 0.222.49 ± 0.111.37 ± 0.158.36 ± 0.452.70 ± 1.54NANA5.80 ± 0.183.45 ± 0.09<0.01
 routine discharge (%)67.593.498.975.9100NANA83.872.9<0.01
 mean total charges ($)57,062 ± 1,60049,839 ± 1,30145,393 ± 1,422109,467 ± 4,86149,172 ± 11,005NANA63,945 ± 2,01122,946 ± 611<0.01
ruptured
 in-hospital mortality (%)6.610.6NA10.3NANANA2.93.1<0.01
 mean LOS (days)11.86 ± 1.2010.59 ± 1.69NA26.11 ± 6.42NANANA15.78 ± 1.846.98 ± 0.63<0.01
 routine discharge (%)42.556.7NA36.0NANANA49.038.7<0.01
 mean total charges ($)105,339 ± 11,668127,652 ± 18,269NA220,115 ± 26,696NANANA138,713 ± 13,95655,553 ± 5,946<0.01
* Mean values are represented as the mean ± SE. Abbreviations: Angio = angiography; Endo = endovascular treatment; NA = not available; SRS = stereotactic radiosurgery.
TABLE 3:

Results of multivariate modeling of patient-level factors as predictors of mortality, length of stay, discharge proportion, and total charges*

Patient Characteristicsp Value
MortalityLOSTotal ChargesDischarge Proportion
admission source0.00170.3910.00010.0049
admission type0.00010.00170.72210.4442
sex0.56360.06550.54730.0423
elective0.00010.31980.59460.0863
comorbidity index0.17230.00010.00010.0001
age0.0030.00860.11730.0001
hemorrhage0.00010.00010.00010.0001
* Values in bold face are statistically significant.
Fig. 3.
Fig. 3.

Comparison of outcomes measures, mortality (A and B), LOS (C and D), discharge proportion (E and F), and total charges (G and H), stratified by age and hemorrhage status at presentation. Angio = angiography; Endo = endovascular; Obs = observation; SRS = stereotactic radiosurgery; Surg = surgery.

Among patients in whom the AVM did not rupture, those treated radiosurgically fared best with no reported mortalities, the lowest LOS (1.37 days), and the highest discharge proportion (98.9%). By comparison, patients treated endovascularly had the highest mortality rate (1.6%), and yet had a relatively low LOS index (2.49 days) and a high discharge proportion (93.4%). Patients treated surgically tended to remain in the hospital longer (5.45 days [surgery] and 8.36 days [surgery plus endovascular treatment], p > 0.05), and had lower discharge proportions (67.5% [surgery] and 75.9% [surgery plus endovascular treatment], p > 0.05). Patients who underwent surgery and angiography had very low mortality (0.45%) and an improved discharge proportion (83.8%).

Patients experiencing AVM rupture had very different outcomes. In general, their mortality and LOS were significantly higher than for equivalent unruptured patients. Those who underwent embolization had the highest mortality (10.6% [endovascular treatment] and 10.3% [endovascular treatment plus surgery]), which is nearly 60% higher than the next highest (6.6% [surgery], p < 0.05). Surgery plus angiography had the lowest mortality rate at 2.87%. Those who underwent surgery plus endovascular treatment had the worst outcomes profile, with all indices significantly worse than those who had no treatment at all (p < 0.05 for each index). The presence of any procedure significantly increased LOS (6.98 days [no therapy] and > 10.5 days [all therapies], p > 0.05). Hemorrhage was correlated with higher charges (p > 0.05), on average doubling charges for each treatment category. There were too few radiosurgical cases to include in these analyses.

We analyzed admissions for comorbid conditions, procedures, and potential adverse events (Table 4). Hemorrhage and procedures performed were the most important factors in predicting complication rates. Although patients who suffered AVM rupture had overall higher complication rates, the change was largest for extraventricular drain usage and pulmonary complications, averaging a nearly 10-fold increase across treatment modalities. Comparing treatments, patients who underwent surgery were 4 times as likely to undergo ventriculostomy (3.74% vs 0.85% [endovascular treatment], p < 0.01). Surgically treated patients also experienced potential adverse events at much higher rates than both other groups of patients, including pulmonary, venous thromboembolism, cardiac, renal, gastrointestinal, infectious, pneumonia, and wound complications (p < 0.01). The 2 types of complications wherein surgical patients did not have significantly difference rates were for implant complications and accidental puncture/laceration.

TABLE 4:

Complications and associated procedures for patients admitted with a primary diagnosis of AVM from 2000 to 2009 by treatment modality and stratified by presentation hemorrhage status*

InterventionComplications & Associated Procedures Rates (%)
EVDImpLacPulmDVTCardRenalGIInfectPNAWound
unruptured
 no Tx0.630.260.211.410.310.090.720.382.580.830
 op2.830.710.412.980.270.880.430.682.090.750.86
 endo0.120.290.411.320.120.310.060.371.130.130
 SRS00.510000000.5500
 op + endo1.800.331.014.881.011.4101.024.790.661.08
 op + angio2.270.110.593.510.960.250.260.831.691.550.11
ruptured
 no Tx10.490.9205.901.2300.460.846.240.410
 op11.701.63012.630.800.7501.782.455.112.50
 endo16.842.593.8113.061.42001.349.346.810
 SRS00000000000
 op + endo18.022.342.5533.1914.204.6706.4215.399.322.34
 op + angio15.420.85011.300.891.792.023.759.252.820.89
* Card = cardiac; DVT = deep venous thrombosis; EVD = external ventricular drainage; GI = gastrointestinal; Imp = implant; Infect = infection; Lac = laceration; PNA = pneumonia; Pulm = pulmonary; TX = treatment.

Analysis of admission type and source of admission also revealed differences (Table 5), potentially indicative of patient demographics and severity of illness. Radiosurgically treated patients were the youngest contingent at 34.1 years (p < 0.01). Those admitted through the emergency room or transferred urgently were nearly twice as likely to undergo surgery over endovascular treatment (8% vs 4%, p < 0.01) and 4 times more likely to undergo surgery than radiosurgery (8% vs 2%, p < 0.01). Patients admitted on Saturday or Sunday were also more likely to receive surgical than endovascular (5.21% vs 1.94%, p < 0.01) or radiosurgical (0.53%, p < 0.01) therapy.

TABLE 5:

Admission characteristics of patients treated with open surgery, endovascular therapy, and radiosurgery with a primary diagnosis of AVM from 2000 to 2009*

CharacteristicTreatmentp Value
OpEndoSRS
admission source (%)
 routine869095<0.01
 ED842<0.01
admission type (%)
 elective767891<0.01
 emergency1383<0.01
weekend (%)5.211.940.53<0.01
mean age (yrs)37.4 ± 0.440.2 ± 0.434.1 ± 1.3<0.01
* Mean values are ± SE.

Discussion

The treatment of cerebral AVMs over the first decade of the 21st century has rapidly evolved with the advent of multimodality therapies, including open excision, endovascular treatment, and radiosurgery, and such advances continue to shape our treatment approach. Examining trends in parameters of care and patient outcomes is imperative in any period of rapid evolution in treatment, and enables us to assess how well new therapies meet the underlying goals of care, including safety, efficacy, and cost-effectiveness. This analysis has demonstrated several important trends.

Over this period of 9 years, the total charges for care and cost per day of care have increased for all, both averaging 5.8% increases yearly over the nominal rate of inflation. This is in line with general medical inflation as assessed by other high-resource procedures such as coronary artery bypass grafting and hip replacement surgeries (ICD-9-CM 36.11 [5.4%] and ICD-9-CM 81.51 [3.4%]). However, stratification of the data by procedure performed and hemorrhage status shows that both of these variables significantly impact costs. If we define value as the ratio of unit of outcome received per unit of cost, we find that the most resource-intensive therapy, surgery plus endovascular treatment for patients with hemorrhage, shows a distinct decrease in value received for care delivered and should therefore be critically evaluated on a case-by-case basis to determine if expected benefit is worthwhile given the high rates of poor outcome.

The comparative effectiveness of the treatment modalities can be assessed on a nationwide basis. The proportion of AVMs treated with microsurgical excision has remained relatively constant over this period of time. However, the data show tremendous and durable expansion in the proportion of AVMs treated endovascularly, either alone or in combination. There is a statistically significant decrease in the proportion of patients treated with open microsurgical excision of the AVM as patient age increases. This trend also correlates with the most dramatic decrease in overall LOS among the 45- to 64-year-old age group, suggesting that there may be a parallel between the adoption of endovascular modalities for AVMs and decrease in LOS. Microsurgical treatment remains the most common treatment for patients admitted urgently, such as those admitted over weekends or through the emergency room or emergency transfers. The prevalence of surgery among these patients is at least in part an indicator of severity of disease, such as patients who require emergency decompression. Furthermore, patients with poor access to care tend to be overrepresented in these emergency care categories. Their access to procedures typically offered on an outpatient basis, such as radiosurgery, is diminished, even if their disease could have been adequately managed through that modality.

These data suggest that the choice of therapy should be considered carefully and independently for patients regardless of rupture status (ruptured or unruptured). In both cases, surgery plus angiography is associated with the most favorable outcomes, and on a value basis is the superior choice. One surprising finding was that patients who received what many consider “maximal therapy,” consisting of surgery plus endovascular therapy, experienced the worst suite of outcomes and represent the worst value proposition. These patients had poor immediate outcomes at discharge at nearly twice the costs for patients regardless of rupture status. It is notable that embolization, either alone or in combination, was linked with substantially increased mortality risk, and for this reason should be undertaken with care and full knowledge of implications. Furthermore, embolization is associated with additional days of stay and substantial charges, and yet it adds little to improve outcome. On a larger scale, real costs related to the care of patients who underwent surgery plus endovascular treatment are likely higher given that among those who survive, fewer go home at discharge and likely incur substantial additional costs for long-term care and rehabilitation.

The data presented suggest that patient-level data may be useful when considering the choice of treatment regimens. Indeed, hemorrhage status figures prominently in our outcomes analyses, with presence of hemorrhage universally connected with poorer outcomes. Age also had a prominent effect, but the direction of the effect was less consistent. Age and hemorrhage have also been shown to correlate with surgical outcome in the Lawton supplementary grading system.12 Other factors commonly used in grading schemes, size, location, eloquence, and nidal compactness, are not directly obtainable from such national data sets. Based on the senior author's (M.T.L.) approach to triage and treatment of AVMs, it seems likely that universus multimodal treatment may act as a surrogate for the complexity of the lesion. More complex lesions tend to require additional interventions, such as embolization, to reduce risk to the patient prior to resection. We anticipate that further assessment of these patient-level factors in more detailed institutional and multiinstitutional data sets will bear out these findings.

There are limitations inherent to the data source. It is not possible to assess the relative superiority of treatment modalities from the data analyzed. Rather, the analyses are designed to evaluate associations between treatments and certain outcome measures. It is not possible to discern causality from the results.

It is impossible to know what proportion of patients who underwent endovascular therapy were treated with the goal of cure compared with those who underwent partial embolization prior to adjuvant therapies on separate hospital admissions. Conversely, in patients who underwent multiple inpatient procedures, we cannot accurately attribute adverse outcome events to a given intervention. For instance, the data clearly demonstrate that ventriculostomy among patients undergoing surgery is 4 times more prevalent, but we cannot know if patients had more severe presentations requiring presurgical treatment or whether the need for ventriculostomy was a result of the surgical intervention. Surgery plus endovascular therapy for patients in whom the AVM has ruptured also demonstrated poor outcomes at high cost, or extremely low value, but since the data source does not allow us to easily control for severity of presenting disease, it is possible that this therapy option acts as a surrogate for extremely high-risk lesions that would have poor outcome regardless of therapy chosen. Analysis of admission type and source likewise revealed significant differences between the patient populations that could be indicative of patient demographics and the severity of their presenting condition.

Not all therapies are completed in a single hospitalization. Tracking individual patients across multiple hospital admissions could alleviate some of these limitations. However, these data have been de-identified, and only a small subset of states provide patient-level identifiers to allow researchers to track readmissions, so a nationwide analysis of questions related to subsequent admissions is not possible. In the case of radiosurgery, admission may not require admission universally, and in fact admission may be a marker of complication or severity of disease. Even if this sample is biased to be sicker than the average patient undergoing radiosurgery, in which case the patient is likely to be an outpatient, these patients still perform better than those who undergo other types of treatment in terms of outcomes. Although evaluation of a more representative sample including outpatients would require different outcomes metrics, it is anticipated that these outcomes would be more positive than those reported here, and as such the bias is acceptable.

Finally, the extent to which the care parameters we examined reflect the goals of care that patients and society have in AVM management remains uncertain. Parameters such as complete AVM obliteration, survival, functional outcomes, quality of life, and complication rates, among others, must be assessed to really examine the value of care delivered in a meaningful way. These data are unfortunately not tabulated on a national level. It is critical that we develop nationally coordinated databases to facilitate long-term study of care management in a way that will more closely reflect goals of care and enable us to truly evaluate the safety, efficacy, and cost-efficiency of care parameters in a manner that provides value and utility to patients and society. Importantly, from the neurosurgical standpoint, this may be particularly feasible in a small field such as neurosurgery, where national coordination may be somewhat easier than in larger fields.

Conclusions

Charges for treating cerebral AVMs have increased dramatically over the first decade of the 21st century: 5.8% annually over the rate of nominal inflation during that period of time. However, cost-efficiency is more important than cost of care. Although it is more difficult to ascertain, cost per unit of value derived is a more appropriate parameter. Data sources such as the NIS allow for analysis of comparative effectiveness as well as comparative cost-efficiency of multiple alternative treatments across a nationwide landscape. This analysis provides a first look at national trends in AVM management from the standpoint of safety, efficacy, and cost-efficiency of care. We demonstrate that there are differences among treatment modalities that can significantly influence patient outcomes. The surgeon's choice of therapies must be undertaken with great care and a clear understanding of anticipated benefits and their attendant risks to the patient.

Disclosure

Dr. Lawton receives royalties from Mizuo America, Inc.

Author contributions to the study and manuscript preparation include the following. Conception and design: Davies. Acquisition of data: Davies. Analysis and interpretation of data: all authors. Drafting the article: all authors. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Statistical analysis: Davies, Yanamadala. Administrative/technical/material support: Lawton. Study supervision: Lawton.

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  • 2

    Blamek STarnawski RMiszczyk L: Linac-based stereotactic radiosurgery for brain arteriovenous malformations. Clin Oncol (R Coll Radiol) 23:5255312011

    • Search Google Scholar
    • Export Citation
  • 3

    Elixhauser ASteiner CHarris DRCoffey RM: Comorbidity measures for use with administrative data. Med Care 36:8271998

  • 4

    Hernesniemi JRomani RLehecka MIsarakul PDashti RCelik O: Present state of microneurosurgery of cerebral arteriovenous malformations. Acta Neurochir Suppl 107:71762010

    • Search Google Scholar
    • Export Citation
  • 5

    Houchens RElixhauser A: HCUP Methods Series Report #2003-2 Calculating Nationwide Inpatient Sample Variances Rockville, MDHealthcare Cost and Utilization Project, Agency for Healthcare Research and Quality2005. (http://www.hcup-us.ahrq.gov/reports/methods/CalculatingNISVariances200106092005.pdf) [Accessed May 25 2012]

    • Search Google Scholar
    • Export Citation
  • 6

    Kalanithi PSchubert RDLad SPHarris OABoakye M: Hospital costs, incidence, and inhospital mortality rates of traumatic subdural hematoma in the United States. Clinical article. J Neurosurg 115:101310182011

    • Search Google Scholar
    • Export Citation
  • 7

    Lad SPKalanithi PSPatil CGItthimathin PBatya SBronte-Stewart H: Socioeconomic trends in deep brain stimulation (DBS) surgery. Neuromodulation 13:1821862010

    • Search Google Scholar
    • Export Citation
  • 8

    Lad SPNathan JKSchubert RDBoakye M: Trends in median, ulnar, radial, and brachioplexus nerve injuries in the United States. Neurosurgery 66:9539602010

    • Search Google Scholar
    • Export Citation
  • 9

    Lad SPPatil CGBerta SSantarelli JGHo CBoakye M: National trends in spinal fusion for cervical spondylotic myelopathy. Surg Neurol 71:66692009

    • Search Google Scholar
    • Export Citation
  • 10

    Lad SPPatil CGLad EMHayden MGBoakye M: National trends in vertebral augmentation procedures for the treatment of vertebral compression fractures. Surg Neurol 71:5805852009

    • Search Google Scholar
    • Export Citation
  • 11

    Lad SPSantarelli JGPatil CGSteinberg GKBoakye M: National trends in spinal arteriovenous malformations. Neurosurg Focus 26:1E102009

    • Search Google Scholar
    • Export Citation
  • 12

    Lawton MTKim HMcCulloch CEMikhak BYoung WL: A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:7027132010

    • Search Google Scholar
    • Export Citation
  • 13

    Lunsford LDKano HKondziolka DYang HCFlannery TJAwan NR: Stereotactic radiosurgery as the initial management for Spetzler-Martin Grade I or II arteriovenous malformations. J Neurosurg 115:A4202011. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 14

    Ogilvy CSStieg PEAwad IBrown RD JrKondziolka DRosenwasser R: AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Stroke 32:145814712001

    • Search Google Scholar
    • Export Citation
  • 15

    Patil CGAlexander ALGephart MGLad SPArrigo RTBoakye M: A population based study of inpatient outcomes after operative management of non-traumatic intracerebral hemorrhage in the United States. World Neurosurg [epub ahead of print]2011

    • Search Google Scholar
    • Export Citation
  • 16

    Patil CGLad SPHarsh GRLaws ER JrBoakye M: National trends, complications, and outcomes following transsphenoidal surgery for Cushing's disease from 1993 to 2002. Neurosurg Focus 23:3E72007

    • Search Google Scholar
    • Export Citation
  • 17

    Patil CGSantarelli JLad SPHo CTian WBoakye M: Inpatient complications, mortality, and discharge disposition after surgical correction of idiopathic scoliosis: a national perspective. Spine J 8:9049102008

    • Search Google Scholar
    • Export Citation
  • 18

    Sandalcioglu IEWanke IZappala VForsting MSure U: The management of arteriovenous malformations. J Neurosurg Sci 55:57692011

    • Search Google Scholar
    • Export Citation
  • 19

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 20

    van Beijnum Jvan der Worp HBBuis DRAl-Shahi Salman RKappelle LJRinkel GJ: Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306:201120192011

    • Search Google Scholar
    • Export Citation
  • 21

    Yashar PAmar APGiannotta SLYu CPagnini PGLiu CY: Cerebral arteriovenous malformations: issues of the interplay between stereotactic radiosurgery and endovascular surgical therapy. World Neurosurg 75:6386472011

    • Search Google Scholar
    • Export Citation

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Article Information

Contributor Notes

Address correspondence to: Michael T. Lawton, M.D., Department of Neurological Surgery, University of California, San Francisco, 505 Parnassus Avenue, M780, Box 0112, San Francisco, California 94143-0112. email: lawtonm@neurosurg.ucsf.edu.Please include this information when citing this paper: DOI: 10.3171/2012.5.FOCUS12107.

© AANS, except where prohibited by US copyright law.

Headings
Figures
  • View in gallery

    A: Overall AVM admissions between 2001 and 2009. B: Annual mean hospital charges for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009. C: Discharge proportion for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009. D: Average LOS for patients admitted with a primary diagnosis of cerebrovascular anomaly between 2001 and 2009

  • View in gallery

    A: Proportion of AVMs treated with open surgery, endovascular treatment, radiosurgery, or observation by year. B: Proportion of AVMs treated with open excision, endovascular treatment, radiosurgery, or observation stratified by age group. C: Median total charges by year for open surgery, endovascular, radiosurgery, or observation from 2000 to 2009.

  • View in gallery

    Comparison of outcomes measures, mortality (A and B), LOS (C and D), discharge proportion (E and F), and total charges (G and H), stratified by age and hemorrhage status at presentation. Angio = angiography; Endo = endovascular; Obs = observation; SRS = stereotactic radiosurgery; Surg = surgery.

References
  • 1

    Barr JCOgilvy CS: Selection of treatment modalities or observation of arteriovenous malformations. Neurosurg Clin N Am 23:63752012

    • Search Google Scholar
    • Export Citation
  • 2

    Blamek STarnawski RMiszczyk L: Linac-based stereotactic radiosurgery for brain arteriovenous malformations. Clin Oncol (R Coll Radiol) 23:5255312011

    • Search Google Scholar
    • Export Citation
  • 3

    Elixhauser ASteiner CHarris DRCoffey RM: Comorbidity measures for use with administrative data. Med Care 36:8271998

  • 4

    Hernesniemi JRomani RLehecka MIsarakul PDashti RCelik O: Present state of microneurosurgery of cerebral arteriovenous malformations. Acta Neurochir Suppl 107:71762010

    • Search Google Scholar
    • Export Citation
  • 5

    Houchens RElixhauser A: HCUP Methods Series Report #2003-2 Calculating Nationwide Inpatient Sample Variances Rockville, MDHealthcare Cost and Utilization Project, Agency for Healthcare Research and Quality2005. (http://www.hcup-us.ahrq.gov/reports/methods/CalculatingNISVariances200106092005.pdf) [Accessed May 25 2012]

    • Search Google Scholar
    • Export Citation
  • 6

    Kalanithi PSchubert RDLad SPHarris OABoakye M: Hospital costs, incidence, and inhospital mortality rates of traumatic subdural hematoma in the United States. Clinical article. J Neurosurg 115:101310182011

    • Search Google Scholar
    • Export Citation
  • 7

    Lad SPKalanithi PSPatil CGItthimathin PBatya SBronte-Stewart H: Socioeconomic trends in deep brain stimulation (DBS) surgery. Neuromodulation 13:1821862010

    • Search Google Scholar
    • Export Citation
  • 8

    Lad SPNathan JKSchubert RDBoakye M: Trends in median, ulnar, radial, and brachioplexus nerve injuries in the United States. Neurosurgery 66:9539602010

    • Search Google Scholar
    • Export Citation
  • 9

    Lad SPPatil CGBerta SSantarelli JGHo CBoakye M: National trends in spinal fusion for cervical spondylotic myelopathy. Surg Neurol 71:66692009

    • Search Google Scholar
    • Export Citation
  • 10

    Lad SPPatil CGLad EMHayden MGBoakye M: National trends in vertebral augmentation procedures for the treatment of vertebral compression fractures. Surg Neurol 71:5805852009

    • Search Google Scholar
    • Export Citation
  • 11

    Lad SPSantarelli JGPatil CGSteinberg GKBoakye M: National trends in spinal arteriovenous malformations. Neurosurg Focus 26:1E102009

    • Search Google Scholar
    • Export Citation
  • 12

    Lawton MTKim HMcCulloch CEMikhak BYoung WL: A supplementary grading scale for selecting patients with brain arteriovenous malformations for surgery. Neurosurgery 66:7027132010

    • Search Google Scholar
    • Export Citation
  • 13

    Lunsford LDKano HKondziolka DYang HCFlannery TJAwan NR: Stereotactic radiosurgery as the initial management for Spetzler-Martin Grade I or II arteriovenous malformations. J Neurosurg 115:A4202011. (Abstract)

    • Search Google Scholar
    • Export Citation
  • 14

    Ogilvy CSStieg PEAwad IBrown RD JrKondziolka DRosenwasser R: AHA Scientific Statement: Recommendations for the management of intracranial arteriovenous malformations: a statement for healthcare professionals from a special writing group of the Stroke Council, American Stroke Association. Stroke 32:145814712001

    • Search Google Scholar
    • Export Citation
  • 15

    Patil CGAlexander ALGephart MGLad SPArrigo RTBoakye M: A population based study of inpatient outcomes after operative management of non-traumatic intracerebral hemorrhage in the United States. World Neurosurg [epub ahead of print]2011

    • Search Google Scholar
    • Export Citation
  • 16

    Patil CGLad SPHarsh GRLaws ER JrBoakye M: National trends, complications, and outcomes following transsphenoidal surgery for Cushing's disease from 1993 to 2002. Neurosurg Focus 23:3E72007

    • Search Google Scholar
    • Export Citation
  • 17

    Patil CGSantarelli JLad SPHo CTian WBoakye M: Inpatient complications, mortality, and discharge disposition after surgical correction of idiopathic scoliosis: a national perspective. Spine J 8:9049102008

    • Search Google Scholar
    • Export Citation
  • 18

    Sandalcioglu IEWanke IZappala VForsting MSure U: The management of arteriovenous malformations. J Neurosurg Sci 55:57692011

    • Search Google Scholar
    • Export Citation
  • 19

    Spetzler RFMartin NA: A proposed grading system for arteriovenous malformations. J Neurosurg 65:4764831986

  • 20

    van Beijnum Jvan der Worp HBBuis DRAl-Shahi Salman RKappelle LJRinkel GJ: Treatment of brain arteriovenous malformations: a systematic review and meta-analysis. JAMA 306:201120192011

    • Search Google Scholar
    • Export Citation
  • 21

    Yashar PAmar APGiannotta SLYu CPagnini PGLiu CY: Cerebral arteriovenous malformations: issues of the interplay between stereotactic radiosurgery and endovascular surgical therapy. World Neurosurg 75:6386472011

    • Search Google Scholar
    • Export Citation
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