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. Author manuscript; available in PMC: 2016 Sep 1.
Published in final edited form as: Am Heart J. 2015 Jun 11;170(3):447–454.e18. doi: 10.1016/j.ahj.2015.06.004

The design and implementation of a new surveillance system for venous thromboembolism using combined active and passive methods

Aaron M Wendelboe a, Janis Campbell a, Micah McCumber a, Dale Bratzler a, Kai Ding a, Michele Beckman b, Nimia Reyes b, Gary Raskob a
PMCID: PMC4598067  NIHMSID: NIHMS726735  PMID: 26385027

Abstract

Estimates of venous thromboembolism (VTE) incidence in the United States are limited by lack of a national surveillance system. We implemented a population-based surveillance system in Oklahoma County, OK, for April 1, 2012 to March 31, 2014, to estimate the incidences of first-time and recurrent VTE events, VTE-related mortality, and the proportion of case patients with provoked versus unprovoked VTE. The Commissioner of Health made VTE a reportable condition and delegated surveillance-related responsibilities to the University of Oklahoma, College of Public Health. The surveillance system included active and passive methods. Active surveillance involved reviewing imaging studies (such as chest computed tomography and compression ultrasounds) from all inpatient and outpatient facilities. Interrater agreement between surveillance officers collecting data was assessed using κ. Passive surveillance used International Classification of Disease, Ninth Revision (ICD-9) codes from hospital discharge data to identify cases. The sensitivity and specificity of various ICD-9–based case definitions will be assessed by comparison with cases identified through active surveillance. As of February 1, 2015, we screened 54,494 (99.5%) of the imaging studies and identified 2,725 case patients, of which 91.6% were from inpatient facilities, and 8.4% were from outpatient facilities. Agreement between surveillance officers was high (κ ≥0.61 for 93.2% of variables). Agreement for the diagnosis of pulmonary embolism and diagnosis of deep vein thrombosis was κ = 0.92 (95% CI 0.74-1.00) and κ = 0.89 (95% CI 0.71-1.00), respectively. This surveillance system will provide data on the accuracy of ICD-9–based case definitions for surveillance of VTE events and help the Centers for Disease Control and Prevention develop a national VTE surveillance system.


The US Surgeon General’s 2008 “Call to Action to Prevent Deep Vein Thrombosis (DVT) and Pulmonary Embolism (PE)”1 raised the importance of conducting surveillance for venous thromboembolism (VTE). Current estimates of the burden of VTE in the United States (350,000-900,000 events and 100,000-300,000 deaths annually) come from 2 principal sources. The first is cohort studies in selected counties and then generalized to the US population.2,3 The second is administrative claims data.4-8 Both of these methods have limitations. The estimates from the cohort studies come from a largely white population and may not be representative of the diversity of the US population. Although the inclusion of present on admission (POA) codes has increased the positive predictive value of International Classification of Disease, Ninth Revision, Clinical Modification (ICD-9 CM) codes to identify inpatient VTE cases,6 there are remaining limitations in using administrative data to document cases of VTE because (1) coding may reflect old diagnoses that are no longer active diagnoses, (2) coding practices vary between facilities, (3) the inability of deidentified data to differentiate between incident and recurrent events and between incident events and duplicate events caused by patient transfers, (4) the inability to determine dates of diagnosis (traditionally based on facility discharge dates), (5) nonhospitalized patients and those who had sudden death from PE have usually not been included in these estimates, and (6) the ideal case definition using selected ICD-9 CM codes has not been established given the varying performance of VTE-related ICD-9 CM codes.

In addition to removing the uncertainty in the estimates of VTE incidence, other aspects of the epidemiology of VTE disease would also be informed by improved surveillance. For example, it is difficult to differentiate between provoked and unprovoked events. Although certain strong risk factors have been well established, such as surgery, hospitalization, and cancer, a large number of patients experience VTE in the absence of an identifiable risk factor (ie, unprovoked VTE). The racial and ethnic distribution of VTE events in the United States, for both provoked and unprovoked events, remains incompletely understood. In addition, contemporary data are needed on the utilization of appropriate prophylaxis against VTE in patients at risk and to document the proportion of VTE events, which may have been potentially preventable.

Venous thromboembolism is a condition well suited for surveillance using modern techniques and diagnostic imaging. Because a diagnosis of DVT or PE based solely on the evaluation of clinical signs has proven unreliable, imaging studies are required for accurate diagnosis.9 Noninvasive and highly sensitive and specific diagnostic procedures, including computed tomography angiography (CTA) for PE and compression ultrasound (CUS) for DVT, are routinely used in clinical practice for the diagnosis of VTE. Thus, the College of Public Health at the University of Oklahoma Health Sciences Center, in collaboration with the Centers for Disease Control and Prevention (CDC), the Oklahoma State Department of Health, and the Oklahoma City–County Health Department, established a novel pilot population-based surveillance system for VTE events in Oklahoma County, OK, from April 1, 2012 to March 31, 2014. Oklahoma County was suitable for this pilot testing because of the strong similarity of its population demographics to the US national population. We describe this novel surveillance approach for VTE events using combined active and passive surveillance and discuss how these methods may inform the development of a national surveillance system as well as contribute to increased understanding of the burden of VTE disease.

Methods

Surveillance system objectives

The primary aims of our pilot surveillance system were to (1) develop and implement a population-based surveillance system for DVT and PE in Oklahoma County, OK, that includes both active and passive surveillance activities and which can accurately capture outpatient, inpatient, and death-related VTE events and distinguish first episode (incident) from recurrent VTE events; (2) estimate the annual incidence of first-episode VTE events and DVT and PE separately, (3) estimate the annual incidence of recurrent VTE events and of the components of DVT and PE, (4) estimate the 30-day, 90-day, and 6-month mortality associated with a diagnosis of VTE and the component events of DVT or PE; (5) describe the above VTE disease burden indicators by age, gender, and race/ethnicity, including the minority groups of American Indian, Black, Hispanic, and Asian; (6) collect data on risk factors associated with documented VTE events; and (7) identify hypotheses for future research to reduce the burden of VTE disease (see Table I).

Table I.

Objectives for the VTE surveillance system using combined active and passive methods

Objectives
  1. Develop and implement a pilot, population-based surveillance system for DVT and PE in Oklahoma County, OK, that includes both active and passive surveillance activities and which can accurately capture outpatient, inpatient, and death-related VTE events and distinguish first episode (incident) from recurrent VTE events;

  2. Estimate the annual incidence of first-episode VTE events and of the components of DVT and PE separately;

  3. Estimate the annual incidence of recurrent VTE events and of the components of DVT and PE;

  4. Estimate the 30-day, 90-day, and 6-month mortality associated with a diagnosis of VTE and the component events of DVT and PE;

  5. Describe the above VTE disease burden indicators by age, gender, and race/ethnicity, including the minority groups of American Indian, Black, Hispanic, and Asian;

  6. Collect data on risk factors associated with documented VTE events;

  7. Identify hypotheses for future research to reduce the burden of VTE disease.

Surveillance system and population

A key and unique feature of this surveillance system is the collaboration with the Oklahoma State Commissioner of Health, who established VTE diagnoses as reportable conditions for 2010 to 2015 and delegated to the College of Public Health the authority to conduct the surveillance (Oklahoma Statute §631-106B). The surveillance was conducted as an activity authorized by federal10 and state statutes for protection of public health, and, therefore, institutional review board approval for access to the health information was not required. The surveillance was conducted in compliance with the requirements of the US Health Insurance Portability and Accountability Act.

Oklahoma County is representative of the US population by race and ethnicity (Table II), although it has a higher percentage of American Indians (7.7% vs 1.7%).11 In addition, it is an urban metropolitan service area in the center of the state for which few residents travel out of the county or the state for their health care. Hospital discharge data (described in detail below) for the state were accessed to determine that 98 Oklahoma County residents received care for a VTE-related event out of Oklahoma County during 2010 to 2012.

Table II.

Racial, ethnic, gender, and income distribution of the population in the United States, Oklahoma State, and Oklahoma County, 201211

United States
Oklahoma
County
Race/ethnicity n % n %
Population 313,914,040 100 741,781 100
Race
 White 239,645,013 76.3 553,227 74.6
 Black 43,140,238 13.7 127,854 17.2
 American Indian 5,226,034 1.7 57,462 7.7
 Asian 18,326,450 5.8 28,223 3.8
 Hawaiian/Pacific Islander 1,250,274 0.4 1,500 0.2
 Other 16,232,503 5.2 26,956 3.6
Ethnicity
 Hispanic 52,961,017 16.9 116,932 15.8
 Non-Hispanic 260,953,023 83.1 624,849 84.2
Gender
 Male 154,436,243 49.2 363,306 49.0
 Female 159,477,797 50.8 378,475 51.0
Median income (dollars) 53,046 45,082

We implemented both active and passive surveillance methods in an effort to quantify and measure the extent to which each approach successfully identified cases. The active surveillance system was designed to serve as the criterion standard and to optimize specificity. The passive surveillance system was designed to optimize sensitivity. The Figure is a flowchart of all surveillance activities.

Figure.

Figure

Flowchart for surveillance system for VTE in Oklahoma County, OK—April 1, 2012 to March 31, 2014. Abbreviations: ASC, ambulatory surgical centers; IP, inpatient; OP, outpatient; HCI, health care information; ID, identification.

Active surveillance

Active surveillance consisted of surveillance officers (graduate students in public health generally with clinical backgrounds) visiting all of the 13 inpatient facilities and all of the eligible outpatient facilities in Oklahoma County on a regular basis. Criteria for eligible inpatient and outpatient facilities are summarized in Table III. Surveillance officers reviewed the text of relevant imaging reports from April 1, 2012 to March 31, 2014, to classify VTE cases as definite or probable cases or noncases (see case definition, Table IV). We also included the Oklahoma City Veterans Affairs (VA) Medical Center. Eligible facilities were identified by using 3 different data sources: (1) historic hospital discharge data (2009-2010) to estimate the potential caseload; (2) the Oklahoma State Health Department’s database of facilities licensed for CTA, magnetic resonance imaging (MRI), and CUS equipment in the county; and 3) the national accrediting body of facilities using those same diagnostic equipment. Before initiating surveillance, we met with the Greater Oklahoma City Hospital Council and introduced the surveillance project to the chief executive officers of the county’s hospitals. We also communicated with each inpatient and outpatient facility by mail and telephone. We met with the health information management director of each facility to establish surveillance activities, provide them with the case definition, and tailor our case methods to their facility processes. We screened outpatient facilities for eligibility based on the relevant diagnostic equipment they used and whether they diagnosed patients with VTE conditions.

Table III.

Inpatient and outpatient facility inclusion criteria

Inpatient and outpatient
Inclusion
 criteria
  1. Located within Oklahoma County

  2. Licensed for the following diagnostic equipment: CT, MRI, V/Q scan, contrast venography, or ultrasound.

  3. At least 1 licensed radiologist on staff to diagnose VTE conditions using defined diagnostic equipment.

  4. Licensed health care provider in specialty at any level from December 2012 National Provider Identification listing from radiology (neuroradiology, nuclear radiology, radiation oncology, diagnostic radiology, diagnostic ultrasound, surgery, surgical critical care, vascular surgery, urology, pediatric urology, and thoracic surgery), allopathic and osteopathic physicians (general practice, pulmonary disease, interventional cardiology, hematology and oncology, clinical cardiac electrophysiology, internal medicine, family medicine, and independent medical examiner), pathology hematology, and podiatric medicine and surgery service providers.

Exclusion
 criteria
  1. If licensed diagnostic equipment is too old to currently diagnose VTE conditions.

  2. If patient volume with a VTE condition was <5 patients per year

Table IV.

Case definitions for DVT and PE

DVT PE
Definite
  1. Imaging is confirmatory

    or

  2. Autopsy

    or

  3. Venous thrombectomy confirms thrombus is present

  1. Imaging is confirmatory

    or

  2. Autopsy

    or

  3. Pulmonary embolectomy confirms embolism is present

Probable
  1. Imaging is indeterminate, and review of records shows mention of DVT or suspected DVT and treatment given:
    • 1)
      Anticoagulant
      or
    • 2)
      DVT-related procedure: vena cava filter or thrombolysis (systemic or catheter directed)
  1. Imaging is indeterminate or not available/not done, and review of records shows mention of PE or suspected PE and treatment given:
    • 1)
      Anticoagulant
      or
    • 2)
      PE-related procedure: vena cava filter or thrombolysis (systemic or catheter directed)
      or
  2. Death certificate—contributing cause of death

Possible: ≥2 of the following:
  1. ICD-9 CM code

    or

  2. DVT related CPT code

    or

  3. ICD-10 CM code

    or

  4. POA indicator listed as “Y” for DVT

  1. ICD-9 CM code

    or

  2. PE-related CPT code

    or

  3. ICD-10 CM code

    or

  4. POA code indicator listed as “Y” for PE

Each facility (both inpatient and outpatient) generated lists of all patients who had received one of the qualifying imaging studies (irrespective of the radiologists’ diagnosis) or a diagnostic or procedure code (online Appendix A and B) during the surveillance period, regardless of the patient’s symptoms. Because of varying medical records systems, facilities used a variety of methods to identify these patients, including querying their system for ICD-9 CM procedure codes, current procedural terminology (CPT) codes, and free text for the test (such as “CTA” or “ultrasound”). We worked with a variety of electronic medical records systems, including Cerner, Centricity, Meditech (Horizon Patient Folder), and EPIC as well as a few facilities still using paper-based records.

Patient records were retrieved by facility staff and reviewed by surveillance officers to identify those whose residence was within Oklahoma County (as determined by county and ZIP code information) for inclusion in the surveillance. Subsequently, the surveillance officers determined eligibility based on the occurrence of a VTE event during the surveillance period (April 1, 2012 to March 31, 2014), which was followed by review of the final impression from the imaging report and complete data abstraction of eligible cases. Screening the imaging report for a PE or DVT diagnosis required approximately 1 minute per record, and data abstraction typically required 45 to 60 minutes per record. Data abstraction included patient-identifying information, demographic variables, medical history (including history of VTE), signs and symptoms related to their VTE diagnosis, major and minor risk factors, and VTE prophylaxis and treatment, including medication regimens and dates administered.

We collected data on age, gender, race (defined as white, black, American Indian, Asian, Pacific Islander, and other) and ethnicity (defined as Hispanic and non-Hispanic), obesity (measured by height and weight), hospitalization, surgery or trauma within the prior 12 months, cancer (except basal or squamous cell carcinoma of the skin), paralysis of the leg, pregnancy, myocardial infarction, stroke, systemic lupus erythematosus, and inflammatory bowel disease. Reason for hospitalization and indication for and type of surgery were also collected. Dates for each risk factor were collected when available, and, when unavailable, any data regarding time frame were collected and categorized into <3 months, 3 to 5.9 months, 6 to 11.9 months, and ≥12 months.

Surveillance officers entered case-patient data directly into Velos eResearch using encrypted laptops with secure internet connections. The Velos-based database was housed behind the university’s information technology firewall, and the case-patient data were securely stored and compliant with the Health Insurance Portability and Accountability Act regulations. We limited the use of paper-based records to increase security as well as efficiency of data entry.

Passive surveillance

Passive surveillance consisted of acquiring all-payer hospital discharge data (with patient-identifying information) from the Oklahoma State Department of Health’s Division of Health Care Information. Because the VA is not required to report to state agencies, their data are not included in the hospital discharge data. The ICD-9 CM codes used in this system are listed in the online Appendix A and B. We were able to access and use patient-specific data because the State Health Commissioner delegated to the College of Public Health the authority to conduct the surveillance (Oklahoma Statute §631-106B).

We obtained hospital discharge data with patient identifiers from all inpatient, outpatient, and ambulatory surgery center facilities for all cases diagnosed and treated in Oklahoma County and all events associated with that individual for each year 2010 to 2012 using our broad VTE definition (online Appendix A and B) (2013-2014 data will be obtained when available). Cases were identified by using either the primary ICD-9 CM diagnosis field or any of the 15 contributing ICD-9 CM diagnosis fields.

We also received the January 1, 2010 to April 30, 2014, mortality files compiled from death certificates (subsequent years will be obtained upon availability). Cases were identified using ICD-10 codes and text in the cause of death and significant contributing causes of death fields (online Appendix A and B).

The data were merged and deduplicated within and across years, between discharge types (ie, inpatient, outpatient, and ambulatory surgical care), and across data types (ie, hospital discharge data and mortality data) using Link Plus,12 a probabilistic record linkage software designed to link records with incomplete or variable information according to patient-identifying information (name, date of birth, address, and social security number). The probabilistic linkage algorithm assigns probability scores that indicate how likely it is that a pair of records refer to the same person. A threshold score of 3 was used to automatically accept and reject potential links with all uncertain pairs manually reviewed by 2 independent reviewers. Once complete, 2 manual reviews were compared to confirm or reject matches.

Case definition

We used tiered case definitions and case finding methods based on the amount and quality of the diagnostic data available as shown in Table IV. All DVT events of the upper and lower extremities are included, including acute, chronic, and recurrent. Superficial venous thromboses were excluded. For active surveillance, a finding of DVT or PE based on an imaging study including CTA, CUS, MRI, ventilation-perfusion (V/Q) scan, or pulmonary angiogram was required for either a definite or probable case. Final case classification was assigned by study investigators (see interrater reliability below). Furthermore, patients were classified as a probable case when the death certificate listed PE as a primary or contributing cause of death.

Passive surveillance relied on ICD-9 CM (diagnosis and procedure), CPT, or POA codes for identification of possible VTE events. Thus, the only case classification available was as a possible case (in which ≥2 qualifying codes were required). The full case definition is included in the appendix.

Comparing active with passive surveillance

Once available, the passive surveillance data (ie, hospital discharge data and mortality data) will be linked to the active data and deduplicated using probabilistic record linkage methods similar to those described in the passive surveillance above. In addition, we will use the same method to link live cases identified using active surveillance to the mortality file.

Statistical methods

Descriptive statistics were used to summarize population demographics. The distribution of case patients for each stage of surveillance and disease manifestation was presented for each facility type (inpatient vs outpatient). All analyses were conducted using SAS 9.3 (SAS Institute, Inc, Cary, NC).

Interrater reliability for data collection was evaluated by taking a random sample of 5% (with a minimum of 5 records per facility) of the cases that were identified from 7 inpatient facilities and selected for quality assurance. At least 2 secondary surveillance officers independently collected data for each identified case, and agreement was assessed (using the κ statistic) between the primary surveillance officer and the 2 secondary reviewers.

We used the free marginal method13 to calculate κ to assess agreement for all categorical variables. Agreement was categorized into very good (κ = 0.81-1.0), good (κ = 0.61-0.80), moderate (κ = 0.41-0.60), and poor to fair (κ ≤0.40).

Funding was provided through a cooperative agreement (DD14-1407) with the CDC for the design and implementation of the surveillance system and publication of the design manuscript. The authors are solely responsible for the design and conduct of this study; all study analyses, the drafting and editing of the paper, and its final contents.

Results

All 13 inpatient facilities in Oklahoma County and the Oklahoma City VA Medical Center were included in this surveillance system. Fifty-six outpatient facilities were identified as being potentially eligible for surveillance; however, after contacting each facility, only 8 facilities met the criteria to be included in the surveillance, each of which contributed data to the surveillance system. As of February 1, 2015, we have screened 54,494 (99.5%) of 54,782 identified imaging records of patients having had one of the diagnostic procedures (ie, CTA, MRI, V/Q scan, and CUS) during the surveillance period (Table V). From the records screened, we have identified 2,725 case patients with VTE using the active surveillance system (of which 2,496 [91.6%] case patients are from inpatient facilities and 229 [8.4%] case patients are from outpatient facilities). Among the 2,231 case patients for whom data collection is complete, 1,290 (63%) have DVT, 476 (23%) have PE, and 293 (14%) have both DVT and PE. In addition, among the 172 (7.7%) case patients enrolled from outpatient facilities for whom data collection has been completed, 156 (91%) case patients have DVT, 11 (6%) case patients have PE, and 5 (3%) case patients have both DVT and PE (Table VI). Using hospital discharge data for 2010 to 2012, we identified 98 residents (2.4% of the case patients) of Oklahoma County who received a diagnosis for a VTE-related event outside Oklahoma County who were missed by the active surveillance.

Table V.

The distribution of case patients for each stage of surveillance stratified by facility type

Identified patients
with diagnostic
procedure
Screened records
Patients meeting
case definition
Case patients with
data collection
complete
Facility type n % n % n % n %
Inpatient facilities 50,535 92.2 50,466 92.6 2496 91.6 2059 92.3
Outpatient facilities 4247 7.8 4028 7.4 229 8.4 172 7.7
Total 54,782 100 54,494 100 2725 100 2231 100

Table VI.

The distribution of case patients stratified by facility type and disease manifestation

Inpatient
facilities
Outpatient
facilities
Total
Disease manifestation n % n % n %
VTE cases 2059 100 172 100 2231 100
DVT only 1290 62.7 156 90.7 1446 64.8
PE only 476 23.1 11 6.4 487 21.8
Both DVT and PE 293 14.2 5 2.9 298 13.4

Our data collection instrument had 44 variables. Agreement between data collectors was high, with 41 (93.2%) variables having κ, ≥0.61. The agreement for our 2 key measurements, diagnosis of PE and diagnosis of DVT, were κ = 0.92 (95% CI 0.74-1.00) and κ = 0.89 (95% CI 0.71-1.00), respectively. The 3 variables with moderate agreement were symptoms of the leg (κ = 0.59; 95% CI 0.42-0.77), history of DVT (κ = 0.59; 95% CI 0.42-0.77), and history of hospitalization (κ = 0.45; 95% CI 0.27-0.62). The agreement between the 2 study investigators’ classification of cases according to the case definition was also high, DVT, κ = 0.84 (95% CI 0.76-0.93) and PE, κ = 0.94 (95% CI 0.88-1.00).

Discussion

We established a pilot population-based surveillance system for VTE using both active and passive methods in Oklahoma County, OK, to inform CDC regarding the development of future national VTE surveillance. We designed this system to (1) improve VTE-related estimates of the incidence of first-time and recurrent events and mortality rates, (2) differentiate between provoked and unprovoked events as well as describe these patients by demographic characteristics (including race/ethnicity), and (3) identify the contribution of patients with VTE events in the outpatient setting.

This surveillance system has been operating as intended as evidenced by the progress made in identifying potential case patients, applying the case definition, and collecting the demographic and diagnostic information regarding the VTE event. Among the 54,670 patients flagged for screening based on having a diagnostic procedure during the surveillance period, 99.6% have been screened. In addition, data have been collected for >80% of all identified cases. This amount of progress lends confidence to the continued success of the surveillance system through the end of the surveillance period.

This pilot surveillance system was not designed to be sustainable in its present form. Instead, we designed it to inform us and CDC regarding the performance of each aspect of VTE disease surveillance. However, without a standard by which to assess the performance of hospital discharge and administrative claims data, the sensitivity and specificity of a national surveillance system will be unknown. Hence, the active surveillance was developed to serve as the criterion standard by maximizing specificity through the use of imaging studies to confirm and classify cases. On the other hand, because ICD-9 CM codes have the tendency to “follow” patients over time, querying the hospital discharge database is a highly sensitive technique for identifying possible cases. Sensitivity was further enhanced by using a broad set of codes designed to maximize the identification of possible cases. The final step of linking the active and passive surveillance databases by patient-identifying information and then investigating the discordant cases will allow us to assess the performance (ie, sensitivity, specificity, and positive predictive values) of case definitions based on ICD-9 CM codes. We will also be able to evaluate the ability of our active system to detect cases by sampling those possible cases from the hospital discharge data who did not link to the active cases and following up back to determine if they were a true case missed by our active methods or a false-positive based on using ICD-9 CM codes. Using the cleaned, deduplicated, linked database, we will be able to provide estimates of first-time and recurrent VTE events that are likely more accurate than any that are currently available by claims data.

Another strength of this system will be the ability to better describe risk factors for VTE events and to differentiate between provoked and unprovoked events. Among the case patients with provoked VTE events, we will be able to measure the utilization of VTE prevention measures and identify points of intervention to improve the implementation of prevention if needed. This may improve our ability to identify a certain proportion of potentially preventable cases (which could be used as a performance metric for hospitals in the future). Finally, given the racially diverse population in Oklahoma County, we aim to be able to describe the incidence and risk factors in minority populations that have been historically understudied.

The last objective of our surveillance system is to determine the number of patients with VTE events being diagnosed and/or managed in an outpatient setting. The barriers to outpatient management of VTE in the United States include (1) initial treatment has traditionally consisted of parenteral therapy, which is easier to administer in the hospital,14 (2) remuneration for health care facilities and providers is higher in an inpatient setting,15,16 and (3) the patient population often has comorbid conditions requiring inpatient care. On the other hand, a factor which may increase the outpatient management of VTE is the development of new oral medications.14,17 Our finding that approximately 8% of patients were diagnosed in the outpatient setting is lower but similar to 11% in a German retrospective cohort study. 18 By conducting active surveillance in outpatient facilities with CT and CUS machines, we will be able to better understand the proportion of patients referred to tertiary care facilities for further treatment and care and thus inform future scaled-up national surveillance regarding the importance of including outpatient facilities.

Our surveillance system is subject to certain limitations. One limitation is the time lag between the hospitalization and when the hospital discharge data are available for the passive surveillance. Specifically, the hospital discharge data are not available until approximately 1 year after the end of that discharge year. In contrast, the active data are typically delayed by no more than a month (while waiting for the patient to be discharged and all the data to be entered into the facility’s electronic medical record). Thus, the data collected by active and passive methods cannot be linked and analyzed until ≥1 year after the event. Other limitations include the cost involved to conduct active surveillance (which is unlikely to be maintained over long periods), missing risk factor information in the medical record, variability in the way facilities identify potentially eligible patients for screening, and the amount of time required for surveillance officers to screen potentially eligible patients and subsequently enter their information into the database.

Additional limitations include factors contributing to us potentially missing a VTE case. One scenario is those patients who seek and are diagnosed outside the catchment area (ie, Oklahoma County). We will, however, include these cases if they receive follow-up care within the catchment area during the surveillance window. Another scenario is those VTE cases that never had the relevant imaging studies, did not have an eligible ICD-9 code, and, for those who died, had no mention on the death certificate. Finally, although the demographics of Oklahoma County are remarkably similar to the US national population, there may be other features of our surveillance population, which may not be generalizable to the US population. This latter limitation is the key reason why a national surveillance system is required. Although incidence estimates derived from a population-based study restricted to a county or state may have limitations in generalizability, the methods evaluated in the pilot study should be scalable for use in a broader national effort.

Conclusions

In conclusion, we developed a pilot population-based surveillance system for VTE in Oklahoma County, OK. This novel system incorporates both active and passive elements. The most important factor in conducting our surveillance was the collaboration with CDC and the Oklahoma Commissioner of Health. This allowed us to work with all facilities in the county and collect the required information. We are in the process of better understanding the quality of individual ICD-9 CM codes in identifying true cases. In addition, these results will help inform future national surveillance and monitoring for VTE events. Future topics we plan to address using these data include identifying the proportion of preventable VTE events, better elucidating the incidence of provoked versus unprovoked events, and describing the extent to which patients receive the evidence-based recommended treatment for their VTE condition.

Acknowledgments

This surveillance system was funded by a cooperative agreement with the CDC DD14-1407. We are also deeply grateful for the work of the surveillance officer, Natalie Feland, Aubrey Balch, Jannate Ahmed, Evaren Page, and Ashley Sword-Buster, for their tireless dedication in collecting the data. We are also grateful for Pravina Kota for her information technology support, including the development of the database.

CDC disclaimer: The findings and conclusions in this report are those of the author(s) and do not necessarily represent the official position of the CDC.

Appendix A

Deep vein thrombosis—related ICD-9 codes, CPT codes, and ICD-10 codes

ICD-10
codes
Definition
I80 Phlebitis and thrombophlebitis
I800 Phlebitis and thrombophlebitis of superficial vessels of lower
extremities
I8000 Phlebitis and thrombophlebitis of superficial vessels of
unspecified lower extremity
I8001 Phlebitis and thrombophlebitis of superficial vessels of right
lower extremity
I8002 Phlebitis and thrombophlebitis of superficial vessels of left
lower extremity
I8003 Phlebitis and thrombophlebitis of superficial vessels of lower
extremities, bilateral
I801 Phlebitis and thrombophlebitis of femoral vein
I8010 Phlebitis and thrombophlebitis of unspecified femoral vein
I8011 Phlebitis and thrombophlebitis of right femoral vein
I8012 Phlebitis and thrombophlebitis of left femoral vein
I8013 Phlebitis and thrombophlebitis of femoral vein, bilateral
I802 Phlebitis and thrombophlebitis of other and unspecified deep
vessels of lower extremities
I8020 Phlebitis and thrombophlebitis of unspecified deep vessels of
lower extremities
I80201 Phlebitis and thrombophlebitis of unspecified deep vessels of
right lower extremity
I80202 Phlebitis and thrombophlebitis of unspecified deep vessels of
left lower extremity
I80203 Phlebitis and thrombophlebitis of unspecified deep vessels of
lower extremities, bilateral
I80209 Phlebitis and thrombophlebitis of unspecified deep vessels of
unspecified lower extremity
I8021 Phlebitis and thrombophlebitis of iliac vein
I80211 Phlebitis and thrombophlebitis of right iliac vein
I80212 Phlebitis and thrombophlebitis of left iliac vein
I80213 Phlebitis and thrombophlebitis of iliac vein, bilateral
I80219 Phlebitis and thrombophlebitis of unspecified iliac vein
I8022 Phlebitis and thrombophlebitis of popliteal vein
I80221 Phlebitis and thrombophlebitis of right popliteal vein
I80222 Phlebitis and thrombophlebitis of left popliteal vein
I80223 Phlebitis and thrombophlebitis of popliteal vein, bilateral
I80229 Phlebitis and thrombophlebitis of unspecified popliteal vein
I8023 Phlebitis and thrombophlebitis of tibial vein
I80231 Phlebitis and thrombophlebitis of right tibial vein
I80232 Phlebitis and thrombophlebitis of left tibial vein
I80233 Phlebitis and thrombophlebitis of tibial vein, bilateral
I80239 Phlebitis and thrombophlebitis of unspecified tibial vein
I8029 Phlebitis and thrombophlebitis of other deep vessels of
lower extremities
I80291 Phlebitis and thrombophlebitis of other deep vessels of right
lower extremity
I80292 Phlebitis and thrombophlebitis of other deep vessels of left
lower extremity
I80293 Phlebitis and thrombophlebitis of other deep vessels of lower
extremity, bilateral
I80299 Phlebitis and thrombophlebitis of other deep vessels of
unspecified lower extremity
I803 Phlebitis and thrombophlebitis of lower extremities, unspecified
I808 Phlebitis and thrombophlebitis of other sites
I809 Phlebitis and thrombophlebitis of unspecified site
I82 Other venous embolism and thrombosis
I821 Thrombophlebitis migrans
I822 Embolism and thrombosis of vena cava and other thoracic veins
I8221 Embolism and thrombosis of superior vena cava
I82210 Acute embolism and thrombosis of superior vena cava
I82211 Chronic embolism and thrombosis of superior vena cava
I8222 Embolism and thrombosis of inferior vena cava
I82220 Acute embolism and thrombosis of inferior vena cava
I82221 Chronic embolism and thrombosis of inferior vena cava
I8229 Embolism and thrombosis of other thoracic veins
I82290 Acute embolism and thrombosis of other thoracic veins
I82291 Chronic embolism and thrombosis of other thoracic veins
I823 Embolism and thrombosis of renal vein
I824 Acute embolism and thrombosis of deep veins of lower extremity
I8240 Acute embolism and thrombosis of unspecified deep veins of
lower extremity
I82401 Acute embolism and thrombosis of unspecified deep veins of
right lower extremity
I82402 Acute embolism and thrombosis of unspecified deep veins of
left lower extremity
I82403 Acute embolism and thrombosis of unspecified deep veins of
lower extremity, bilateral
I82409 Acute embolism and thrombosis of unspecified deep veins of
unspecified lower extremity
I8241 Acute embolism and thrombosis of femoral vein
I82411 Acute embolism and thrombosis of right femoral vein
I82412 Acute embolism and thrombosis of left femoral vein
I82413 Acute embolism and thrombosis of femoral vein, bilateral
I82419 Acute embolism and thrombosis of unspecified femoral vein
I8242 Acute embolism and thrombosis of iliac vein
I82421 Acute embolism and thrombosis of right iliac vein
I82422 Acute embolism and thrombosis of left iliac vein
I82423 Acute embolism and thrombosis of iliac vein, bilateral
I82429 Acute embolism and thrombosis of unspecified iliac vein
I8243 Acute embolism and thrombosis of popliteal vein
I82431 Acute embolism and thrombosis of right popliteal vein
I82432 Acute embolism and thrombosis of left popliteal vein
I82433 Acute embolism and thrombosis of popliteal vein, bilateral
I82439 Acute embolism and thrombosis of unspecified popliteal vein
I8244 Acute embolism and thrombosis of tibial vein
I82441 Acute embolism and thrombosis of right tibial vein
I82442 Acute embolism and thrombosis of left tibial vein
I82443 Acute embolism and thrombosis of tibial vein, bilateral
I82449 Acute embolism and thrombosis of unspecified tibial vein
I8249 Acute embolism and thrombosis of other specified deep vein
of lower extremity
I82491 Acute embolism and thrombosis of other specified deep vein
of right lower extremity
I82492 Acute embolism and thrombosis of other specified deep vein
of left lower extremity
I82493 Acute embolism and thrombosis of other specified deep vein
of lower extremity, bilateral
I82499 Acute embolism and thrombosis of other specified deep vein
of unspecified lower extremity
I824Y Acute embolism and thrombosis of unspecified deep veins of
proximal lower extremity
I824Y1 Acute embolism and thrombosis of unspecified deep veins of
right proximal lower extremity
I824Y2 Acute embolism and thrombosis of unspecified deep veins of
left proximal lower extremity
I824Y3 Acute embolism and thrombosis of unspecified deep veins of
proximal lower extremity, bilateral
I824Y9 Acute embolism and thrombosis of unspecified deep veins
of unspecified proximal lower extremity
I824Z Acute embolism and thrombosis of unspecified deep veins
of distal lower extremity
I824Z1 Acute embolism and thrombosis of unspecified deep veins
of right distal lower extremity
I824Z2 Acute embolism and thrombosis of unspecified deep veins
of left distal lower extremity
I824Z3 Acute embolism and thrombosis of unspecified deep veins
of distal lower extremity, bilateral
I824Z9 Acute embolism and thrombosis of unspecified deep veins
of unspecified distal lower extremity
I825 Chronic embolism and thrombosis of deep veins of
lower extremity
I8250 Chronic embolism and thrombosis of unspecified deep veins
of lower extremity
I82501 Chronic embolism and thrombosis of unspecified deep veins
of right lower extremity
I82502 Chronic embolism and thrombosis of unspecified deep veins
of left lower extremity
I82503 Chronic embolism and thrombosis of unspecified deep veins
of lower extremity, bilateral
I82509 Chronic embolism and thrombosis of unspecified deep veins
of unspecified lower extremity
I8251 Chronic embolism and thrombosis of femoral vein
I82511 Chronic embolism and thrombosis of right femoral vein
I82512 Chronic embolism and thrombosis of left femoral vein
I82513 Chronic embolism and thrombosis of femoral vein, bilateral
I82519 Chronic embolism and thrombosis of unspecified femoral vein
I8252 Chronic embolism and thrombosis of iliac vein
I82521 Chronic embolism and thrombosis of right iliac vein
I82522 Chronic embolism and thrombosis of left iliac vein
I82523 Chronic embolism and thrombosis of iliac vein, bilateral
I82529 Chronic embolism and thrombosis of unspecified iliac vein
I8253 Chronic embolism and thrombosis of popliteal vein
I82531 Chronic embolism and thrombosis of right popliteal vein
I82532 Chronic embolism and thrombosis of left popliteal vein
I82533 Chronic embolism and thrombosis of popliteal vein, bilateral
I82539 Chronic embolism and thrombosis of unspecified popliteal vein
I8254 Chronic embolism and thrombosis of tibial vein
I82541 Chronic embolism and thrombosis of right tibial vein
I82542 Chronic embolism and thrombosis of left tibial vein
I82543 Chronic embolism and thrombosis of tibial vein, bilateral
I82549 Chronic embolism and thrombosis of unspecified tibial vein
I8259 Chronic embolism and thrombosis of other specified deep
vein of lower extremity
I82591 Chronic embolism and thrombosis of other specified deep
vein of right lower extremity
I82592 Chronic embolism and thrombosis of other specified deep
vein of left lower extremity
I82593 Chronic embolism and thrombosis of other specified deep
vein of lower extremity, bilateral
I82599 Chronic embolism and thrombosis of other specified deep
vein of unspecified lower extremity
I825Y Chronic embolism and thrombosis of unspecified deep veins
of proximal lower extremity
I825Y1 Chronic embolism and thrombosis of unspecified deep veins
of right proximal lower extremity
I825Y2 Chronic embolism and thrombosis of unspecified deep veins
of left proximal lower extremity
I825Y3 Chronic embolism and thrombosis of unspecified deep veins
of proximal lower extremity, bilateral
I825Y9 Chronic embolism and thrombosis of unspecified deep veins
of unspecified proximal lower extremity
I825Z Chronic embolism and thrombosis of unspecified deep veins
of distal lower extremity
I825Z1 Chronic embolism and thrombosis of unspecified deep veins
of right distal lower extremity
I825Z2 Chronic embolism and thrombosis of unspecified deep veins
of left distal lower extremity
I825Z3 Chronic embolism and thrombosis of unspecified deep veins
of distal lower extremity, bilateral
I825Z9 Chronic embolism and thrombosis of unspecified deep veins
of unspecified distal lower extremity
I826 Acute embolism and thrombosis of veins of upper
extremity
I8260 Acute embolism and thrombosis of unspecified veins of
upper extremity
I82601 Acute embolism and thrombosis of unspecified veins of right
upper extremity
I82602 Acute embolism and thrombosis of unspecified veins of left
upper extremity
I82603 Acute embolism and thrombosis of unspecified veins of
upper extremity, bilateral
I82609 Acute embolism and thrombosis of unspecified veins of
unspecified upper extremity
I8261 Acute embolism and thrombosis of superficial veins of
upper extremity
I82611 Acute embolism and thrombosis of superficial veins of right
upper extremity
I82612 Acute embolism and thrombosis of superficial veins of left
upper extremity
I82613 Acute embolism and thrombosis of superficial veins of
upper extremity, bilateral
I82619 Acute embolism and thrombosis of superficial veins of
unspecified upper extremity
I8262 Acute embolism and thrombosis of deep veins of upper extremity
I82621 Acute embolism and thrombosis of deep veins of right
upper extremity
I82622 Acute embolism and thrombosis of deep veins of left
upper extremity
I82623 Acute embolism and thrombosis of deep veins of upper
extremity, bilateral
I82629 Acute embolism and thrombosis of deep veins of unspecified
upper extremity
I827 Chronic embolism and thrombosis of veins of upper extremity
I8270 Chronic embolism and thrombosis of unspecified veins of
upper extremity
I82701 Chronic embolism and thrombosis of unspecified veins of
right upper extremity
I82702 Chronic embolism and thrombosis of unspecified veins of
left upper extremity
I82703 Chronic embolism and thrombosis of unspecified veins of
upper extremity, bilateral
I82709 Chronic embolism and thrombosis of unspecified veins of
unspecified upper extremity
I8271 Chronic embolism and thrombosis of superficial veins of
upper extremity
I82711 Chronic embolism and thrombosis of superficial veins of
right upper extremity
I82712 Chronic embolism and thrombosis of superficial veins of left
upper extremity
I82713 Chronic embolism and thrombosis of superficial veins of
upper extremity, bilateral
I82719 Chronic embolism and thrombosis of superficial veins of
unspecified upper extremity
I8272 Chronic embolism and thrombosis of deep veins of
upper extremity
I82721 Chronic embolism and thrombosis of deep veins of right
upper extremity
I82722 Chronic embolism and thrombosis of deep veins of left
upper extremity
I82723 Chronic embolism and thrombosis of deep veins of upper
extremity, bilateral
I82729 Chronic embolism and thrombosis of deep veins of
unspecified upper extremity
I82A Embolism and thrombosis of axillary vein
I82A1 Acute embolism and thrombosis of axillary vein
I82A11 Acute embolism and thrombosis of right axillary vein
I82A12 Acute embolism and thrombosis of left axillary vein
I82A13 Acute embolism and thrombosis of axillary vein, bilateral
I82A19 Acute embolism and thrombosis of unspecified axillary vein
I82A2 Chronic embolism and thrombosis of axillary vein
I82A21 Chronic embolism and thrombosis of right axillary vein
I82A22 Chronic embolism and thrombosis of left axillary vein
I82A23 Chronic embolism and thrombosis of axillary vein, bilateral
I82A29 Chronic embolism and thrombosis of unspecified axillary vein
I82B Embolism and thrombosis of subclavian vein
I82B1 Acute embolism and thrombosis of subclavian vein
I82B11 Acute embolism and thrombosis of right subclavian vein
I82B12 Acute embolism and thrombosis of left subclavian vein
I82B13 Acute embolism and thrombosis of subclavian vein, bilateral
I82B19 Acute embolism and thrombosis of unspecified subclavian vein
I82B2 Chronic embolism and thrombosis of subclavian vein
I82B21 Chronic embolism and thrombosis of right subclavian vein
I82B22 Chronic embolism and thrombosis of left subclavian vein
I82B23 Chronic embolism and thrombosis of subclavian vein, bilateral
I82B29 Chronic embolism and thrombosis of unspecified subclavian
vein
I82C Embolism and thrombosis of internal jugular vein
I82C1 Acute embolism and thrombosis of internal jugular vein
I82C11 Acute embolism and thrombosis of right internal jugular vein
I82C12 Acute embolism and thrombosis of left internal jugular vein
I82C13 Acute embolism and thrombosis of internal jugular
vein, bilateral
I82C19 Acute embolism and thrombosis of unspecified internal
jugular vein
I82C2 Chronic embolism and thrombosis of internal jugular vein
I82C21 Chronic embolism and thrombosis of right internal jugular vein
I82C22 Chronic embolism and thrombosis of left internal jugular vein
I82C23 Chronic embolism and thrombosis of internal jugular
vein, bilateral
I82C29 Chronic embolism and thrombosis of unspecified internal
jugular vein
I828 Embolism and thrombosis of other specified veins
I8281 Embolism and thrombosis of superficial veins of lower
extremities
I82811 Embolism and thrombosis of superficial veins of right lower
extremities
I82812 Embolism and thrombosis of superficial veins of left lower
extremities
I82813 Embolism and thrombosis of superficial veins of lower
extremities, bilateral
I82819 Embolism and thrombosis of superficial veins of unspecified
lower extremities
I8289 Embolism and thrombosis of other specified veins
I82890 Acute embolism and thrombosis of other specified veins
I82891 Chronic embolism and thrombosis of other specified veins
I829 Embolism and thrombosis of unspecified vein
I8290 Acute embolism and thrombosis of unspecified vein
I8291 Chronic embolism and thrombosis of unspecified vein
I870 Postthrombotic syndrome
I8700 Postthrombotic syndrome without complications
I87001 Postthrombotic syndrome without complications of right
lower extremity
I87002 Postthrombotic syndrome without complications of left
lower extremity
I87003 Postthrombotic syndrome without complications of bilateral
lower extremity
I87009 Postthrombotic syndrome without complications of unspecified
extremity
I8701 Postthrombotic syndrome with ulcer
I87011 Postthrombotic syndrome with ulcer of right lower extremity
I87012 Postthrombotic syndrome with ulcer of left lower extremity
I87013 Postthrombotic syndrome with ulcer of bilateral lower extremity
I87019 Postthrombotic syndrome with ulcer of unspecified lower
extremity
I8702 Postthrombotic syndrome with inflammation
I87021 Postthrombotic syndrome with inflammation of right lower
extremity
I87022 Postthrombotic syndrome with inflammation of left lower
extremity
I87023 Postthrombotic syndrome with inflammation of bilateral
lower extremity
I87029 Postthrombotic syndrome with inflammation of unspecified
lower extremity
I8703 Postthrombotic syndrome with ulcer and inflammation
I87031 Postthrombotic syndrome with ulcer and inflammation of
right lower extremity
I87032 Postthrombotic syndrome with ulcer and inflammation of left
lower extremity
I87033 Postthrombotic syndrome with ulcer and inflammation of
bilateral lower extremity
I87039 Postthrombotic syndrome with ulcer and inflammation of
unspecified lower extremity
I8709 Postthrombotic syndrome with other complications
I87091 Postthrombotic syndrome with other complications of right
lower extremity
I87092 Postthrombotic syndrome with other complications of left
lower extremity
I87093 Postthrombotic syndrome with other complications of
bilateral lower extremity
I87099 Postthrombotic syndrome with other complications of
unspecified lower extremity
O2230 Deep phlebothrombosis in pregnancy, unspecified trimester
O2231 Deep phlebothrombosis in pregnancy, first trimester
O2232 Deep phlebothrombosis in pregnancy, second trimester
O2233 Deep phlebothrombosis in pregnancy, third trimester
O2250 Cerebral venous thrombosis in pregnancy, unspecified trimester
O2251 Cerebral venous thrombosis in pregnancy, first trimester
O2252 Cerebral venous thrombosis in pregnancy, second trimester
O2253 Cerebral venous thrombosis in pregnancy, third trimester
O2291 Venous complication in pregnancy, unspecified, first trimester
O2292 Venous complication in pregnancy, unspecified, first trimester
O2293 Venous complication in pregnancy, unspecified, first trimester
O871 Deep phlebothrombosis in the puerperium
O873 Cerebral venous thrombosis in the puerperium
O879 Venous complication in the puerperium, unspecified
O2290 Venous complication in pregnancy, unspecified, unspecified
trimester
Z7901 Long-term (current) use of anticoagulants
Z7902 Long-term (current) use of antithrombotics/antiplatelets
Z86718 Personal history of other venous thrombosis and embolism
Z8672 Personal history of thrombophlebitis
Z8679 Personal history of other diseases of the circulatory system

Pulmonary embolism—related ICD-9 codes, CPT codes, and ICD-10 codes

ICD-10
codes
Definition
I26 PE
I260 PE with acute cor pulmonale
I2601 Septic PE with acute cor pulmonale
I2602 Saddle embolus of pulmonary artery with acute cor
pulmonale
I2609 Other PE with acute cor pulmonale
I269 PE without acute cor pulmonale
I2690 Septic PE without acute cor pulmonale
I2692 Saddle embolus of pulmonary artery without acute cor
pulmonale
I2699 Other PE without acute cor pulmonale
I82890 Acute embolism and thrombosis of other specified veins
I8291 Chronic embolism an thrombosis of unspecified vein
O032 Embolism after incomplete spontaneous abortion
O037 Embolism after complete or unspecified spontaneous abortion
O047 Embolism after (induced) termination of pregnancy
O072 Embolism after failed attempted termination of pregnancy
O082 Embolism after ectopic and molar pregnancy
O88 Obstetric embolism
O882 Obstetric thromboembolism
O8821 Thromboembolism in pregnancy
O88211 Thromboembolism in pregnancy, first trimester
O88212 Thromboembolism in pregnancy, second trimester
O88213 Thromboembolism in pregnancy, third trimester
O88219 Thromboembolism in pregnancy, unspecified trimester
O8822 Thromboembolism in childbirth
O8823 Thromboembolism in the puerperium
O883 Obstetric pyemic and septic embolism
O8831 Pyemic and septic embolism in pregnancy
O88311 Pyemic and septic embolism in pregnancy, first trimester
O88312 Pyemic and septic embolism in pregnancy, second trimester
O88313 Pyemic and septic embolism in pregnancy, third trimester
O88319 Pyemic and septic embolism in pregnancy, unspecified trimester
O8832 Pyemic and septic embolism in childbirth
O8833 Pyemic and septic embolism in the puerperium
O888 Other obstetric embolism
O8881 Other embolism in pregnancy
O88811 Other embolism in pregnancy, first trimester
O88812 Other embolism in pregnancy, second trimester
O88813 Other embolism in pregnancy, third trimester
O88819 Other embolism in pregnancy, unspecified trimester
O8882 Other embolism in childbirth
O8883 Other embolism in the puerperium
T800XXA Air embolism after infusion, transfusion, and therapeutic
injection, initial encounter
T81718A Complication of other artery after a procedure, not elsewhere
classified, initial encounter
T8172XA Complication of vein after a procedure, not elsewhere
classified, initial encounter
T82817A Embolism of cardiac prosthetic devices, implants, and grafts,
initial encounter
T82818A Embolismof vascular prosthetic devices, implants, and grafts,
initial
Z7901 Long-term (current) use of anticoagulants
Z7902 Long-term (current) use of antithrombotics/antiplatelets
Z86711 Personal history of PE
Z86718 Personal history of other venous thrombosis and embolism
Z8679 Personal history of other diseases of the circulatory system

Appendix B

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Footnotes

Disclosures

This project was funded by CDC funding: DD14-1407. Dr Bratzler would like to disclose a consultancy for CDC and Sanofi Pasteur. Dr Raskob would like to disclose a consultancy and honoraria for Bayer Healthcare, BMS, Boehringer Ingelheim, Daiichi Sankyo, Janssen Pharmaceuticals, Pfizer, and ISIS Pharmaceuticals. Dr Wendelboe would like to disclose an honoraria from Bristol-Myers Squibb. None of the other authors have any disclosures.

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