Share this article on:

NYPD Cancer Incidence Rates 1995–2014 Encompassing the Entire World Trade Center Cohort

Kleinman, Eli J. MD, MPH; Christos, Paul J. PhD, MS; Gerber, Linda M. PhD; Reilly, John P. MD; Moran, William F. AD; Einstein, Andrew J. MD, PhD; Neugut, Alfred I. MD, PhD

Journal of Occupational & Environmental Medicine: October 2015 - Volume 57 - Issue 10 - p e101–e113
doi: 10.1097/JOM.0000000000000542
Online-Only

Objective: The aim of this study was to compare cancer incidence rates (CIRs), between preexposure (1995–2000) and postexposure (2002–2014) periods in the entire New York City Police Department cohort exposed to the 2001 World Trade Center (WTC) disaster.

Methods: CIR derived from active duty officer records, including postexposure data on retired officers.

Results: We observed 870 cancer cases in 859 officers (1995–2014), including 193 active duty cases pre-WTC and 677 cases (484 active duty, 193 retired) post-WTC. Overall, median CIR increased 1.44-fold compared with pre-WTC, with brain cancer increasing 3.27-fold, and kidney cancer increasing similarly. Thyroid cancer and non-Hodgkin's lymphoma increased 2.29 and 1.68-fold, respectively.

Conclusions: Findings should be interpreted cautiously, given the small number of cancers at specific sites, and possibility of confounders. However, apparent increases in cancers overall, and in highlighted sites, remain of concern, underscoring the need for continued monitoring of this cohort.

Office of the Supervising Chief Surgeon and Medical Division, Personnel Bureau, New York City Police Department, New York, NY, Department of Medicine, Division of Hematology, Bronx, NY (Dr Kleinman); Division of Biostatistics and Epidemiology, Department of Healthcare Policy and Research, Weill Cornell Medical College, New York, NY (Drs Christos and Gerber); Medical Division, New York City Police Department, New York, NY (Dr Reilly); Office of the Supervising Chief Surgeon, New York City Police Department, New York, NY (Lt Moran); Department of Medicine, Division of Cardiology, Department of Radiology, Herbert Irving Comprehensive Cancer Center, College of Physicians and Surgeons, Columbia University Medical Center and New York-Presbyterian Hospital, New York, NY (Dr Einstein); Department of Medicine, Herbert Irving Comprehensive Cancer Center, College of Physicians and Surgeons, and Department of Epidemiology, Mailman School of Public Health, Columbia University Medical Center, New York, NY (Dr Neugut).

Address correspondence to: Eli J. Kleinman, MD, MPH, Office of the Supervising Chief Surgeon, 1 Lefrak City Plaza, Suite 1644, 59-17 Junction Blvd., Corona, NY 11368 (eli.kleinman@nypd.org)

This study was funded entirely by the City of New York Police Department Medical Division, which received no Federal or State funding, nor any private or corporate grants, thus posing no conflicts of interest.

Drs Einstein and Neugut contributed equally to this manuscript.

The New York City Police Department (NYPD), one of the world's largest municipal police departments, employs nearly 40,000 uniformed officers, almost all of whom were exposed to the 2001 World Trade Center (WTC) disaster. The destruction of the WTC released a variety of toxic substances into the environment,1,21,2 which have been linked to inflammatory and sarcoid-like respiratory tract diseases, dermatologic, and gastrointestinal conditions.3–93–93–93–93–93–93–9 Although potentially carcinogenic substances have been identified in environmental samples from the various WTC sites, no specific cancers have been directly linked to these exposures. There is concern, however, that some of the reported toxins—either alone or in combination—posed carcinogenic risks,10–1510–1510–1510–1510–1510–15 perhaps via transient inflammation, mutation induction, unmasking of oncogenes, inactivation of oncogene inhibitors, immunologic, or other unidentified mechanisms.16–1916–1916–1916–19

Only a few cohort studies on cancer in police officers have been published in general, following concerns that police may be routinely exposed to a variety of potential carcinogens or stresses related to their occupation.20–2420–2420–2420–2420–24 Cancer studies were undertaken following the 2001 WTC disaster on uniformed or mixed cohorts of firefighters, other emergency responders, construction workers, and civilians, each with differing exposure histories before and after the event, and employing a variety of methodologies (ie, surveys, screening examinations), on subjects enrolled in WTC monitoring programs.25–2825–2825–2825–28

Our study examines cancer incidence rate (CIR) data in active duty officers over a 20-year period between 1995 and 2014, encompassing the entire cohort of 39,946 identically trained police officers (active and retired)29 employed on September 11, 2001, with verified histories of exposure at one or more designated WTC sites, and no significant prior history of, or ongoing work-related exposures. We specifically report overall and site-specific CIRs for the time periods 1995 to 2000 and 2002 to 2014. For the postexposure period, CIR data were recorded for the entire WTC exposed cohort (N = 39,946), both active and retired, followed from 2002 to 2014.

Back to Top | Article Outline

METHODS

In this descriptive, retrospective cohort study, we evaluated yearly CIRs, derived from the integrated personnel/medical records of active NYPD officers, from 1995 through 2014, and specifically followed the exposed September 11, 2001 cohort of 39,946 individuals, both active and retired, from 2002 to 2014. Age-adjusted CIRs were compared between the preexposure and postexposure time periods, 1995 to 2000 and 2002 to 2014, respectively, as well as evaluated yearly from 1995 through 2014.

Back to Top | Article Outline

NYPD Medical Records

Cancer information for active duty uniformed NYPD officers was extracted from comprehensive, integrated medical/personnel records—maintained from initial pre-hiring examinations until retirement—by NYPD Medical Division personnel, the only individuals authorized to review such files. Information regarding any and all visits to the Medical Division for illness or injuries, their impact on duty status, in addition to all submitted physician and hospital records, are contained therein, and archived for over 50 years.

Identification of cancer diagnoses in officers was generated via International Classification of Diseases, 9th Revision (ICD-9) code queries of our computer database, after which charts of identified cases were reviewed and verified for details, including presenting symptoms, method of diagnosis, medical reports (pathology, imaging), ICD-9 diagnosis codes, and pathologic subtypes, as was information regarding family history, predisposing cancer risk factors, and all changes in duty status. Records were mined for all relevant information pertaining to the specific cancer diagnosis in question and, when warranted, further information was obtained through personal interview.

Back to Top | Article Outline

Case Ascertainment

The NYPD medical record-keeping and pension systems make it virtually impossible for cancer diagnoses to have evaded reporting or otherwise be missed. Even when illness fails to impact duty status, or when cancer treatments have been undertaken while “off duty,” almost all cancers invariably involve surgery, chemotherapy, or radiation therapy at one time or another, resulting in some period of “limited duty” assignment. As all short and long-term changes in duty status come to the Medical Division's attention, coupled with direct oversight of authorization and payment for prescriptions and medical services, as well as finalization of all pension applications, our system ensures that cancer information is up-to-date. Although a few skin or in-situ cancers could conceivably have been missed, it should be noted that the NYS Cancer Registry does not record Basal Cell and Squamous skin cancers and does not require reporting of in-situ cancers of the cervix or prostate. Moreover, with the acknowledged multi-year lag in cancer-data updates at New York and other state tumor registries, our cancer data are complete and represent an equivalent, or a better standard.

Back to Top | Article Outline

WTC Exposure

In this internal, retrospective cohort study, years 1995 to 2000 were defined as the “preexposure” and 2002 to 2014 as the “postexposure” period. The shorter 6-year preexposure period was made necessary by the incorporation—in 1995—of the differing medical record systems of three distinct NYC police departments (Transit, Housing, and City), into one uniform database. Age-adjusted CIRs were compared between these two defined time periods, as well as evaluated yearly from 1995 to 2014.

Descriptive WTC exposure information for cancer-affected officers was derived from WTC “Notice of Participation” (benefits eligibility) documents filed by exposed officers, and subject to departmental verification procedures, via examination of Duty Rosters, Memo Books, Command Logs, Time-keeping Records, or affidavits. These documents contain specific information pertaining to

1. Exposure dates, time, and site location: (Ground Zero WTC, Chelsea Piers Temporary Morgue, Staten Island Freshkills Landfill, NYC Medical Examiner's Office locations, Hudson River Barges).

2. Type of duties: rescue/recovery operations in the presence or absence of the debris cloud, sifting debris at the Freshkills landfill, escorting WTC debris on Hudson River barges, handling remains, or property at temporary morgues or Medical Examiner's locations.

3. Duration of exposure: defined as less than 1000 hours, 1000 to 2000 hours, more than 2000 hours, in keeping with delineations used in our previous WTC pulmonary study.30

Due to the chaotic events immediately following the disaster, with rolling duties and overlapping exposures encountered by many officers at different sites, clear-cut distinctions regarding relative exposure intensities could not reliably be made. Moreover, collection of comprehensive exposure information for non–cancer-affected officers could not be realized, due to unique study constraints affecting this cohort beyond our control, as well as limited available resources. Thus, this study was not designed to test associations between exposure-dose and subsequent cancer development (ie, risk ratios could not be calculated), but rather, to follow the entire exposed September 11, 2001 cohort from 2002 to 2014, and internally comparing the CIRs with the preexposure (1995 to 2000) time period. As a result, all cited findings should be considered descriptive, for hypothesis-generation purposes.

Back to Top | Article Outline

Study Population

The NYPD WTC cohort consists of 39,946 active duty police officers in service on September 11, 2001, followed through 2014. Table 1 summarizes demographic characteristics of the cohort, for each year of the study (2002–2014).29 The cohort size (ie, all uniformed NYPD officers employed on September 11, 2001) served as the denominator for calculating the CIRs for all cancers combined and site-specific cancers for each year of the study. CIRs for 1995 to 2000 are also reported, based on the annual employed NYPD workforce for each of those “preexposure” years.

Back to Top | Article Outline

Retired Officers

Officers retired before the 2001 WTC disaster had no financial or other incentive to routinely provide cancer information to their NYPD employers. Consequently, only limited pre-9/11 cancer information for retired officers was available—from voluntarily submitted records—between 1995 and 2000, and could therefore not be entered into the comparison analysis of CIRs between the pre and postexposure time periods.

Officers who retired following their 2001 WTC exposure also had no incentive to report cancers to the NYPD, until subsequent passage of the NY State 9/11 Presumption, and Federal Compensation legislation in 2005 and 2010.31,3231,32 Thus, cancer data for this group became available only after 2005, or from voluntary participation in NYPD WTC Monitoring Program initiatives (2002, 2007, and 2012), and is now complete, up-to-date, and included in our analysis.

Back to Top | Article Outline

Smoking

“Smoker” was defined as ever-smoked and “non-smoker,” as never-smoked. The impact of smoking status on the CIR could not be fully assessed, due to legal constraints precluding NYPD employers from inquiring about lifestyle habits, and other inquiries of this nature, once hired. Information on smoking status could, thus, only be gleaned from submitted medical records, or voluntary participation in NYPD monitoring or health-fair initiatives.

Back to Top | Article Outline

Statistical Considerations

Crude incidence rates for all cancers combined and for individual cancer diagnoses were first calculated from 1995 to 2000. The total uniformed police force for each year was used as the population denominator for calculating the crude incidence rates for each year from 1995 to 2000. On September 11, 2001, the total active police force consisted of N = 39,946 officers.29 This cohort was considered “exposed” and was subsequently followed for cancer incidence from 2002 to 2014. Crude incidence rates for all cancers combined and for individual cancer diagnoses were calculated from 2002 to 2014. All yearly population denominators for 1995 to 2000, and the 2001 fixed cohort denominator that was followed from 2002 to 2014 were stratified by age group in the following categories: 21 to 30, 31 to 40, 41 to 50, 51 to 60, 61 to 70, and 70+ years of age. Yearly denominators were also stratified by gender and ethnicity (White, Black, Hispanic, Asian, and Native American).

All crude incidence rates calculated separately for each year (ie, for all cancers combined and for individual cancer diagnoses) were age-adjusted to the 2000 U.S. Standard Population to allow for direct comparison of all incidence rates across the 20-year study period. The process of age-adjustment entails applying the NYPD age-specific incidence rates (for each age-group category within a given year) to the age distribution of the 2000 U.S. Standard Population (age distribution of standard based on same age-group categories as defined above), and then calculating the expected number of cases that would have occurred in the 2000 U.S. Standard Population given the age-specific incidence rates from the NYPD cohort. The summation of the expected number of cases across all age groups, divided by the total 2000 U.S. Standard Population, constitutes the final age-adjusted incidence rate for a given year (ie, age-adjusted incidence rates calculated for all cancers combined and for individual cancer diagnoses). All age-adjusted incidence rates are expressed per 100,000 population. Median age-adjusted incidence rates for the time periods 1995 to 2000, 2002 to 2012, and 2002 to 2014 were also computed to evaluate the percent change in the median age-adjusted incidence rate between each latter defined time period and the 1995 to 2000 time period (for all cancers combined and for individual cancer diagnoses). Ninety-five percent confidence intervals (95% CIs) for all age-adjusted incidence rates were calculated to assess the precision of the obtained estimates. Because yearly incidence rates for individual cancer diagnoses were based on a small number of cancer diagnoses in the NYPD cohort, all age-adjusted incidence rates for individual cancer diagnoses should be interpreted with caution.

For comparison purposes, age-adjusted U.S. population CIRs from 1995 to 2012 (also age-adjusted to the 2000 U.S. Standard Population) were extracted using SEER*Stat 8.2.1 (Surveillance Research Program, National Cancer Institute SEER*Stat software [http://www.seer.cancer.gov/seerstat] version 8.2.1, 4/7/15).33 Median age-adjusted incidence rates for the time periods 1995 to 2000 and 2002 to 2012 (last available year was 2012 from SEER) were computed to evaluate the percent change in the median age-adjusted incidence rate between the 2002 to 2012 time period and the 1995 to 2000 time period for the U.S. population (based on SEER) (for all cancers combined and for individual cancer diagnoses). Percent change in the median age-adjusted incidence rate between the 1995 to 2000 and 2002 to 2012 defined time periods (based on SEER) was then compared with the corresponding percent change in the September 11, 2001 NYPD cohort, to evaluate whether age-adjusted incidence rate changes in the NYPD 9/11 cohort were similar or different to changes in the U.S population (based on SEER) between the two defined time periods. Wilcoxon rank-sum tests were performed to compare the median age-adjusted incidence rates for 1995 to 2000 versus 2002 to 2012 (ie, percent change), for both the NYPD cohort and SEER-based general population. However, given the large the number of site-specific cancers evaluated, all results should be considered as hypothesis-generating due to the statistical issue of multiplicity of outcomes.

Because previous WTC exposure studies typically calculated standardized incidence ratios (SIRs) to compare cancer experience in the exposed cohorts to expected rates based on the U.S. population (typically based on SEER), we also calculated select SIRs (and associated 95% CIs) by dividing the observed cases for 2002 to 2012 in the NYPD exposed cohort by the expected cases that would have occurred in 2002 to 2012 if the SEER rates were operating in the NYPD exposed cohort. Expected cases were calculated by multiplying the SEER rates for each calendar year and 10-year age group by the total number of NYPD officers (active/retired) in the same year and 10-year age group, and then summing to determine total number of expected cases in the 2002 to 2012 time period. Thus, the SIRs are considered age and calendar-year adjusted.

All P values are two-sided with statistical significance evaluated at the 0.05 alpha level. All analyses were performed in SPSS Version 23.0 (SPSS Inc., Chicago, IL) and SAS Version 9.4 (SAS Institute, Inc., Cary, NC).

Back to Top | Article Outline

RESULTS

There were 870 cancer sites reported among 854 police officers (677 active, 193 retired), between 1995 and 2014. In the preexposure period (1995–September 10, 2001), there were 193 active duty cancer cases (retired officers did not begin reporting cancers before 2005). In the postexposure period (September 11, 2001–2014), there were 677 cancer cases (484 active, 193 retired). Of the 668 individuals diagnosed with one or more cancer sites, 103 (15.42%, 72 active, 31 retired) were deceased at the close of the study.29

We observed an overall 1.44-fold increase in the median age-adjusted CIR for all cancer sites combined in exposed officers within the 2002 to 2012 postexposure period (median = 98.93 per 100,000), compared with the 1995 2000 preexposure period (median = 68.85 per 100,000) (P = 0.22) (corresponding median ratio for SEER = 0.98; P = 0.01), with a 3.27-fold increase in brain cancer (BC) (P = 0.26) (corresponding median ratio for SEER = 0.99; P = 0.50), a 3-fold increase in kidney cancer (KC) (P = 0.02) (corresponding median ratio for SEER = 1.31; P = 0.001), a 2.29-fold increase for thyroid cancer (TC) (P = 0.09) (corresponding median ratio for SEER = 1.80; P = 0.001), and a 1.68-fold increase for non-Hodgkin's lymphoma (NHL) (P = 0.39) (corresponding median ratio for SEER = 1.05; P = 0.01) (Figs. 1–5Figs. 1–5Figs. 1–5Figs. 1–5Figs. 1–5) (Table 2). Although P values are reported above, it should be noted that the NYPD yearly age-adjusted incidence rates are more variable, as compared with SEER, and thus time period analyses for the NYPD cohort are likely underpowered. Therefore, we descriptively highlight the magnitude of the percent increases between the two time periods (for both NYPD and SEER), and P values of 0.30 or less should be considered as indicative of potential trends for hypothesis-generation purposes.

Peak age-adjusted CIR increases for BC were observed in 2003, 68.28 per 100,000, and 2006, 28.61 per 100,000; for KC in 2002, 15.77 per 100,000, in 2005, 35.90 per 100,000, and 2013, 10.56 per 100,000; for TC in 2007, 10.72 per 100,000, and 2009, 19.09 per 100,000; and for NHL in 2003, 17.05 per 100,000 (Table 2).

For TC, the median age-adjusted incidence rates for 1995 to 2000, 2002 to 2012, and 2002 to 2014 were 1.79, 4.10, and 4.10 per 100,000, respectively, for NHL, 1.04, 1.75, and 1.75 per 100,000, respectively; and for primary BC, 1.04, 3.40, and 2.27 per 100,000, respectively. In the case of KC, median age-adjusted incidence rate increases postexposure could not be statistically computed, as the median CIR during 1995 to 2000 was 0 per 100,000; however, we observed similar absolute rate increases in KC, in the postexposure period (Table 2). SIRs for all cancers, TC, BC, NHL, and KC for the 2002 to 2012 time period were 0.52 (95% CI 0.48–0.56), 0.65 (95% CI 0.47–0.83), 1.21 (95% CI 0.72–1.69), 0.58 (95% CI 0.37–0.79), and 0.92 (95% CI 0.62–1.22), respectively, indicating that the NYPD 9/11/01 exposed cohort exhibited cancer rates lower than that of the general population (except for BC). However, the internal comparison of the CIR's among the NYPD population, before and after September 11, 2001, was the primary comparison of interest in this study.

Other cancer sites also showed postexposure increases, most notably, colon, lung, female breast, and acute myelogenous leukemia, whereas others showed postexposure decreases, but due to the small numbers in some, and possible surveillance bias or other confounders in others, it is not possible to reliably comment on the incidence rates for these site-specific cancers (Tables 3 and 4Tables 3 and 4).

Back to Top | Article Outline

Exposure Characteristics Among Cancer-Affected Officers

Exposure Sites/Intensity

All 668 of the individuals with post-WTC cancer diagnoses were exposed at one or more of the designated WTC sites at some time between September 11, 2001 and September 11, 2002, with (56%) of cancer-affected officers present at Ground Zero in the first 24 hours, and (81%) serving at Ground Zero sometime thereafter (between September 13, 2001 and September 11, 2002). Exposure intensity information was incomplete in a small number (14.66%) of cancer-affected officers, due to their failure to file “Notice of Participation” documents, detailing the extent of their exposure.

Back to Top | Article Outline

Exposure Duration

Five percent of cancer-affected officers were exposed for greater than 2000 hours, 7.7% between 1000 and 2000 hours, and 72% less than 1000 hours.

Back to Top | Article Outline

Smoking

Smoking history responses were available for 65.7% of the cancer-affected officers, with 16.5% of the responses classified as smokers and 49.2% as nonsmokers.

Back to Top | Article Outline

Environmental and Other Risk Modifiers

Records of individuals with notably increased cancer sites, which were deemed unlikely to have been affected by significant surveillance bias (ie, BC, KC, TC, NHL), were further reviewed for evidence of known predisposing risk factors for those specific cancers (ie, radiation or benzene exposure, history of thyroid or renal disease, family history of hematopoietic cancers),34–3934–3934–3934–3934–3934–39 as well as for evidence of other chronic, non–WTC-related workplace exposures (radiation, radar, benzene, petro-chemical). This was accomplished by cross-referencing the cancer diagnoses with officers’ residential distance (zip code <20 miles) from New York's Indian Point Nuclear facility,40–4540–4540–4540–4540–4540–45 or work assignments at NYPD Highway, Aviation, Firearms & Tactics Section or Fleet Services divisions, wherein such exposures could conceivably occur (Table 5A Table 5B).

Back to Top | Article Outline

DISCUSSION

A number of recent reviews of cancer in police officers21–2321–2321–23 have found overall incidence and mortality rates similar to those of the general population, with suggestions of increases in a variety of cancers, including thyroid, skin, male breast, gastrointestinal, testicular, lymphoproliferative, and brain, among others.20 Hypotheses regarding causation include exposure to radar and gun-cleaning solvents, in addition to the stresses of shift-work, or other possible contributory lifestyle factors.20–2320–2320–2320–23 A study of cancer in a regional NY state police cohort between 1976 and 2006 reported a general cancer risk similar to that of the general NYS regional population, with an elevated risk of Hodgkin's disease, and a slightly elevated risk of BC in officers with 30 years or more of service, the authors postulating a possible contribution of long-term exposure to radar.22

Studies of cancer among monitored uniformed responders, and mixed cohorts of responders and others, exposed to the 2001 WTC disaster—each with differing occupational exposure histories—have been undertaken through a variety of methodologies, in recent years.25–2825–2825–2825–28 Zeig-Owens et al27 reported a modest increase in overall cancer incidence in WTC-exposed firefighters when compared with the general population. Jordan et al25 found no significant association between overall mortality and degrees of exposure, in a mixed responder/nonresponder cohort. Solan et al,28 studying a mixed cohort of protective services, construction workers, cleaning/installation crews, and others, and categorizing degrees of exposure by specific parameters, reported an increased cancer risk overall, as well as for thyroid, hematopoietic/lymphoid, and prostate cancers, in the very highly exposed.

Caveats regarding these studies include the very short latency periods from exposure to cancer development, the questionable comparability of standard populations to dissimilar uniformed cohorts (firefighters, police), the inherent difficulties in defining degrees of exposure across cohorts with varying experiences and rolling duties (ie, exposure before or after the debris cloud vs sifting through landfill debris vs morgue duties, and so on), as well as the surveillance bias inherent in studying subjects enrolled in monitoring programs.46–4846–4846–48

The chief strength of our descriptive, retrospective cohort study lies in its representing a complete review of all the available cancer incidence data, between 2002 and 2014, including the entire exposed 2001 NYPD cohort of identically trained police officers, and internally comparing cancer rates between the pre and postexposure periods in active duty officers, and reporting postexposure rates in retired officers. The information on our cancer-affected officers, culled from comprehensive medical records maintained by the NYPD Medical Division, was individually verified for accuracy of diagnoses and extent of exposure, and screened for evidence of known non-WTC factors that may have contributed to the development of these cancers. Records were also examined for known characteristics predisposing individuals to BC, KC, TC and NHL, four cancers herein highlighted, which include medical or environmental radiation, radar or benzene exposure, family history of thyroid disease or cancer, preexisting renal disease or family history of KC, or family history of hematologic malignancies.33–3833–3833–3833–3833–3833–38

In view of the small number of cancer cases observed and potential for CIR instability, the issue of multiplicity of outcomes when evaluating a large number of site-specific cancers, the absence of evidence for direct causal associations between carcinogens at the WTC sites and specific cancers,11,19,4811,19,4811,19,48 and mindful of unidentified confounders that could have impacted our results, great effort was undertaken to identify potential biases. Despite some overlap in increased cancer sites reported in small police cohorts—unrelated to WTC exposure20–2320–2320–2320–23—we observed apparent elevations in rates of BC, KC, TC, and NHL in NYPD police officers in the time interval following the WTC disaster (2002 to 2014), as compared with the preexposure interval (1995 to 2000).

It is of some interest that risk also appeared to be increased for TC and NHL among WTC-exposed firefighters, who have entirely different work-related exposures and underwent extensive post-WTC surveillance.25 However, the overwhelming majority of NYPD officers diagnosed with BC, KC, TC, and NHL—sites not prominently featured in awareness campaigns, nor easily lent to self-examination—had no evidence of predisposing work exposures, and came to medical attention only as a result of serious symptomatology, and not through routine screening (Table 5).

Moreover, although TC and KC and other cancers have increased dramatically in the US since 2000 attributed to incidental detection on CT scans,49–5249–5249–5249–52 or a possible secular effect—our intimate experience with the NYPD “culture,” coupled with vigorous efforts to uncover evidence of heightened surveillance for these cases, did not suggest that this significantly accounted for the elevated CIR.

The contribution of such potential biases could not be discounted, however, for some of the more common cancers also found elevated in our cohort, which included colon, lung, female breast, and acute myelogenous leukemia. Such issues also would pertain to the site-specific cancers that were found to be reduced in the postexposure period (Table 4).

The SEER data rates (Table 2) corresponding to the highlighted cancers we report on revealed markedly higher rates of all cancers in the general population than our cohort. In comparison to the 1995 to 2000 period, the median SEER rate nearly doubled in the 2002 to 2012 period for TC, and showed a modest increase for KC, whereas the overall cancer, BC, and NHL median rates appeared relatively stable between the two time periods. The SIR—provided for consistency of reporting with other WTC cohort studies—also revealed BC slightly, but not significantly, elevated at 1.21 (95% CI 0.72–1.69).

The expected impact of the “healthy worker effect,” along with the diminished surveillance activity for these cancer sites within the NYPD cohort are likely responsible for these discrepancies, lending further credence to suggestions that using general populations as a reference standard in police studies is fraught with hazard.53–5653–5653–5653–56 Moreover, the observed tripling of rates for BC and KC, and approximate doubling of TC and NHL within the NYPD cohort between the two time periods, is troubling, particularly as these cancer-site increases are somewhat counterintuitive to sites we might have predicted to be elevated from this exposure. We, thus, remain skeptical that comparisons based on cancer rates taken from the general population more reliably reflect a reference baseline than our own internal comparison of the CIRs between the pre and postexposure periods.

As indicated above, there are a number of possible limitations to our study. The small absolute number of overall and site-specific cancers, the lack of clear evidence of cancer-causal effect of WTC exposure, and the possibility of unidentified confounders, make drawing definitive conclusions imprudent at this time.

The absence of exposure-dose data or complete information for the non–cancer-affected members of the cohort is a limitation. However, in view of the inconsistent findings of previous studies25–2825–2825–2825–28 regarding associations of WTC cancers with exposure intensity, and the unlikely changes in monitoring recommendations that would result based on nebulous distinctions between exposure categories, we chose comparison of CIRs before and after the WTC disaster as our primary focus.

In addition, due to binding labor/contract constraints, we were not permitted to routinely gather information regarding lifestyle characteristics such as smoking, obesity, and other possible cancer-risk modifiers, from our employees.57–6057–6057–6057–60 Such information was, thus, available only through review of records of cancer-affected members, or from officers’ voluntary participation in NYPD WTC monitoring campaigns.

We could not fully compare pre and post-WTC CIR for retired officers, as complete pre-9/11 cancer information for retired officers was not available in the years before 2001, and until after 2005, as there was no financial incentive for retirees to report such information, until passage of WTC Compensation legislation in 2005 and 2010,31,3231,32 after which such cancer information was forthcoming.

Another possible limitation is the short latency period for the cancers reported. The NIOSH, noting the paucity of published information regarding latencies for most cancers, recommended adoption of “plausible” latency periods for various malignancies, calling for minimum latencies of 0.4, 2.5, and 4.0 years, to be assumed for hematologic, thyroid, and other solid tumors, respectively,61 and to which we adhered, for consistency of reporting across cohorts. The cancers highlighted in our study—having no known published latencies—showed a relatively early peak for BC and KC when compared with the NIOSH assumptions, whereas those of TC, NHL, and other sites, tracked within the NIOSH-recommended time-frames (Figs. 2–5Figs. 2–5Figs. 2–5Figs. 2–5).

The NYPD cohort gender gap, still under-representing females at 17%, may somewhat underestimate TC risk, for which there is a female predilection, having risen 4% in the general population over recent years.62,6362,63

Back to Top | Article Outline

CONCLUSIONS

For the 2002 to 2012 post-WTC exposure period, the median incidence rate of cancer sites overall, among nearly 40,000 exposed NYPD police officers, appears to have increased by 1.5-fold when compared with the pre-exposure period (1995–2000). Among many cancer sites showing postexposure increases, the most notable sites unlikely to have been significantly affected by surveillance bias include brain cancer and kidney cancer, whose rates appear to have tripled compared with pre-exposure rates, as well as thyroid cancer and non-Hodgkin's lymphoma, which approximately doubled between the two time periods.

Due to the small number of overall and site-specific cancers, our findings must be interpreted with caution and as hypothesis-generating with regard to causality, as definitive conclusions cannot be drawn at this juncture. Nevertheless, despite relatively low SIRs derived from SEER data, the apparent increases in our internal comparison study, in overall cancers, and in the cancer-sites we highlight, remain of concern. More than half of the original NYPD responders have now retired, underscoring the need for continued monitoring of this cohort while the opportunity exists, particularly as many of the reported increased cancer sites long remain asymptomatic, eluding diagnosis until late stages. Research that will identify clearer linkages between WTC exposures and specific cancers, and early markers for the reported cancer sites, along with cost-effective screening strategies64–6864–6864–6864–6864–68 will help the medical community protect this cohort, and others at risk.

Back to Top | Article Outline

Acknowledgment

The authors gratefully acknowledge the Offices of the NYPD Police Commissioner and Deputy Commissioner of Personnel for their unwavering support of this study, as well as the dedicated NYPD Police Surgeons, Nurses and Medical Division staff, Interns M. Burk, M. Ciuffo B.S., Sgt. S. Davis, P.O. A. Deleone, M. Morales, J. Gordillo, for their tireless work on this project, and the assistance of Sec’y E. Leone for the considerable administrative requirements of this study.

Back to Top | Article Outline

REFERENCES

1. Lioy PJ, Weisel CP, Millette JR, et al. Characterization of the dust/smoke aerosol that settled east of the World Trade Center (WTC) in lower Manhattan after the collapse of the WTC 11 September 2001. Environ Health Perspect 2002; 110:703–714.
2. Samet JM, Geyh AS, Utell MJ. The legacy of World Trade Center dust. N Engl J Med 2007; 356:2233–2236.
3. Prezant DJ, Weiden M, Banauch GI, et al. Cough and bronchial responsiveness in firefighters at the World Trade Center site. N Engl J Med 2002; 347:806–815.
4. Skloot G, Goldman M, Fischler D, et al. Respiratory symptoms and physiologic assessment of ironworkers at the World Trade Center disaster site. Chest 2004; 125:1248–1255.
5. Banauch GI, Alleyne D, Sanchez R, et al. Persistent hyperreactivity and reactive airway dysfunction in firefighters at the World Trade Center. Am J Respir Crit Care Med 2003; 168:54–62.
6. Izbicki G, Chavko R, Banauch GI, et al. World Trade Center “sarcoid-like” granulomatous pulmonary disease in New York City Fire Department rescue workers. Chest 2007; 131:1414–1423.
7. Jordan HT, Stellman SD, Prezant D, et al. Sarcoidosis diagnosed after September 11, 2001, among adults exposed to the World Trade Center disaster. J Occup Environ Med 2011; 53:966–974.
8. Huang MJ, Li J, Liff JM, et al. Self-reported skin rash or irritation symptoms among World Trade Center Health Registry participants. J Occup Environ Med 2012; 54:451–458.
9. Li J, Brackbill RM, Stellman SD, et al. Gastroesophageal reflux symptoms and comorbid asthma and posttraumatic stress disorder following the 9/11 terrorist attacks on World Trade Center in New York City. Am J Gastroenterol 2011; 106:1933–1941.
10. U.S. EPA. 2003. EPA's Response to the World Trade Center Collapse: Challenges, Successes, and Areas for Improvement. EPA/R-03/012. Washington, DC: U.S. Environmental Protection Agency. Available at: www.epa.gov/oig/reports/2003/WTC_report_20030821.pdf. Accessed August 21, 2003.
11. McGee JK, Chen LC, Cohen MD, et al. Chemical analysis of World Trade Center fine particulate matter for use in toxicologic assessment. Environ Health Perspect 2003; 111:972–980.
12. Fox PR, Puschner B, Ebel JG. Assessment of acute injuries, exposure to environmental toxins, and five-year health surveillance of New York Police Department working dogs following the September 11, 2001, World Trade Center terrorist attack. J Am Vet Med Assoc 2008; 233:48–59.
13. Wang S, Prophete C, Soukup JM, et al. Roles of MAPK pathway activation during cytokine induction in BEAS-2B cells exposed to fine World Trade Center (WTC) dust. J Immunotoxicol 2010; 7:298–307.
14. Freeman MD, Kohles SS. Plasma levels of polychlorinated biphenyls, non-Hodgkin lymphoma, and causation. J Environ Public Health 2012; 2012:258981.
15. Knerr S, Schrenk D. Carcinogenicity of “non-dioxinlike” polychlorinated biphenyls. Crit Rev Toxicol 2006; 36:663–694.
16. Sansom OJ, Meniel V, Wilkins JA, et al. Loss of Apc allows phenotypic manifestation of the transforming properties of an endogenous K-ras oncogene in vivo. Proc Natl Acad Sci U S A 2006; 103:14122–14127.
17. Cheung KL, Lee JH, Khor TO, et al. Nrf2 knockout enhances intestinal tumorigenesis in Apc(min/+) mice due to attenuation of anti-oxidative stress pathway while potentiates inflammation. Mol Carcinog 2014; 53:77–84.
18. Vlaanderen J, Straif K, Pukkala E, et al. Occupational exposure to trichloroethylene and perchloroethylene and the risk of lymphoma, liver, and kidney cancer in four Nordic Countries. Occup Environ Med 2013; 70:393–401.
19. Rusyn I, Chiu WA, Lash LH, et al. Trichloroetnylene: mechanistic, epidemiologic and other supporting evidence of carcinogenic hazard. Pharmacol Ther 2014; 141:55–68.
20. Vena JE, Violanti JM, Marshall J, et al. Mortality of a municipal worker cohort: III. Police officers. Am J Ind Med 1986; 10:383–397.
21. Finkelstein MM. Cancer incidence among Ontario police officers. Am J Ind Med 1998; 34:157–162.
22. Wirth M, Vena JE, Smith EK, et al. The epidemiology of cancer among police officers. Am J Ind Med 2013; 56:439–453.
23. Gu JK, Charles LE, Burchifiel CM, et al. Cancer incidence among Police Officers in a U.S. northeast region: 1976-2006. Int J Emerg Ment Health 2011; 13:279–289.
24. Zuo H, Tell GS, Vollset SE, et al. Interferon-(-induced inflammatory markers and the risk of cancer: the Hordaland Health Study. Cancer 2014; 120:3370–3377.
25. Jordan HT, Brackbill RM, Cone JE, et al. Mortality among survivors of the Sept 11, 2001, World Trade Center disaster: results from the World Trade Center Health Registry cohort. Lancet 2011; 378:879–887.
26. Li J, Cone JE, Kahn AR, et al. Association between World Trade Center exposure and excess cancer risk. JAMA 2012; 308:2479–2488.
27. Zeig-Owens R, Webber MP, Hall CB, et al. Early assessment of cancer outcomes in New York City firefighters after the 9/11 attacks: an observational cohort study. Lancet 2011; 378:898–905.
28. Solan S, Wallenstein S, Shapiro M, et al. Cancer incidence in World Trade Center rescue and recovery workers, 2001-2008. Environ Health Perspect 2013; 121:699–704.
29. New York City Police Department. Personnel Bureau, Employee Management Personnel Database.
30. Kleinman EJ, Cucco RA, Martinez C, et al. Pulmonary function in a cohort of New York City Police Department emergency responders since the 2001 World Trade Center disaster. J Occup Environ Med 2011; 53:618–626.
31. NYS Legislative Bill S7456-2009 & A10741-2009 amending Chapter 104 of the laws of 2005 enacting the September 11th Worker Protection Task Force Act. Section 1 & 3 (2009).
32. James Zadroga 9/11 Health and Compensation Act of 2010 (Public Health Service Act) H.R. 847-2, Title I amendment, adding Title XXXIII.
33. Surveillance, Epidemiology, and End Results (SEER), US Population Data 1969--2011, Washington National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, 2011. Released January 2013. Available at: www.seer.cancer.gov/popdata.
34. Xu L, Li G, Wei Q, et al. Family history of cancer and risk of sporadic differentiated thyroid carcinoma. Cancer 2012; 118:1228–1235.
35. Smedby KE, Hjalgrim H. Epidemiology and etiology of mantle cell lymphoma and other non-Hodgkin lymphoma subtypes. Semin Cancer Biol 2011; 21:293–298.
36. Skarbek P, Turner D, Seftel M. Epidemiology of Non-Hodgkin Lymphoma. Transfus Apher Sci 2013; 49:133–138.
37. Lun Y, Wu X, Xia Q, et al. Hashimoto's thyroiditis as a risk factor of papillary thyroid cancer may improve cancer prognosis. Otolaryngol Head Neck Surg 2013; 148:396–402.
38. Russo P. End stage and chronic kidney disease: associations with renal cancer. Front Oncol 2012; 2:28.
39. Christensson A, Savage C, Sjoberg DD, et al. Association of cancer with moderately impaired renal function at baseline in a large, representative, population-based cohort followed for up to 30 years. Int J Cancer 2013; 133:1452–1458.
40. Mangano JJ. Geographic variation in U.S. thyroid cancer incidence and a cluster near nuclear reactors in New Jersey, New York, and Pennsylvania. Int J Health Serv 2009; 39:643–661.
41. Chen J, Moir D, Lane R, et al. An ecological study of cancer incidence in Port Hope, Ontario from 1992 to 2007. J Radiol Prot 2013; 33:227–242.
42. Boice JD Jr, Lubin JH. Occupational and environmental radiation and cancer. Cancer Causes Control 1997; 8:309–322.
43. Boice JD Jr, Bigbee WL, Mumma MT, et al. Cancer incidence in municipalities near two former nuclear materials processing facilities in Pennsylvania. Health Phys 2003; 85:678–690.
44. Ropeik D, Ropeik D. Taming Radiation Fears, New York Times, The Opinion Pages. Oct 22, 2013:A23
45. Ron E, Lubin JH, Shore RE, et al. Thyroid cancer after exposure to external radiation: a pooled analysis of seven studies. 1995. Radiat Res 2012; 178:AV43–AV60.
46. Nasseri K. Exposure on September 11, 2001, and cancer risk. JAMA 2013; 309:1344.
47. Curtin LR, Klein RJ. Statistical Notes: Direct Standardization (Age-Adjusted Death Rates). Healthy People 2000. Hyattsville, MD: National Center for Health Statistics; 1995.
48. Boyle P, Parkin DM. Statistical methods for registries. In: Jensen OM, Parkin DM, MacLennan R, et al, eds. Cancer Registration: Principles and Methods, Monograph 95. Lyon, France: International Agency for Research on Cancer; 1991:126–158.
49. Costantini AS, Benvenuti A, Vineis P, et al. Risk of leukemia and multiple myeloma associated with exposure to benzene and other organic solvents: evidence from the Italian Multicenter Case-Control Study. Am J Ind Med 2008; 51:803–811.
50. Richardson DB, Wing S, Schroeder J, et al. Ionizing radiation and chronic lymphocytic leukemia. Environ Health Perspect 2005; 113:1–5.
51. Berland LL, Silverman SG, Gore RM, et al. Managing incidental findings on abdominal CT: white paper of the ACR incidental findings committee. J Am Coll Radiol 2010; 7:754–773.
52. Looney AT, Nason GJ, McGuire BB, et al. Incidentalology: a developing urological sub-specialty. Surgeon 2014; 12:301–306.
53. Kirkeleit J, Riise T, Bjørge T, et al. The healthy worker effect in cancer incidence studies. Am J Epidemiol 2013; 177:1218–1224.
54. Shah D. Healthy worker effect phenomenon. Indian J Occup Environ Med 2009; 13:77–79.
55. Steenland K, Moe C. Epidemiology; Bias Issues. In: Frumkin H. Environmental Health from Global to Local. San Francisco, CA: Jossey-Bass; 2005:50–51.
56. Zimmerman FH. Cardiovascular disease and risk factor in law enforcement personnel: a comprehensive review. Cardiol Rev 2012; 20:159–166.
57. Ahn HS, Kim HJ, Welch HG. Korea's thyroid-cancer “epidemic” -- screening and overdiagnosis. N Engl J Med 2014; 371:1765–1767.
58. Vucenik I, Stains JP. Obesity and cancer risk: evidence, mechanisms, and recommendations. Ann N Y Acad Sci 2012; 1271:37–43.
59. Kitahara CM, Linet MS, Beane Freeman LE, et al. Cigarette smoking, alcohol intake, and thyroid cancer risk: a pooled analysis of five prospective studies in the United States. Cancer Causes Control 2012; 23:1615–1624.
60. Hakimi AA, Furberg H, Zabor EC, et al. An epidemiologic and genomic investigation into the obesity paradox in renal cell carcinoma. J Natl Cancer Inst 2013; 105:1862–1870.
61. Howard J. Minimum Latency & Types or Categories of Cancer. World Trade Center Health Program, Revision. May 1, 2013. http://www.cdc.gov/wtc/pdfs/wtchpminlatcancer2013-05-01.pdf. Accessed January 6, 2015.
62. Wirtz A, Nachreiner F. Effects of lifetime exposure to shift work on fitness for duty in police officers. Chronobiol Int 2012; 29:595–600.
63. Nixon IJ, Ganly I, Patel SG, et al. Changing trends in well differentiated thyroid carcinoma over eight decades. Int J Surg 2012; 10:618–623.
64. Pellegriti G, Frasca F, Regalbuto C, et al. Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J Cancer Epidemiol 2013; 2013:965212.
65. Rosario PW, Mineiro Filho AF, Prates BS, et al. Ultrasonographic screening for thyroid cancer in siblings of patients with apparently sporadic papillary carcinoma. Thyroid 2012; 22:805–808.
66. Udelsman R, Zhang Y. The epidemic of thyroid cancer in the United States: the role of endocrinologists and ultrasounds. Thyroid 2014; 24:472–479.
67. Minamimoto R, Senda M, Jinnouchi S, et al. Detection of thyroid cancer by an FDG-PET cancer screening program: a Japanese nation-wide survey. Anticancer Res 2014; 34:4439–4445.
68. Urquidi V, Rosser CJ, Goodison S. Molecular diagnostic trends in urological cancer: biomarkers for non-invasive diagnosis. Curr Med Chem 2012; 19:3653–3663.
Keywords:

9/11; brain cancer; cancer; exposure; kidney cancer; non-Hodgkin's lymphoma; New York City Police Department; police; September 11, 2001; thyroid cancer; World Trade Center

Copyright © 2015 by the American College of Occupational and Environmental Medicine