The destruction of the World Trade Center (WTC) towers on 11 September 2001 released many tons of aerosolized dust and smoke affecting the surrounding community [1
]. Community members, including those who lived, worked, attended schools or cleaned many of the contaminated sites, had potential for adverse health effects from acute exposures to the dust clouds created by the collapsing buildings, as well as chronic exposures to the resuspended dust or fumes from the fires that burned through December 2001 [3
]. Components of the dust and fumes included respirable particulate matter (PM10 and PM2.5), containing a combination of pulverized cement, glass fibers, asbestos, lead, and combustion products, as well as complex mixtures of volatile chemicals including polycyclic aromatic hydrocarbons, polychlorinated biphenyls, and polychlorinated furans and dioxins [7
]. Programs to monitor and treat the adverse health effects in the responders and community members were developed in the years after 9/11. These programs were eventually combined as the WTC Health Program (WTCHP) under the auspices of the Centers for Disease Control and Prevention (CDC), National Institutes of Safety and Occupational Health (NIOSH) [3
] and became law (under the James Zadroga 9/11 Health and Compensation Act H.R. 847) in 2010 for implementation in 2011. The WTCHP serves four distinct groups, the New York City Fire Department (FDNY) responders, the WTC general responders, the Pentagon/Shanksville responders, and community members (“Survivors”), each with their own Clinical Centers of Excellence (CCE). The WTC Environmental Health Center (WTC EHC) is the CCE for the survivor cohort [3
During the past decade, recruitment into these programs has been promoted by many methods, first and foremost through the involvement of numerous community-based organizations as well as multi-media campaigns including advertisements on the subway, radio, and newspapers. Individuals can also be referred to the WTCHP by their medical providers, lawyers, or community advocates. Enrollment is voluntary and must be self-initiated. Community members, called “Survivors”, must document their location and activities on 11 September 2001, as well as time periods and hours spent in the 1.5 m radius of the former WTC complex in the days and weeks following the disaster. As of 31 December 2019, 11,038 individuals were enrolled in the WTC EHC, a fraction of the estimated 500,000 people living or working in the WTC disaster area on 11 September 2001 [6
Cancer development is a complex process, and tumor progression occurs by a sequence of randomly occurring changes in genetic material by a change in cell functions such as proliferation, survival, and growth inhibition, which may take a long time [17
]. The minimum time period (i.e., latency) for cancer patients who have been exposed to WTC dust must have elapsed between the initial date of the individual’s 9/11 exposure and the date of the initial diagnosis of the individual’s cancer for the cancer to be certified. Minimum latency periods for specific types or categories of cancer were described by policy [20
Estimates of minimum latencies are available in the scientific literature for only a small number of the covered cancers associated with exposure to carcinogenic agents present in the aftermath of the 9/11 attacks (also referred to as “9/11 agents”) [20
]. Early studies suggested an unusual occurrence of multiple myeloma in a younger age group in the WTC responders [21
] and an excess incidence (19%) for all cancer sites combined among the WTC-exposed firefighters following 9/11 [3
], with prostate and thyroid cancers contributing to the excess rate. In view of these data, and the presence of multiple carcinogenic agents in the WTC dust and fumes, suggesting biologic plausibility, the WTC Health Program included most cancers as “Certifiable conditions” in October 2012 with the latency rules for specific cancer’s inclusion defined by the WTCHP [20
WTC Health Registry was established by the New York City Department of Health as an epidemiologic study to monitor and document long-term physical and mental health effects of 9/11. Participants were enrolled in the WTC Health Registry between September 2003 and November 2004 and enrollment to the WTC Health Registry is now closed. The WTC Health Registry does not provide health care. WTC EHC is a treatment and surveillance program, enrollment to WTC EHC requires certifiable physical and/or mental health disorders related to 9/11. Individuals can enroll in both the WTC Health Registry (HR) and WTC EHC. There have been reports about WTC-related cancers from FDNY and other WTC responder programs as well as cancers in affected community members by the WTC Health Registry [2
]. However, there has been no formal reports describing cancers at the WTC EHC. To fill this knowledge gap, we describe the characteristics of all reported cancers after 9/11 in the WTC EHC to facilitate future studies on cancers in community members exposed to an environmental disaster. To enhance our ability to characterize cancers, we relied on the extensive demographic, exposure, and clinical information obtained during surveillance in a clinical WTC EHC database and created an additional cancer-dedicated database with detailed information on all cancer types (WTC EHC Pan-Cancer database) [27
]. Our goal was to improve our ability to characterize individual cancer types, common characteristics across cancer types, and support subsequent studies of cancers among local community members. We now report a case series of the cancers identified in the WTC EHC and included in the WTC EHC Pan-Cancer database as of 31 December 2019.
In this study, we described the distribution of the cancer types in a cohort of community members (“Survivors”) who self-referred to the WTC EHC in New York City. The study population was racially and ethnically diverse, and almost half were women. Breast cancer is the most common cancer diagnosed in the WTC EHC, followed by prostate, thyroid and combined hematopoietic and lymphoid cancers. Differences in cancer distribution were detected between men and women and rare cancers, including male breast cancers and mesotheliomas, have been identified. We also describe high rates of patients with multiple primary cancers.
The dust, debris, and fumes from the WTC disaster contained known and suspected carcinogens, including polycyclic aromatic hydrocarbons, asbestos, benzene, and dioxins [3
], all of which are associated with multiple cancer types. Previous studies reported increased cancer rates in rescue and recovery workers exposed to the WTC dust and fumes [7
]. A pooled cohort of 29,993 US firefighters showed excess cancer mortality and incidence [37
], with significant increases in incidence of digestive and respiratory cancers, and mesothelioma. In an extended follow-up study, excess incidence of prostate and thyroid cancers was reported among rescue and recovery workers, while small but statistically significantly higher than expected rates were found for skin melanoma in both rescue and recovery workers and civilians, and female breast cancer and non-Hodgkin’s lymphoma among civilians [22
]. However, there are few studies of cancers in the local community members (“Survivors”). This paper reports characteristics of the cancers in a NIOSH designated clinical program for local community members.
We developed a pan-cancer database to facilitate understanding of the relationship between environmental exposures and cancers. Information on cancer characteristics is obtained from a careful review of pathology reports, medical records or state tumor registries with documentation of source included [27
]. Cancers are identified from self-report from currently enrolled patients, newly self-referred patients enrolling in the program, as well as from linkages with state cancer registries. Importantly, according to the NIOSH guidelines and standards, patients enrolled in the WTC EHC are required to have defined “certifiable” physical and/or mental health conditions [27
]. The availability of both cancer and cancer-free subjects in this study gave us an opportunity to investigate the possible differences between these groups, both of whom have been exposed to WTC dust. We describe a large variety of cancer types identified in the WTC EHC program. In contrast to the overall distribution of cancer types in studies of rescue and recovery workers, we report on racially and ethnically diverse population, almost half of which were women. Breast cancer is the most common cancer diagnosed in the WTC EHC, followed by prostate, thyroid and combined hematopoietic and lymphoid cancers. This finding is consistent with data from the WTC Health Registry analysis of cancers in community members [22
]. Our distribution of cancers is likely influenced by the large number of women in the WTC EHC, which is in contrast to the predominantly male responder programs. Among men, prostate and lymphoid and hematopoietic tissue cancers were the most common cancers in the WTC EHC, similar to that described for the predominantly male rescue and recovery workers [7
We also describe high rates of multiple primary cancers in the WTC EHC. Over 13% of patients had multiple primary malignancies. Over 13% of breast cancer patients in our population had a second primary cancer (13.6%) and 17% of prostate cancer patients had multiple primary cancers. Among lung cancer patients, 24.3% had multiple primary cancers. Multiple primary cancers were reported for thyroid cancer in responders [26
], which is consistent with our data.
We, as well as others, describe a large variety of cancers (41 types of cancers) as well as multiple cancers per patient among WTC-exposed local community members. The large variety of cancer types is consistent with that described in other WTC-exposed populations. The data from our pan-cancer database will allow us to investigate the involvement of key carcinogenic mechanisms and processes in the future by investigating the specific cancer characteristics and related biomarker information.
Inclusion of women in the WTC EHC allowed us to analyze cancer characteristics in this understudied group. We describe differences in cancer characteristics among women and men. Importantly, prostate cancer, lymphomas and lung cancers were the most common cancer in men, whereas breast, lung and thyroid cancers were the most common cancers in women.
Age on 11 September 2001 showed a statistically significant association with cancer risk, with a 1.09-fold greater risk for each one-year increase in general and 1.13-fold increase in prostate cancer in responders [24
]. When compared to the Surveillance, Epidemiology, and End Results (SEER) program data [38
] and cancer statistics published by the American Cancer Society [39
], there is a suggestion that many cancers in the WTC EHC are presenting at an earlier than expected age, whereas some cancer types, such as testicular cancers, are presented at older than expected age. The diverse distribution of race/ethnicity and sex in our population suggests that future studies of individual cancers in the WTC EHC program should consider these variables along with other potential confounders.
This study has important strengths. This is one of the few descriptions of cancers in WTC-exposed local community members rather than those involved in rescue and recovery activities. The diverse population of nearly 50% of women allows for the description of different cancer frequencies in women compared to men and will allow for future studies of WTC-related health effects in women. The description of a large variety of solid as well as lymphoid and hematopoietic tissue malignancies supports the diverse nature of the malignancies and the need to study these cancers as a group (pan-cancer analysis) as well as individually. As such, this study sets the stage for future studies of environmental exposure and cancer latency, cancer characteristics, and underlying mechanisms of cancer development. The finding of rare as well as common cancers in this population may provide clues about environmental exposures and the underlying mechanisms of the development of these cancers. The potential for continued follow-up of these patients will provide further insight into cancer behavior and prognosis.
There are several limitations to our study. Our population is a self-referred population and, therefore, subject to selection bias and also only cancers named as “certifiable” by the WTCHP could be included. For this reason, we cannot directly assess cancer incidence or mortality rates in this population. Our patients have been enrolled in WTC health program and they are being offered screening within this program routinely. This screening may explain the detection of some but not all cancers since many enroll with previously diagnosed cancer and we do not report overall prevalence of cancers. We may have some missing cancer diagnoses since some of our patients had cancers diagnosed before the WTCHP allowed certification and some of these patients may have died from these early cancers before we identified them for this study.