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Revista Brasileira de Cancerologia
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Original Article • Rev. Bras. Cancerol. 70 (4) • 2024 • https://doi.org/10.32635/2176-9745.RBC.2024v70n4.4710 linkcopy

Open-access Work-Related Hematologic Cancers Identified in Patients at Hospital do Cancer I of the National Cancer Institute, RJ, Brazil

AuthorshipSCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Introduction:  Cancer is a disease with global public health impact and the work environment can have high concentrations of physical, chemical and biological agents, exposing workers to carcinogens.

Objective:  To evaluate the profile of cases of hematological cancers suspected of being work-related cancer.

Method:  Assessment of sociodemographic and occupational data of patients with hematological cancers to elaborate the occupational history followed by analysis of the relationship between exposure to carcinogens and cancer, considering the epidemiological criteria of temporality, biological plausibility and consistency.

Results:  22 cases evaluated demonstrated a relationship between cancer and occupational exposure, the main agents being benzene, solvents, oils, petroleum derivatives and formaldehyde, non-ionizing radiation and glues.

Conclusion:  Occupational exposure may contribute to the occurrence of work-related cancer. The occupational record is an important tool for establishing the cause-and-effect relationship between exposure to risk factors and hematological cancers, helping health professionals in the process of notifying these cases in Brazil.

Key words:
Occupational Cancer; Occupational Risks; Surveillance of the Workers Health; Hematologic Neoplasms

RESUMO

Introdução:  O câncer é uma doença de impacto para a saúde pública mundial e o ambiente de trabalho pode apresentar altas concentrações de agentes físicos, químicos e biológicos expondo os trabalhadores a agentes cancerígenos.

Objetivo:  Avaliar o perfil de casos de cânceres hematológicos suspeitos de câncer relacionado ao trabalho.

Método:  Avaliação de dados sociodemográficos e ocupacionais de pacientes com cânceres hematológicos para compor histórico ocupacional, seguida da análise da relação entre a exposição aos agentes cancerígenos e o câncer, considerando os critérios epidemiológicos de temporalidade, plausibilidade biológica e consistência.

Resultados:  Um total de 22 casos avaliados demonstrou relação entre o câncer e a exposição ocupacional, sendo os principais agentes o benzeno, solventes, óleos, derivados de petróleo e formaldeído, radiações não ionizantes e colas.

Conclusão:  A exposição ocupacional pode contribuir para a ocorrência de câncer relacionado ao trabalho. O recordatório ocupacional é uma ferramenta importante para estabelecer a relação de causa e efeito entre a exposição aos fatores de risco e os cânceres hematológicos auxiliando os profissionais de saúde no processo de notificação desses casos no Brasil.

Palavras-chave:
Câncer Ocupacional; Riscos Ocupacionais; Vigilância em Saúde do Trabalhador; Neoplasias Hematológicas

RESUMEN

Introducción:  El cáncer es una enfermedad con impacto en la salud pública global y el ambiente laboral puede tener altas concentraciones de agentes físicos, químicos y biológicos, exponiendo a los trabajadores a cancerígenos.

Objetivo:  Evaluar el perfil de los casos de cánceres hematológicos sospechosos de ser cáncer de origen laboral.

Método:  Evaluación de datos sociodemográficos y ocupacionales de pacientes con cánceres hematológicos para ensamblar la historia ocupacional seguida del análisis de la relación entre la exposición a carcinógenos y el cáncer, considerando criterios epidemiológicos de temporalidad, plausibilidad biológica y consistencia.

Resultados:  22 casos evaluados demostraron relación entre cáncer y exposición ocupacional, siendo los principales agentes benceno, solventes, aceites, derivados del petróleo y formaldehído; radiaciones no ionizantes y pegamentos.

Conclusión:  La exposición ocupacional puede contribuir a la aparición de cáncer relacionado con el trabajo. El registro ocupacional es una herramienta importante para establecer la relación de causa y efecto entre la exposición a factores de riesgo y los cánceres hematológicos, ayudando a los profesionales de la salud en el proceso de notificación de estos casos en el Brasil.

Palabras clave:
Cáncer Profesional; Riesgos Laborales; Vigilancia de la Salud del Trabajador; Neoplasias Hematológicas

INTRODUCTION

Cancer is a non-communicable disease (NCD) impacting public health, one of the main four causes of early death worldwide1. It is the second major cause of populational death in Brazil and the National Cancer Institute (INCA)2 estimates 704 thousand new cases of cancer (including non-melanoma skin cancer) for each year of the triennium 2023-2025.

The most common types of male cancer are prostate, colon and rectum, lung, stomach and oral cavity. For women, the most frequent are breast, colorectal, cervical, lung and thyroid. Of the hematological cancers, non-Hodgkin lymphoma is ranked ninth for men and tenth for women among the ten most frequent cancers in Brazil.

The rising cancer incidence is related to demographic-epidemiologic transition as ageing and increase of NCD. In addition, exposure to environmental risk factors accounts for 60% to 90% of cancers, among them those related to unhealthy diet, physical inactivity, tobacco and smoke use, chemical, biologic and physical agents found in work environment3. According to Hoff4, work-related cancer (WRC) is responsible for 4% to 40% of cancer cases, depending on the type of tumor and epidemiologic study utilized to calculate the attributable fraction. In 2015, 27% of the cases of workers affected by work-related diseases died by cancer5.

Strong evidences reveal that the appearance of hematological cancers as leukemias, lymphomas and myelomas in young adults can be associated with exposure to potentially carcinogenic chemicals as benzene and pesticides found in work environments6,7. Nevertheless, WRC persists as a nationally sub-notified disease due to technical-operational difficulties to notify at the Information System of Notifiable Health Harms (Sinan)8.

The present study described the profile of suspected WRC hematologic cancers in patients attended to at INCA's Hospital do Câncer I (HCI) for notification at Sinan.

METHOD

Descriptive study-based investigation of hematologic cancers diagnosed at the hospital. Eligible cases were selected in loco by purposive sampling after active search at INCA database. Outpatient male and female 20 years old or older patients living in the State of Rio de Janeiro, with suspected or confirmed diagnosis of leukemia, non-Hodgkin lymphoma and multiple myeloma assisted at HCI/INCA Oncology and Hematology Clinic and by Social Workers or admitted at the wards from August 2019 to March 2020 have been selected.

Structured questionnaire-based individual interviews previously pre-tested with oncologic patients with other than hematologic cancer diagnosis were conducted by skilled and trained health professionals of the Environment, Work and Cancer Department (ATATC) of the Coordination of Prevention and Surveillance (Conprev) and Social Service of HCI/INCA. Patients in poor physical and/or emotional status to respond to the interview were not eligible as well as those with positive lab tests for the following oncogenic viruses: human immunodeficiency virus (HIV), hepatitis virus B and C, human papilloma virus, human herpes viruses and Epstein Barr virus.

196 eligible patients were identified to be interviewed and respond to the questionnaire. They were invited just before their outpatient visits to join the study and, if accepted, signed the informed consent form (ICF).

However, due to COVID-19 imposed limitations, especially for cancer patients, not all the patients were interviewed. Therefore, 52 patients were approached, four refused to join (two males and two females) and eventually 48 questionnaires were applied. After reviewing the interviewees’ charts, two HIV-positive patients were rejected due to the study exclusionary criteria.

46 sociodemographic questionnaires have been applied to collect data on color/race, education, social security, month family income, tobacco and alcohol use. The patients responded to questions about labor activities in the last 20 years (working one or more years), time in each activity, workload, exposure to carcinogenic agents, for instance: have you been exposed to benzene while in this occupation? (yes/no). Histopathological confirmation of the type of cancer was obtained after reviewing the electronic chart available at INCA intranet (clinical mode).

The evaluation of the cause-and-effect relation between the cancer diagnosed and occupational exposure consisted in analyzing the responses about the occupation, time in years in activity and exposure to carcinogenic agents. Subsequently, in order to establish the positive association with WRC, six ATATC multidisciplinary professionals evaluated the occupational recall of the interviewees and attempted to find scientific literature support, especially monographs of the International Agency for Research on Cancer (IARC) which classifies certain occupational exposures as carcinogenic or acknowledged as carcinogenic7,9,10. The team's consensual decision was based on temporality, biological plausibility and consistency between the occupational activity and type of cancer diagnosed11.

The following variables were included to present the sociodemographic and occupational characteristics of the patients: sex (female, male), age-range (20-39; 40-59; 60-79; 80-99 years), skin color (White or Black), residence (Rio de Janeiro, other municipalities), family income in minimum wages (≤ 1; 2-4; >4); education (elementary, high-school, university), social security status (sickness benefit, retired, without social security, pension), occupation/job (yes, no), age when started working (5-10 years; 10-15 years; 15-20 years; 20-25 years; 25-30 years; 30-35 years; 35-40 years). In addition, the characteristics of way of life, especially tobacco use (smoker, ex-smoker, never smoked, age when started smoking, cigarettes smoked per day and age when quit smoking) and frequency of alcohol use have also been collected.

The primary sites of the neoplasms were grouped according to the International Classification of Diseases and Related Health Problems 10th edition12 (ICD-10): leukemias (acute myeloid leukemia – AML – C92.0, chronic myeloid leukemia – CML – C92.1, chronic lymphocytic leukemia – CLL – C91.1 and other leukemias – C94.7); lymphomas (non-Hodgkin lymphoma – NHL – C85.0 and unspecified lymphoma – C85.9) and multiple myeloma – MM – C90.0.

Occupational exposures were separated in ten groups: Group 1 (benzene, solvents, oils, petroleum derivatives and formaldehyde); Group 2 (glues); Group 3 (household cleaners); Group 4 (agriculture and household pesticides); Group 5 (hair dyes); Group 6 (medicines and other chemicals); Group 7 (metals); Group 8 (non-ionizing radiation); Group 9 (ionizing radiations); Group 10 (biological material).

The results were obtained and presented through descriptive statistics with absolute and relative frequency of categorical variables utilizing the software Epi Info 713.

This study is part of the research project "Identificação dos casos de câncer relacionados ao trabalho atendidos no Instituto Nacional de Câncer José Alencar Gomes da Silva", approved by INCA's Research Ethics Committee, report number 3569132 (CAAE (submission for ethical review): 70791417.4.0000.5274) in compliance with Directive 466/201214 of the National Health Council.

RESULTS

Males were predominant (56.2%) over females (43.4%) in the age-range of 20-80 years with predominance of 60-79 years of age. The majority of the interviewees claimed they were Black (54.4%), 56.5% completed elementary school, 32.6%, high-school and 10.8%, university. 76% earned between two and four minimum wages and 69.5% had no social security (Table 1).

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Table 1
Sociodemographic, life habits and occupational characteristics of patients diagnosed with hematologic cancers at HCI/INCA from 2019 to 2020 (n = 46)

All the interviewees worked in the last 20 years. The age when they started working ranged from 5 to 40 years, the most frequent were young adults (5 to 20 years).

50% claimed they quit smoking and 47.8% never smoked, only one interviewee smokes currently (2.1%). 23.9% (15-20 years of age) of them tried smoking.

Regarding alcohol use, 50% claimed they did not drink alcohol and 8.7%, rarely or never. Alcohol use during one week was higher among those who claimed they drank two or three times a week.

Non-Hodgkin lymphoma was predominant among the types of cancer with 23 cases (41.3%) followed by leukemias, 12 cases (26.0%) and multiple myeloma with 11 cases (23.9%). The distribution among subtypes of lymphomas and leukemias was: non-Hodgkin lymphoma (19 cases, 41.3%), unspecified lymphomas (four cases, 8.7%), acute myeloid leukemia (three cases, 6.5%), chronic myeloid leukemia (five cases, 10.8%), chronic lymphocytic leukemia (three cases, 6.52%), other leukemias (one case, 2.2%).

Most of the individuals claimed they have been exposed during their work life to more than one group of exposure agents, but the frequency was higher for Group 1: benzene, solvents, oils, petroleum derivatives and formaldehyde (21 cases; 95.4%) and Group 8: non-ionizing radiations (15; 68.1%). Exposure to Group 9 (Table 2) has not been reported.

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Table 2
Exposure Groups of carcinogenic agents of 22 (n) suspicious cases of work-related cancer

Professions and occupations varied widely: administrative activities (operational, accounting analysts, personnel supervisor, educational supervisor, operational supervisor, human resources assistant), commerce and services (waiter assistant, school cafeteria staff, bank staff, trader, sales, trainee in paints shop, market fair), general services (general services assistant, general services), civil construction (grinder, foreman, mason, mason aide), household (housewife), military and other professions (stamps engraver, kite manufacturer, fireworks manufacturer, car wash, mechanic, car mechanic, motor shop, driver, bus driver, ambulance driver, equipment operator, printer, taxi driver) and self-employed worker.

After analyzing suspicious WRC, the experts classified 22 cases of suspected association of work with the hematological cancer diagnosed, with predominance of the following types of cancer: non-Hodgkin lymphoma (Table 3), acute myeloid leukemia, chronic myeloid leukemia and chronic lymphocytic leukemia (Table 4) and multiple myeloma (Table 5).

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Table 3
Profile of WRC cases of non-Hodgkin lymphoma* according to age, occupation, time of activity and exposure agents (n = 11)
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Table 4
Profile of WRC cases of leukemia according to age, occupation, time in activity and carcinogenic agents (n = 7)
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Table 5
Profile of WRC cases of multiple myeloma according to age, occupation, time of work and exposure agents (n = 4)

Completed notifications of WRC cases were sent to the Health Secretary of Rio de Janeiro for further filing at Sinan.

DISCUSSION

The relation between occupational exposure and types of cancer was attributed to 22 cases in the present study, consistent with a similar study by Baldo et al.11 who notified 305 cases of the 579 investigations conducted. A research carried out by "Hospital de Câncer de Barretos (SP)" found 550 cases of the 1,063 investigations performed15 with a simplified screening questionnaire.

Black men, older than 60 years of age, who completed elementary school were predominant, with expressive participation of those who started working with less or with 15 years of age and between 16 and 20 years old and complete elementary school. This is a relevant information since cancer has a long-term latency, although the time between exposure and disease of hematologic cancer is shorter10. Vazquez et al.15 concluded in their study that 61.8% of the patients had less than eight years of education.

The majority of the participants was ex-smokers, suggesting that tobacco use may have contributed in some moment of their work life to potentialize the effects of the carcinogenic occupational exposure.

In addition, it is possible that they would be in treatment and quit smoking because of the disease. The number and percent of individuals that never smoked (47.8%) was consistent with 42.6% found in the study of Barretos (SP). Data on alcohol use indicated that half of the interviewees did not use alcohol on a regular bases, while those who did, reduced their intake to three times a week at the most.

Occupational exposure was consistent with the classification of IARC that refers acknowledged evidences between exposure and disease to 38 occupational agents, 12 exposure situations (industries and occupations), 41 agents and six circumstances as probable causes of cancer16. Specifically for hematologic cancers investigated herein, chemical agents as benzene, formaldehyde, 1,3 butadiene, antineoplastic drugs and a few pesticides and exposure to radiations and infections by oncologic viruses are relevant17,18.

Although the present study and other Brazilian investigations11,15 indicate an expressive number of WRC, only 3,693 cases (Sinan) have been notified between 2007 and 2022 in the country. However, notification is not a simple process, skilled professionals are required to conduct active search and obtain occupational recall because clinical files are missing or incomplete in that regard11,19.

Based on the results of a study which utilized Social Security information to present the distribution of benefits granted due to cancer between 2008 and 2014, Sales-Fonseca et al.20 noticed that the number of accident-related disease benefits (WRC) was 100-fold lower than social security benefits. Nevertheless, 4,263 workers were granted the benefit, higher than the cases notified at Sinan for the same period.

Failing to acknowledge the association of work with cancer is not only a Brazilian reality, it is world issue. The existing scientific literature found that in Taiwan, Norway, Australia and Singapore, for instance, there are less cases than anticipated, considering an attributable fraction of 5% for occupational factors and development of cancer21.

Nearly all the suspected cases analyzed were exposed to chemical agents of Group 1 (benzene, solvents, industrial oils and formaldehyde (21; 95.4%). Group 8 (non-ionizing radiations) stands out as well (15; 68.1%). Exposure to glues, household cleaners, pesticides, hair dyes, metals, medicines and biological material were found but in lower proportions.

The aim of the study of Azevedo and Silva et al.22 was to estimate attributable fractions to modifiable risk factors in Brazil and reached a percent of 16.79% for occupational factors related leukemias as benzene, formaldehyde, gamma radiation and chemicals utilized in industrial rubber manufacturing process.

These results are consistent with meta-analyzes to evaluate occupational exposures and risks of non-Hodgkin lymphomas from a case-control study23 conducted in Minnesota, USA between 2005 and 2009, which indicated significant associations among myelodysplastic syndromes/leukemias and exposure to benzene (odds ratio – OR = 1.77, confidence interval – CI 95%, 1.19, 2.63; and OR = 2.10, CI 95%, 1.35, 3.28, respectively). Another similar study24 conducted in Shanghai revealed the association among AML and occupational risk factors as benzene, glues and adhesives and paints and pigments.

The detailed analysis of the occupations and exposure of suspected cases revealed the variety of chemical, physical and/or biologic agents the workers were exposed to, sometimes in the same period and occupation. Cancer was diagnosed for young adults (26 years) in cases 1 and 4, an age range which contributes to the work force; these cases were exposed to carcinogenic agents as benzene and solvents and mobile use classified by IARC as Group 2B. Latency of hematologic cancers is shorter than solid tumors25.

The interviewees of seven cases currently analyzed (4, 6, 8, 27, 35, 36 and 48) reported occupational exposure to benzene in at least one occupation for years. But in 12 cases (1, 11, 12, 14, 16, 18, 23, 26, 30, 32, 40 and 44), the interviewees reported exposure to several types of solvents or gasoline. This result was expected and is well described in the literature since hematologic cancers are related to exposure to benzene26, formaldehyde27, rubber related chemical agents and vulcanization28, radiations29 among other agents.

Difficulty to interview all the cases consulted at INCA during the period analyzed (partially due to COVID-19 pandemic), identification of past exposures requiring memory retrieve (not always possible), poor implementation of occupational recall as hospital routine are some of the study limitations, in addition to efforts to schedule the interviews and poor articulation within SUS to identify and notify WRC across the health network. Routine capture of occupational recall by hospital professionals is being expected to minimize these issues, further to a more robust study currently in development including new approaches.

CONCLUSION

The present investigation showed the importance of occupational recall to establish the cause-and-effect relation of the exposures to risk factors in working environments and the appearance of hematologic cancers. It is a key tool to help health professionals in the identification of WRC cases.

  • FUNDING SOURCES
    None.

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Edited by

Publication Dates

  • Publication in this collection
    13 Jan 2025
  • Date of issue
    2024

History

  • Received
    08 May 2024
  • Accepted
    08 Oct 2024
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