ORIGINAL ARTICLE
Occupation & Environmental Medicine http://dx.doi.org/10.3346/jkms.2014.29.8.1061 • J Korean Med Sci 2014; 29: 1061-1068
Influenza Vaccination and Associated Factors among Korean Cancer Survivors : A Cross-Sectional Analysis of the Fourth & Fifth Korea National Health and Nutrition Examination Surveys Kyung-Hyun Choi,1 Sang Min Park,2 Kiheon Lee,3 Ju Hyun Lee,4 and Joo-Sung Park5 Center for Health Promotion & Cancer Prevention, Dongnam Institute of Radiological & Medical Sciences, Busan; 2Department of Family Medicine, Seoul National University Hospital, Seoul National University College of Medicine, Seoul; 3JW LEE Center for Global Medicine and Department of Family Medicine, Seoul National University College of Medicine and Seoul National University Bundang Hospital, Seongnam; 4Department of Family Medicine, National Police Hospital, Seoul; 5 Department of Family Medicine, Dong-A University College of Medicine, Busan, Korea 1
Received: 11 March 2014 Accepted: 7 May 2014 Address for Correspondence: Sang Min Park, MD Department of Family Medicine, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea Tel: +82.2-2072-3331, Fax: +82.2-766-3276 E-mail: [email protected]
Influenza vaccination is important for cancer survivors, a population with impaired immunity. This study was designed to assess influenza vaccination patterns among Korean cancer survivors. In this cross-sectional analysis, data were obtained from standardized questionnaires from 943 cancer survivors and 41,233 non-cancer survivors who participated in the Fourth and Fifth Korea National Health and Nutrition Examination Surveys (2007-2011). We identified the adjusted influenza vaccination rates and assessed factors associated with influenza vaccination using multivariate logistic regression. Cancer survivors tended to have a higher adjusted influenza vaccination rate than the general population. The rates for influenza vaccination in specific cancer types such as stomach, hepatic, colon, and lung cancers were significantly higher than non-cancer survivors. Among all cancer survivors, those with chronic diseases, elderly subjects, and rural dwellers were more likely to receive influenza vaccination; those with cervical cancer were less likely to receive influenza vaccination. Cancer survivors were more likely to receive influenza vaccinations than non-cancer survivors, but this was not true for particular groups, especially younger cancer survivors. Cancer survivors represent a sharply growing population; therefore, immunization against influenza among cancer survivors should be concerned as their significant preventative healthcare services. Keywords: Influenza Vaccines; Cancer Survivors; Korean
INTRODUCTION Five-year relative cancer survival rates have been improving worldwide (1, 2). In Korea, the prevalence of cancer was 1,925.9 per 100,000 people in 2010; in other words, approximately 1 in 52 persons is a cancer patient (3). As the number of cancer survivors has increased, most cancer survivors require routine preventive healthcare services to maintain health and, furthermore, to improve their quality of life (4). Influenza is an important cause of acute respiratory diseases (5). Cancer survivors are considered a high-risk group for influenza and post-influenza complications (6, 7). The higher risk for influenza in cancer survivors can be due to specific conditions such as neutropenia according to chemotherapy, impaired immunity associated with disease or treatement of disease, concomitant use of corticosteroids (8). Additionally, the rates of morbidity and mortality are high among cancer survivors compared to those among the general population (9-11). Current Centers for Disease Control and Prevention guidelines
recommend annual influenza vaccinations for all immunocompromised individuals including cancer patients (12). However, despite recommendations for influenza vaccination, cancer survivors were less likely than controls to be vaccinated against influenza in some previous studies (13, 14). In particular, non-elderly adults with cancer had lower rates of influenza vaccination than their elderly counterparts in previous surveillance studies (15). It is important to clarify the rate of influenza vaccination among cancer survivors and identify the sociodemographic circumstances and behavioral factors that affect influenza vaccination rates, because these findings will help identify subgroups to be targeted by preventative interventions of cancer survivors (16). Although some studies have examined influenza vaccination rates among Korean cancer survivors, population-level data were rarely used. Previous study of influenza vaccination in Korean cancer survivors examined levels of utilization H1N1 vaccination practices and factors related to the vaccination. The present results indicated low levels of utilization and significant pre-
© 2014 The Korean Academy of Medical Sciences. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
pISSN 1011-8934 eISSN 1598-6357
Choi K-H, et al. • Influenza Vaccination and Associated Factors among Korean Cancer Survivors dictors of vaccination such as age, educational level, time since cancer diagnosis, and comorbidities (17). This study compared influenza vaccination rates between Korean cancer survivors and non-cancer survivors using data from the Fourth and Fifth Korean National Health and Nutrition Examination Survey (2007-2009, KNHANES IV and 2010-2011, KNHANES V) and investigated the factors associated with vaccination uptake.
MATERIALS AND METHODS Study population We used the data of the KNHANES IV (2007-2009) and KNHA NES V (2010-2011); these are nationwide surveys that represent the general Korean population and include comprehensive information on health status, health behavior, and sociodemographics. A stratified multistage probability sampling design was used. Face-to-face interviews were conducted at participants’ homes by trained interviewers to gather health information. Each participant gave informed consent prior to inclusion in the studies. The initial sample for the present study comprised 42,176 candidates who completed both the health interview and health examination surveys. Of these, 943 cancer survivors were selected as the study population, and 41,233 non-cancer survivors were selected as the controls. Cancer survivors in this study were defined as patients from the time of diagnosis through the remaining years of life according to the definition of National Coalition for Cancer Survivorship (NCCS). Associated factors and definition of influenza vaccination From the surveys, we collected information about various factors potentially associated with the influenza vaccination. The risk factors were divided into three groups: sociodemographic, behavioral, and clinical factors. The sociodemographic factors were current age ( < 65 yr or ≥ 65 yr), sex, education level (less than high school education, or high school education or more), marital status, household monthly income ( < 3,000,000 KRW [USD 2,682], or ≥ 3,000,000 KRW), area of residence (urban or rural), and health insurance types (medical assistance or none, government health insurance without private health insurance, government health insurance with private health insurance). The behavioral risk factors included smoking status (nonsmoker or past smoker, current smoker), alcohol consumption (nondrinker or non-risky drinker, risky drinker), physical activity (inactive, inadequately active, active), and self-perceived health status. Risky drinking was defined as alcohol consumption exceeding 3 standard drinks per day (18). Physical activity was classified as follows: inactive group (no physical activity), active group (moderate physical activity for at least 30 min per day on 5 days per week or vigorous physical activity for at least 20 min per day 3 days per week) and inadequately active group
1062 http://jkms.org
(exercised regularly but at levels that were less than sufficient) (19). Self-perceived health status was classified into two levels according to responses to the question “How do you assess your own health status?” One level included the responses: “very good,” “good”, and “fair” and the other level included the responses “poor”, and “very poor”. The clinical factors included, comorbidities, all cancer types (gastric, hepatic, colon cancer, breast, cervical, lung, thyroid and other cancers), and time since cancer diagnosis ( ≤ 5 yr, 5-10 yr, and > 10 yr). The comorbidities were hypertension, diabetes, chronic renal disease, coronary artery disease, and lung diseases such as asthma, tuberculosis, and chronic obstructive pulmonary disease. Vaccination against influenza was assessed using a self-reported answer to the following question: “Did you receive seasonal influenza (flu) vaccination during the last year?” Cancer survivors were identified using to the following question : “Have you had any cancers until now?” Statistical analysis We used a weighted population sample to reflect the sampling method and response rate. We calculated the estimated proportions and standard errors for baseline characteristics related to influenza vaccination. The statistical significance of differences between groups according to cancer status was assessed using logistic regression. We calculated the adjusted rate of influenza vaccination in non-cancer survivors versus cancer survivors, in younger individuals ( < 65 yr old), and in elderly individuals ( ≥ 65 yr old). We also examined the adjusted rate of influenza vaccination in cancer survivors according to cancer types comparing to non-cancer survivors. In addition, we calculated adjusted odds ratios (aORs) using multivariate logistic regression for all cancer controls, in the younger population ( < 65 yr old), and in the elderly population ( ≥ 65 yr old). We spilt into < 65 yr and ≥ 65 yr of age variables, because the elderly cancer patients aged 65 yr or more are very high risk groups for influenza and related deaths among well-defined risk groups (20, 21). The level of significance was set at P < 0.05. All estimates in the analysis were properly weighted to represent the general Korean population using a complex, multistage, probability sampling design. All statistical analyses were performed using STATA 10.0 (StataCorp., College Station, TX, USA). Because the survey data that we analyzed are publicly available, this study did not require the ethical approval of our Institutional Review Board.
RESULTS General patient characteristics Table 1 shows the baseline characteristics of the study population by cancer status. There were significant differences between the non-cancer controls and cancer survivors for all characteristics except physical activity and health insurance http://dx.doi.org/10.3346/jkms.2014.29.8.1061
Choi K-H, et al. • Influenza Vaccination and Associated Factors among Korean Cancer Survivors Table 1. Characteristics of non-cancer controls (n=41,233) versus cancer survivors (n=943) Variables Age (yr) < 65 ≥ 65 Sex Male Female Education ≥ High school < High school Marriage Married Not married Monthly household income (thousand KRW) ≥ 3,000 < 3,000 Area of residence Urban Rural Smoking Non or past smoker Current smoker Alcohol None Risky drinking* Physical activity† Inactive Inadequately active Active Health insurance (HI) type Medical assistance or none Government HI without private HI Government HI with private HI Self-perceived health status Very good/good/fair Poor/very poor Chronic disease‡ No Yes Cancer type Gastric Hepatic Colon Breast Uterine Cervical Lung Thyroid Others Time since cancer diagnosis (yr) 65 yr old)
Fig. 1. Adjusted rate for influenza vaccination in non-cancer survivors versus cancer survivors, adjusted for patient characteristics (age, sex, educational level, marriage status, monthly income, and residential area). *P value
Occupation & Environmental Medicine http://dx.doi.org/10.3346/jkms.2014.29.8.1061 • J Korean Med Sci 2014; 29: 1061-1068
Influenza Vaccination and Associated Factors among Korean Cancer Survivors : A Cross-Sectional Analysis of the Fourth & Fifth Korea National Health and Nutrition Examination Surveys Kyung-Hyun Choi,1 Sang Min Park,2 Kiheon Lee,3 Ju Hyun Lee,4 and Joo-Sung Park5 Center for Health Promotion & Cancer Prevention, Dongnam Institute of Radiological & Medical Sciences, Busan; 2Department of Family Medicine, Seoul National University Hospital, Seoul National University College of Medicine, Seoul; 3JW LEE Center for Global Medicine and Department of Family Medicine, Seoul National University College of Medicine and Seoul National University Bundang Hospital, Seongnam; 4Department of Family Medicine, National Police Hospital, Seoul; 5 Department of Family Medicine, Dong-A University College of Medicine, Busan, Korea 1
Received: 11 March 2014 Accepted: 7 May 2014 Address for Correspondence: Sang Min Park, MD Department of Family Medicine, Seoul National University Hospital, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 110-744, Korea Tel: +82.2-2072-3331, Fax: +82.2-766-3276 E-mail: [email protected]
Influenza vaccination is important for cancer survivors, a population with impaired immunity. This study was designed to assess influenza vaccination patterns among Korean cancer survivors. In this cross-sectional analysis, data were obtained from standardized questionnaires from 943 cancer survivors and 41,233 non-cancer survivors who participated in the Fourth and Fifth Korea National Health and Nutrition Examination Surveys (2007-2011). We identified the adjusted influenza vaccination rates and assessed factors associated with influenza vaccination using multivariate logistic regression. Cancer survivors tended to have a higher adjusted influenza vaccination rate than the general population. The rates for influenza vaccination in specific cancer types such as stomach, hepatic, colon, and lung cancers were significantly higher than non-cancer survivors. Among all cancer survivors, those with chronic diseases, elderly subjects, and rural dwellers were more likely to receive influenza vaccination; those with cervical cancer were less likely to receive influenza vaccination. Cancer survivors were more likely to receive influenza vaccinations than non-cancer survivors, but this was not true for particular groups, especially younger cancer survivors. Cancer survivors represent a sharply growing population; therefore, immunization against influenza among cancer survivors should be concerned as their significant preventative healthcare services. Keywords: Influenza Vaccines; Cancer Survivors; Korean
INTRODUCTION Five-year relative cancer survival rates have been improving worldwide (1, 2). In Korea, the prevalence of cancer was 1,925.9 per 100,000 people in 2010; in other words, approximately 1 in 52 persons is a cancer patient (3). As the number of cancer survivors has increased, most cancer survivors require routine preventive healthcare services to maintain health and, furthermore, to improve their quality of life (4). Influenza is an important cause of acute respiratory diseases (5). Cancer survivors are considered a high-risk group for influenza and post-influenza complications (6, 7). The higher risk for influenza in cancer survivors can be due to specific conditions such as neutropenia according to chemotherapy, impaired immunity associated with disease or treatement of disease, concomitant use of corticosteroids (8). Additionally, the rates of morbidity and mortality are high among cancer survivors compared to those among the general population (9-11). Current Centers for Disease Control and Prevention guidelines
recommend annual influenza vaccinations for all immunocompromised individuals including cancer patients (12). However, despite recommendations for influenza vaccination, cancer survivors were less likely than controls to be vaccinated against influenza in some previous studies (13, 14). In particular, non-elderly adults with cancer had lower rates of influenza vaccination than their elderly counterparts in previous surveillance studies (15). It is important to clarify the rate of influenza vaccination among cancer survivors and identify the sociodemographic circumstances and behavioral factors that affect influenza vaccination rates, because these findings will help identify subgroups to be targeted by preventative interventions of cancer survivors (16). Although some studies have examined influenza vaccination rates among Korean cancer survivors, population-level data were rarely used. Previous study of influenza vaccination in Korean cancer survivors examined levels of utilization H1N1 vaccination practices and factors related to the vaccination. The present results indicated low levels of utilization and significant pre-
© 2014 The Korean Academy of Medical Sciences. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
pISSN 1011-8934 eISSN 1598-6357
Choi K-H, et al. • Influenza Vaccination and Associated Factors among Korean Cancer Survivors dictors of vaccination such as age, educational level, time since cancer diagnosis, and comorbidities (17). This study compared influenza vaccination rates between Korean cancer survivors and non-cancer survivors using data from the Fourth and Fifth Korean National Health and Nutrition Examination Survey (2007-2009, KNHANES IV and 2010-2011, KNHANES V) and investigated the factors associated with vaccination uptake.
MATERIALS AND METHODS Study population We used the data of the KNHANES IV (2007-2009) and KNHA NES V (2010-2011); these are nationwide surveys that represent the general Korean population and include comprehensive information on health status, health behavior, and sociodemographics. A stratified multistage probability sampling design was used. Face-to-face interviews were conducted at participants’ homes by trained interviewers to gather health information. Each participant gave informed consent prior to inclusion in the studies. The initial sample for the present study comprised 42,176 candidates who completed both the health interview and health examination surveys. Of these, 943 cancer survivors were selected as the study population, and 41,233 non-cancer survivors were selected as the controls. Cancer survivors in this study were defined as patients from the time of diagnosis through the remaining years of life according to the definition of National Coalition for Cancer Survivorship (NCCS). Associated factors and definition of influenza vaccination From the surveys, we collected information about various factors potentially associated with the influenza vaccination. The risk factors were divided into three groups: sociodemographic, behavioral, and clinical factors. The sociodemographic factors were current age ( < 65 yr or ≥ 65 yr), sex, education level (less than high school education, or high school education or more), marital status, household monthly income ( < 3,000,000 KRW [USD 2,682], or ≥ 3,000,000 KRW), area of residence (urban or rural), and health insurance types (medical assistance or none, government health insurance without private health insurance, government health insurance with private health insurance). The behavioral risk factors included smoking status (nonsmoker or past smoker, current smoker), alcohol consumption (nondrinker or non-risky drinker, risky drinker), physical activity (inactive, inadequately active, active), and self-perceived health status. Risky drinking was defined as alcohol consumption exceeding 3 standard drinks per day (18). Physical activity was classified as follows: inactive group (no physical activity), active group (moderate physical activity for at least 30 min per day on 5 days per week or vigorous physical activity for at least 20 min per day 3 days per week) and inadequately active group
1062 http://jkms.org
(exercised regularly but at levels that were less than sufficient) (19). Self-perceived health status was classified into two levels according to responses to the question “How do you assess your own health status?” One level included the responses: “very good,” “good”, and “fair” and the other level included the responses “poor”, and “very poor”. The clinical factors included, comorbidities, all cancer types (gastric, hepatic, colon cancer, breast, cervical, lung, thyroid and other cancers), and time since cancer diagnosis ( ≤ 5 yr, 5-10 yr, and > 10 yr). The comorbidities were hypertension, diabetes, chronic renal disease, coronary artery disease, and lung diseases such as asthma, tuberculosis, and chronic obstructive pulmonary disease. Vaccination against influenza was assessed using a self-reported answer to the following question: “Did you receive seasonal influenza (flu) vaccination during the last year?” Cancer survivors were identified using to the following question : “Have you had any cancers until now?” Statistical analysis We used a weighted population sample to reflect the sampling method and response rate. We calculated the estimated proportions and standard errors for baseline characteristics related to influenza vaccination. The statistical significance of differences between groups according to cancer status was assessed using logistic regression. We calculated the adjusted rate of influenza vaccination in non-cancer survivors versus cancer survivors, in younger individuals ( < 65 yr old), and in elderly individuals ( ≥ 65 yr old). We also examined the adjusted rate of influenza vaccination in cancer survivors according to cancer types comparing to non-cancer survivors. In addition, we calculated adjusted odds ratios (aORs) using multivariate logistic regression for all cancer controls, in the younger population ( < 65 yr old), and in the elderly population ( ≥ 65 yr old). We spilt into < 65 yr and ≥ 65 yr of age variables, because the elderly cancer patients aged 65 yr or more are very high risk groups for influenza and related deaths among well-defined risk groups (20, 21). The level of significance was set at P < 0.05. All estimates in the analysis were properly weighted to represent the general Korean population using a complex, multistage, probability sampling design. All statistical analyses were performed using STATA 10.0 (StataCorp., College Station, TX, USA). Because the survey data that we analyzed are publicly available, this study did not require the ethical approval of our Institutional Review Board.
RESULTS General patient characteristics Table 1 shows the baseline characteristics of the study population by cancer status. There were significant differences between the non-cancer controls and cancer survivors for all characteristics except physical activity and health insurance http://dx.doi.org/10.3346/jkms.2014.29.8.1061
Choi K-H, et al. • Influenza Vaccination and Associated Factors among Korean Cancer Survivors Table 1. Characteristics of non-cancer controls (n=41,233) versus cancer survivors (n=943) Variables Age (yr) < 65 ≥ 65 Sex Male Female Education ≥ High school < High school Marriage Married Not married Monthly household income (thousand KRW) ≥ 3,000 < 3,000 Area of residence Urban Rural Smoking Non or past smoker Current smoker Alcohol None Risky drinking* Physical activity† Inactive Inadequately active Active Health insurance (HI) type Medical assistance or none Government HI without private HI Government HI with private HI Self-perceived health status Very good/good/fair Poor/very poor Chronic disease‡ No Yes Cancer type Gastric Hepatic Colon Breast Uterine Cervical Lung Thyroid Others Time since cancer diagnosis (yr) 65 yr old)
Fig. 1. Adjusted rate for influenza vaccination in non-cancer survivors versus cancer survivors, adjusted for patient characteristics (age, sex, educational level, marriage status, monthly income, and residential area). *P value
