Uptake of vaccination in older Indian patients with cancer: A cross-sectional observational study : Cancer Research, Statistics, and Treatment

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Original Article – Geriatric Oncology Section

Uptake of vaccination in older Indian patients with cancer: A cross-sectional observational study

Sabu, Tabitha M.; Noronha, Vanita; Rao, Abhijith R.1; Kumar, Anita; Gattani, Shreya2; Ramaswamy, Anant; Pillai, Anupa; Dhekale, Ratan3; Castelino, Renita4; Kumar, Sharath5; Sehgal, Arshiya5; Rana, Pallavi6; Gota, Vikram5; Badwe, Rajendra7; Prabhash, Kumar

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Cancer Research, Statistics, and Treatment 6(1):p 52-61, Jan–Mar 2023. | DOI: 10.4103/crst.crst_29_23
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Abstract

INTRODUCTION

Infectious diseases are a major cause of morbidity and mortality among patients with cancer. It is estimated that around 60% of cancer-related deaths are due to infections.[1] This is because the changes in the immune system caused by chemotherapy and disease result in an attenuated immune response.[1,2] Older patients with cancer have an added susceptibility to infectious diseases because of comorbidities and immunosenescence.[3,4]

Vaccination is an effective intervention that results in a substantial decrease in mortality and morbidity of infectious diseases.[5] While there is a well-structured immunization schedule for the pediatric population, adult vaccination is often approached casually.[6] The Indian Geriatric Society recommends the annual administration of influenza, pneumococcal, Tdap (tetanus, diphtheria, and acellular pertussis), and herpes zoster vaccines for all healthy elderly.[7] The Association of Physicians of India (API) recommends the annual influenza, pneumococcal, hepatitis B, herpes zoster, varicella, and typhoid vaccines for all unvaccinated adults as per specified schedules.[8] However, the actual reach and acceptance of vaccines remain low.[6]

India is estimated to have a substantial burden of mortality and morbidity attributable to vaccine-preventable diseases (VPDs) in the general population.[9] As per the data from the National Center for Disease Control, India reported 1,15,630 cases of influenza (H1N1) infections from 2010 to 2017, accounting for 8865 deaths.[10] In the year 2022, there were 13,202 cases and 410 deaths caused by influenza infection.[11] There is a high incidence of pneumonia during and after treatment in patients with cancer, with an estimated incidence rate ratio (IRR) of 5.34 in solid organ cancers and 32.8 in patients with hematological malignancies when compared to those without cancer.[12] Before the COVID-19 pandemic, studies had reported that pneumococcus and influenza were common infections with fatal courses in patients with cancer. These were followed by human immunodeficiency virus (HIV) and parasitic infections.[2]

The Infectious Disease Society of America (IDSA) recommends pneumococcal and inactivated influenza vaccines for all patients with cancer who are aged 6 months and over, excluding patients on anti-B-cell-directed therapy and those on the induction or consolidation phase of leukemia treatment.[13] The optimum time for vaccination to achieve maximum efficacy in patients with cancer planned for chemotherapy is uncertain; it depends on the severity of immunosuppression caused by the chemotherapy.[14] Administering inactivated vaccines during chemotherapy is less effective due to diminished seroconversion; there is a possibility of infection from live vaccines due to the attenuated immune response engendered by the chemotherapy.[15] A review on the guidelines and safety practices of vaccination in patients with cancer suggested that a practical approach would be an administration of inactivated vaccines 2 weeks before initiating chemotherapy and live vaccines 3 to 6 months after the completion of chemotherapy.[16]

In a study on influenza and pneumococcal vaccination during the influenza (H1N1) pandemic in 2009, it was found that there was an adequate response albeit with lower antibody titers in patients on chemotherapy compared with that in the normal population. However, the post-vaccine antibody titers were not adequate in patients receiving rituximab.[17] A study on the immunogenic response to the pneumococcal conjugate vaccine in patients with solid tumors reported similar antibody titers whether vaccination was given on the first day or 2 weeks before chemotherapy.[18] Another study on the antibody response to influenza vaccine in patients with breast and colon cancers reported adequate antibody titers following vaccination after the initiation of chemotherapy. The titers were significantly lower in patients with breast cancer who were vaccinated after starting chemotherapy compared with those in patients who were vaccinated 2 weeks earlier. The study also reported comparable antibody titers between patients with colon cancer who received vaccination 2 weeks before and after the initiation of chemotherapy. The lower seroconversion in patients with breast cancer after the initiation of chemotherapy was attributed to more severe immunosuppressive chemotherapy.[19] The studies in patients with hematological malignancies reported inadequate seroconversion post-vaccination after the initiation of chemotherapy due to the severe bone marrow suppression by the chemotherapy drugs used in hematological malignancies.[20,21]

Immunogenic response to a vaccine can only be assured if vaccination is administered before starting chemotherapy and recommendations favor inactivated vaccine administration 2 weeks before the initiation of chemotherapy.[13] After the administration of chemotherapy, the vaccine response may be attenuated or not achieved.[17,19–21] Delaying cancer treatment for an appropriate vaccine response may not be feasible. Thus, understanding vaccine uptake in the general population and particularly, in older patients with cancer is of prime importance. We aimed to study this in our older patients with cancer.

MATERIALS AND METHODS

General study details

This cross-sectional observational study was conducted from February 2020 to January 2023 in the geriatric oncology outpatient clinic of the Department of Medical Oncology at the Tata Memorial Hospital, a tertiary cancer hospital in Mumbai, India. This study was a part of the overall study (project number 900596) approved by the institutional ethics committee (IEC) on March 20, 2020 (study protocol provided as Supplementary Appendix 1), and was registered with the Clinical Trials Registry of India, CTRI/2020/04/024675. Written informed consent was obtained from all patients enrolled after the date of the IEC approval. The IEC waived the requirement to obtain written informed consent for the patients who had been evaluated in the clinic before the approval date. The study was conducted according to the ethical guidelines established by the Declaration of Helsinki and Good Clinical Practice guidelines. There was no funding for this study.

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Supplementary Appendix 1

Participants

We included all patients aged 60 years and above with a diagnosis of cancer, who presented to the geriatric oncology clinic during the study period. Patients were asked in detail about their vaccination status, and their responses were noted. Patients who were unsure about their vaccination status were excluded.

Aims/objectives

Our primary endpoint was the proportion of patients who had received vaccination against influenza and pneumococcal infections. We also aimed to determine the proportion of patients who had received COVID-19 vaccination before their visit to our clinic. The secondary endpoint was to identify factors that correlated with vaccine uptake.

Study methodology

We asked all the patients who presented to the geriatric oncology clinic about their vaccination history, including whether they had been advised and whether they had received any vaccines, specifically influenza, pneumococcal, and COVID-19. All the patients underwent a geriatric assessment, and their clinicodemographic data were recorded, including age, sex, education (illiterate/studied up to 9th standard/10th standard and beyond), zone of residence, marital status, type of primary tumor, and comorbidities. The patients’ home states were categorized according to the Zonal Council of India into north, south, east, west, and central zones.[22] Patients were asked about their immunization status, and their responses were noted. The data from the geriatric oncology clinic are prospectively entered in real time in a database. This database was accessed to obtain the patient details for this study. We used the search term “vaccination,” to identify patients eligible for the study.

Statistics

This was a time-bound observational study over a period of 3 years, and hence, we did not perform a formal sample size calculation. All statistical analyses were performed using the Statistical Package for the Social Sciences (IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.). The socio-demographic characteristics were described using descriptive statistics. Normally distributed quantitative variables were represented as means with standard deviations (SDs), and categorical variables were reported in absolute numbers and percentages. Vaccine uptake was calculated as the percentage of patients who had received the vaccine among the study cohort. The uptake of the COVID-19 vaccination was calculated from the time that COVID-19 vaccination was available to patients aged ≥60 years, that is, from March 2021 onwards. The association of the vaccination uptake with age, sex, education, geographical place of residence, marital status, comorbidities, and primary tumor was evaluated by a logistic regression model. A P value of less than 0.05 was considered significant.

RESULTS

A total of 1767 patients were evaluated in the geriatric oncology outpatient clinic from February 2020 to January 2023. Five patients were excluded from the study as they were unsure about their vaccination status and did not have their immunization records. Thus, we enrolled 1762 patients in the study. The clinicodemographic profile of these patients is shown in Table 1.

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Table 1:
Clinicodemographic profile of older patients with cancer enrolled in the study evaluating their vaccination status

Only 12 (0.68%) patients had received both pneumococcal and influenza vaccines; one (0.06%) patient had received the influenza vaccine alone. Thus, the total uptake of influenza vaccine was 13 (0.7%). Figure 1 shows the uptake of pneumococcal and influenza vaccines in the study cohort. Table 2 shows the vaccine uptake of the patients evaluated in the geriatric oncology outpatient clinic. In the 684 patients with lung cancer, the uptake of pneumococcal and influenza vaccines was 0.6% (n = 4) and 0.7% (n = 5), respectively. Five (0.76%) of the 661 patients with gastrointestinal tract cancer, two (0.9%) of the 220 with genitourinary cancer, and one (2.5%) of the 40 patients with other types of cancers had received both influenza and pneumococcal vaccines. Of the 1562 patients assessed in the clinic from March 2021 onwards, 1302 (83.3%) had received at least one dose of COVID-19 vaccine.

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Figure 1:
Uptake of pneumococcal and influenza vaccines in older Indian patients with cancer
T2
Table 2:
Vaccine uptake in our cohort of older patients with cancer evaluated in the geriatric oncology outpatient clinic

On univariate logistic regression, there was a statistically significant increase in the COVID-19 vaccine uptake among patients with higher education and married people, who were found to have a greater uptake when compared to unmarried and widow/widower. Patients with carcinoma of the gastrointestinal tract and lung were found to have a significantly higher vaccination uptake when compared to patients with head-and-neck cancer. There was a significantly lower uptake of COVID-19 vaccination in patients from the west zone when compared with those from the central zone. Table 3 shows the univariate logistic regression and Figure 2 shows the forest plot of the odds ratios for the factors analyzed in the uptake of COVID-19 vaccination.

T3
Table 3:
Univariate logistic regression of COVID-19 vaccine uptake with various factors
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Figure 2:
Forest plot showing the odds ratios for the factors analyzed in the uptake of COVID-19 vaccination. An odds ratio of more than one indicates greater uptake, and less than one indicates lesser uptake with respect to the reference population. A P value of less than 0.05 is significant. C.I.= confidence interval; education <10 and >10 indicates education to less than Std 10 and education up to Std 10 and beyond

DISCUSSION

In our study on 1762 older Indian patients with cancer, only 12 (0.68%) had received the pneumococcal vaccine and 13 (0.7%) had received the influenza vaccine. This sobering finding echoed those of other studies from India. A study by Rizvi et al.[9] on 64,714 patients aged above 45 years with chronic diseases (including diabetes, hypertension, chronic obstructive pulmonary disease [COPD], and cancer) found that only 1315 (uptake, 1.5%; 95% CI, 1.4-1.6) had received the influenza vaccination, and 580 (uptake, 0.6%; 95% CI, 0.6-0.7) had received the pneumococcal vaccines. A study from North India on 149 patients with diabetes found the uptake of pneumococcal vaccine and influenza vaccine to be 1 (0.7%) and 3 (2%), respectively.[23] In a study in Rajasthan on pregnant patients with influenza infection, it was found that none of them had been previously vaccinated.[24] Lack of awareness, safety concerns, superstitions, and beliefs have been cited as causes for the low vaccine uptake in India.[25] In the study by Geneev et al.,[23] financial constraints were a major factor contributing to the decreased uptake of pneumococcal and influenza vaccines. It was found that 51.4% of patients refused vaccination even after counseling due to the unaffordability of the vaccine cost. There is a scarcity of data from India on the uptake of influenza and pneumococcal vaccines in patients with cancer. An earlier study revealed that 3% of older Indian patients with cancer had received influenza and pneumococcal vaccines.[26] A study conducted in Vienna on patients with cancer reported that 18% of their patients had taken the influenza vaccine.[27]

A surveillance study by the Center for Disease Control (CDC) reported that 64% of American patients with cancer were immunized with the seasonal influenza vaccine.[28] The higher uptake of influenza and pneumococcal vaccines in patients with cancer in the United States of America (USA) is a reflection of the higher vaccination uptake in the general Western population. As per the 2018 data, around 65% of the population aged 65 years and older were vaccinated with the annual influenza vaccine in the USA and 69% of them had received the pneumococcal vaccine.[29] As per 2020 data, 70% of the Canadian population aged 65 years and over had received the influenza vaccine.[30] In 2022, more than 82% of people aged 65 years and over in the United Kingdom (UK) had received the annual influenza vaccine.[31] In contrast to this, studies from African countries have reported an uptake of less than 1% for influenza and pneumococcal vaccines.[32] A study in Saudi Arabia on diabetic patients reported an uptake of 2.8% and 47.8% for pneumococcal and influenza vaccines, respectively.[33]

To increase the uptake of recommended vaccines, the UK followed a strategy which focused on prompt identification of the eligible population and effective communication regarding the need for vaccination to the identified population.[34]

Studies have revealed that the incidence of community-acquired pneumonia in patients with cancer is 21- to 50-fold higher than that of the general population.[35,36] Patients with lung cancer have an increased risk of community-acquired pneumonia compared to patients with cancer arising at other anatomical sites.[37] Of the 684 patients with primary lung cancer in our study, only five (0.7%) had received the influenza vaccine and four (0.6%) had received the pneumococcal vaccine. The extremely low vaccination uptake in these patients is an added hurdle for effective cancer management.

There are very few follow-up studies on vaccinated patients with cancer. A study on the incidence of pneumonia and hospitalization among patients with cancer reported a lower incidence of pneumonia, less severity, and lower mortality rates in patients who had received the pneumococcal vaccine as compared to unvaccinated patients.[38] This study, which showed a survival benefit in vaccinated patients, further emphasizes the role of vaccination in comprehensive cancer care.

COVID-19 vaccination was introduced in India on January 16, 2021. Older adults and patients with cancer were prioritized to receive the vaccine and were included in the group of persons eligible for vaccination from March 1, 2021.[39] We included 1562 patients in our study after the nationwide introduction of the COVID-19 vaccine; 1302 of these patients (83.3%) were vaccinated with at least one dose of the COVID-19 vaccine before presentation to the geriatric oncology clinic. Earlier on in the pandemic, there was a considerable degree of vaccine hesitancy for COVID-19 vaccination among the eligible population in India.[40] According to the World Health Organization (WHO), vaccine hesitancy is defined as a delay in acceptance or refusal of the vaccine despite its availability.[41] A study conducted at the Tata Memorial Hospital, Mumbai, reported vaccine hesitancy in 60% of the patients with cancer who were 45 years or more. This study was conducted in May 2021, following the introduction of COVID-19 vaccine.[42] A study in Delhi (from March 2021 to June 2021) reported vaccine hesitancy in 29% of the patients with cancer.[43] There was an intensive systematic drive nationally and globally to eliminate hesitancy for COVID-19 vaccination.[44] India has administered more than 2.19 billion COVID-19 vaccinations. As per the updated data until December 2022, more than 95% of the eligible population had received at least one dose of the COVID-19 vaccine.[39] The intense vaccination drive during the pandemic to save lives and livelihoods was reflected in the increased acceptance of the COVID-19 vaccine.

We found that individuals who were married and those who had higher education were more likely to have received the COVID-19 vaccine. There was a lower vaccine uptake in the west zone of India when compared to central India. A significant increase in vaccine uptake was seen in patients with lung cancer and gastrointestinal cancer, when compared to that in patients with head-and-neck cancer. An increased vaccination uptake with higher education has been reported in previous studies as well. In the study by Dhalaria et al.[40] on factors affecting COVID-19 vaccination uptake, it was found that people who had more than 10 years of schooling had higher acceptance than people who had less than 10 years of schooling. Higher education was associated with increased COVID-19 vaccination uptake in the study by Joshi et al. as well.[45] We also found increased uptake of vaccination among married people compared with that in unmarried and widowed persons. In a study from Bangladesh by Rahman et al.,[46] married people were found to have a higher acceptance of COVID-19 vaccination. A study in Saudi Arabia also found a statistically significant increase in the uptake of COVID-19 vaccination in the married population.[47]

In our study, there was a lower uptake of vaccination in the west zone when compared to that in the middle zone. Dhalaria et al. in their study on COVID-19 vaccine coverage in India found a relatively high vaccination uptake in Himachal Pradesh, Jammu, Kashmir, Karnataka, Goa, Sikkim, and Telangana. Low vaccine coverage was found in Jharkhand, Bihar, Meghalaya, Nagaland, Mizoram, Punjab, and Manipur. The study by Dhalaria et al.[40] also found a disparity between different states with regard to vaccine hesitancy; Nagaland had the highest vaccine hesitancy (47%), and Goa had the lowest vaccine hesitancy at 5%.

We also found a significantly higher uptake of COVID-19 vaccination in patients with cancers of the lung and gastrointestinal tract, when compared to that in patients with cancer of the head-and-neck. This was in accordance with the study by Noronha et al.,[42] where a high COVID-19 vaccine hesitancy was reported in patients with head-and-neck cancer compared with that in patients with lung cancer. A higher vaccine hesitancy can be reflected as a lower vaccine uptake.[40] Vaccination uptake is more in patients with preexisting lung conditions such as COPD.[48] Symptoms of lung cancer overlap with those of COPD or pneumonia.[49] This previous lung pathology can be a possible reason for increased vaccination uptake in patients with lung cancer.

Most of the patients (1342, 76%) in our cohort of older Indian patients with cancer were male. This was similar to what was noted in the study by Ximenes et al.[50] on older patients with cancer, which also had a male preponderance. The mean age of our study population was 68.4 (± 5.8) years; the majority (60%) were below 70 years, which was also similar to that of the study cohort of Ximenes et al. where 70% of the study population was below 75 years. The majority of the patients in our study were married (1444, 82%). Approximately half (928, 53%) had comorbidities such as diabetes, hypertension, cardiovascular disease, or COPD. The primary tumor was lung in 684 (39%), gastrointestinal tract in 661 (38%), urogenital in 220 (12%), head-and-neck in 157 (8.9%), and cancer of other anatomical sites in 40 (2.3%). This was similar to the study on older patients with cancer by Soni et al.,[51] where the majority of the study cohort (>88%) were married, and the most common cancer was lung cancer (45.6%), followed by cancer of the gastrointestinal tract.

Vaccination has been recognized as one of the best investments in the health sector. The Global Vaccine Action Plan in 2021 and the Immunization Agenda 2030 aim to intensify the reach of vaccination. It is estimated that around 3.5-5 million deaths are prevented every year by immunization.[52] The very low uptake of pneumonia and influenza vaccine noted in our study was similar to the results from other studies performed in other parts of India, which also reported low uptake of less than 2% of these vaccines.[9,23] The study unmasks the need for more stringent measures to increase the uptake of pneumococcal and influenza vaccines. Higher education and recommendation by doctors are factors for increased vaccine uptake.[42] CDC recommends the assessment of the immunization status of every patient at every visit.[53] In a study on physicians to assess the factors that caused failure to prescribe recommended vaccinations, it was found that the reason the majority (59.8%) of physicians failed to prescribe the recommended vaccinations was that they had forgotten.[54]

Patients with comorbidities are more likely to get vaccinated than healthy persons due to prior exposure to the medical service.[55] In our study, there was no difference in vaccination uptake between patients with comorbidities and those without, which revealed that previous exposure to the healthcare facility did not cause any significant increase in vaccine uptake. This warrants aggressive counseling for immunization by medical professionals.

There were a few limitations to our study. We were unable to analyze the financial status of the patients. This could be an important factor for the uptake of vaccines, especially for pneumococcal and influenza vaccines. We could not analyze the factors influencing the uptake of pneumococcal and influenza vaccines, as the number of patients who had received these vaccines was very small. We were unable to follow up on these patients to assess the oncological outcomes, and the subsequent development of vaccine-preventable diseases was not recorded.

Our study conducted over 3 years on a relatively large cohort revealed a distressingly low uptake of the pneumococcal and influenza vaccines. This information is extremely relevant in the context of cancer treatment as pneumococcal and influenza infections have a catastrophic course in patients with cancer.[12,56] Electronic reminders, familiarization with guidelines, and reviewing immunization records at every patient visit are routine to doctors for increasing the prescription of recommended vaccines.[53,54] The strategy used in the UK, which emphasizes the prompt identification of eligible population, can be adopted in other parts of the world.[34] Compared with the Western world, there are more financial hurdles to be addressed in middle-income countries and this gets reflected in the low uptake.[32] However, there is room for a recommendation from the treating doctor, motivation, and patient education, which are recognized methods to increase vaccination uptake.[25]

CONCLUSION

The uptake of pneumococcal and influenza vaccines is extremely low (0.68% and 0.7%, respectively) among older Indian patients with cancer. A significantly higher proportion (83.3%) of the patients have received at least one dose of the COVID-19 vaccine. There should be a more intense campaign to increase the uptake of routine vaccination in adults.

Author contributions

Conception and/or design of the work: VN, AR, RB, KP; data collection: ARR, AK, SG, AP, RD, RC, SK, AS, TMS; Data analysis and interpretation: PR, TMS, ARR; drafting the article: TMS, VN, AR, RB, KP; critical revision of the article, and final approval of the version to be published: all authors; accountability for all aspects of the work: all authors.

Data sharing statement

Individual de-identified participant data that are related to the results of this study will be made available on reasonable request by Dr. Tabitha Merium Sabu ([email protected]), starting from the date of publication, until 10 years after publication. Requests beyond this time frame will be considered on a case-by-case basis.

Financial support and sponsorship

Nil.

Conflicts of interest

Vanita Noronha, Rajendra Badwe, and Kumar Prabhash are members of the editorial board of Cancer Research, Statistics and Treatment. As such, they may have had access to information and/or participated in decisions that could be perceived as influencing the publication of this manuscript. However, they had recused themselves from the peer review, editorial, and decision-making process for this manuscript, to ensure that the content is objective and unbiased.

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Keywords:

Geriatric; morbidity; mortality; vaccination

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