A cross-sectional study on the seroprevalence of the SARS-CoV-2 IgG antibody in patients with cancer from central Kerala : Cancer Research, Statistics, and Treatment

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Original Article

A cross-sectional study on the seroprevalence of the SARS-CoV-2 IgG antibody in patients with cancer from central Kerala

George, Geomcy; Varghese, Sangeetha Merrin1,; Jose, Manju Rosy; Mateethra, George Chandy2; Sachu, Arun3; Saji, Feba Mary

Author Information
Cancer Research, Statistics, and Treatment: Apr–Jun 2022 - Volume 5 - Issue 2 - p 205-211
doi: 10.4103/crst.crst_289_21
  • Open

Abstract

INTRODUCTION

We are over two years into the coronavirus disease 2019 (COVID-19) pandemic since the first case of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection was reported in Kerala on January 27, 2020.[12] As of March 2022, there were 6,531,392 cases with more than 67,822 deaths reported from COVID-19 in Kerala.[3] Generally, mildly affected or asymptomatic individuals are not screened or tested for COVID-19. As a result, the number of confirmed SARS-CoV-2 infections is vastly under-estimated.

People with cancer belong to the most vulnerable group of patients because of immunosuppression by virtue of either their disease or treatment.[45] They may be prone to severe complications if infected with SARS-CoV-2. An early report from China suggested that patients with cancer who contracted COVID-19 had a three times higher mortality rate when compared to the general population.[6] Contrarily, a study from the United Kingdom reported only mild symptoms in 52% of the patients with cancer and COVID-19. Mortality may depend more on the sex, age, and comorbidities than on the tumor type or anti-cancer treatment.[7]

According to the Centers for Disease Control and Prevention, the current gold standard for confirming SARS-CoV-2 infection is detection of the SARS-CoV-2 RNA using reverse transcriptase- polymerase chain reaction (RT-PCR). However, false-negative test results are not uncommon, especially during the early phase, and late in the course of an infection.[89] Serological tests detecting immunoglobulin G (IgG) antibodies against SARS-CoV-2 are easy to perform and reduce the heterogeneity in results compared to nasopharyngeal specimens sent for RT-PCR.[7] More importantly, evidence of a previous asymptomatic infection can also be captured by a serological test, and thereby, the immune status of different cohorts of patients can be accurately assessed.[10]

The SARS-CoV-2 seropositivity in patients with cancer has not been investigated thus far in Kerala. The antibody response to SARS-CoV-2 in patients receiving cancer-directed therapies may be less pronounced,[11] and concerns about seroconversion in this patient population are often raised. Mounting humoral immunity is crucial not only in mediating recovery from the infection but also to establish and maintain herd immunity through effective vaccination strategies.[12] As vaccination against SARS-CoV-2 is in full swing, monitoring the presence and levels of SARS-CoV-2 IgG is warranted. If the prevalence of the SARS-CoV-2 IgG antibody is low, there is a continued need for strict safety measures[13] and screening for COVID-19 at cancer centers to prevent uncontrolled viral spread among patients with cancer and their treating physicians. Therefore, we aimed to evaluate the SARS-CoV-2 seroprevalence rate in patients with solid malignancies and to assess the factors associated with IgG seropositivity.

MATERIALS AND METHODS

General study details

This cross-sectional study was conducted between December 2020 and June 2021 in the Outpatient Department of the Oncology Unit of Believers Church Medical College, Thiruvalla, a tertiary care center in Central Kerala, India, after obtaining clearance from the Institutional Ethics Committee (IEC/2020/09/186, approved on Nov 20, 2020; Supplementary Appendix 1). Written informed consent was obtained from all participants prior to enrollment in the study. The study was funded by the institution and conducted according to the ethical guidelines established by the Declaration of Helsinki and other guidelines such as Good Clinical Practice Guidelines and those established by the Indian Council of Medical Research (ICMR). The study was not registered with a publicly accessible clinical trials registry such as Clinical Trials Registry-India as it was not an interventional trial.

Participants

We included patients over 18 years old who had been diagnosed with cancer and had attended the Oncology Outpatient Department. We excluded patients who had been vaccinated against COVID-19, those with hematological malignancies, and those with co-existing auto-immune diseases. All other patients (treatment naïve or on treatment) were included in the study [Figure 1].

F1-4
Figure 1:
Patient Flow Diagram

Aims/objectives

Our primary objective was to evaluate the seroprevalence of SARS-CoV-2 in patients with cancer. Our secondary objectives were to assess the factors associated with IgG seropositivity and to explore the patients' attitudes and fears regarding COVID-19.

Study methodology

Two trained clinical pharmacists interviewed the study participants with the help of an interview schedule and asked each patient questions from a pre-decided questionnaire (Supplementary Appendix 2). The antibody test was performed using the VITROS® Anti-SARS-CoV-2 IgG test (Ortho-Clinical Diagnostics, Rochester, NY, USA), a highly accurate test for the detection of serum IgG antibodies to the immune-dominant S1 spike protein of the SARS-CoV-2 virus, having a sensitivity of >90% and a specificity of 100%.[14] The VITROS Anti-SARS-CoV-2 IgG test is approved under the Food and Drug Administration's Emergency Use Authorization. We also recorded basic demographic details and information regarding any symptoms of COVID-19 infection experienced by the patients upto three months prior to the survey (using a checklist of symptoms such as fever, cough, loose stools, and sore throat), site of malignancy, treatment history, and the patients' general experience of the COVID-19 pandemic.

Seroconversion

A signal-to-cutoff ratio (S/Co) ≥1 was taken to indicate a positive result, that is, seroconversion. A value <1 meant that the test was negative for seroconversion.[14]

Statistics

A convenience sample size of 100 was decided to check for seroconversion in order to assume normality as previous studies of seroconversion were lacking in the Indian population. Statistical analysis was performed on the Statistical Package for the Social Sciences (IBM Corp. Released 2012. IBM SPSS Statistics for Windows, Version 21.0. Armonk, NY: IBM Corp.). Categorical variables were expressed as percentages. The association between demographic variables and the presence of IgG antibodies was tested by the Chi-square test. A P value < 0.05 was considered statistically significant.

RESULTS

We enrolled 100 patients in the study. The median age of the cohort was 62 years (inter-quartile range, 53 to 69.8). The most common malignancies included gastrointestinal tumors in 31 (31%) patients. There were 41 (41%) patients receiving chemotherapy, 25 (25%) who had undergone surgery followed by chemotherapy, 12 (12%) who were receiving trimodality therapy (surgery, chemotherapy, and radiation), 3 (3%) receiving radiation alone, and 4 (4%) who were on immunotherapy. [Table 1]. There were 2 (2%) patients who were receiving palliative care. The rest of the patients had completed their treatment.

T1-4
Table 1:
Clinicodemographic profile of patients from Kerala with cancer included in the study on the seropravalance of the SARS-CoV-2 antibody

COVID-19-related symptoms in the preceding three months prior to the survey had been experienced by 19% (19/100) of the patients. Most patients had experienced myalgia and sore throat [Table 2].

T2-4
Table 2:
COVID-19-related variables in patients with cancer

The seroprevalence of COVID-19 IgG antibodies was 11% (95% CI, 4.8–17.1) [Figure 2]. Younger age was the only factor that was significantly associated with the presence of COVID-19 antibodies (P = 0.007). Sex, smoking, and the use of alcohol did not have any association with seroprevalence [Table 3].

F2-4
Figure 2:
Seroprevalence of COVID-19 IgG antibodies
T3-4
Table 3:
Factors associated with seroprevalence of the COVID-19 IgG antibody in patients with cancer

DISCUSSION

According to the ICMR's fourth national serological survey (May 2021), Kerala had the lowest SARS-CoV-2 seroprevalence in India.[15] This suggests that the state of Kerala had managed the COVID-19 pandemic very well in the first and second waves, protecting a significant fraction of the population from infection. However, this also implies that there may be a risk for additional infection waves in the future as many people remain vulnerable to COVID-19 infection. In our study, we found that the SARS-CoV-2 seroprevalence in Kerala in unvaccinated patients with cancer was only 11%. Although 19% of the patients reported experiencing symptoms potentially attributable to COVID-19, only a minority (11%) had specific SARS-CoV-2 antibodies, and an even smaller percentage (1%) had documented COVID-19 infection by RT-PCR testing. At the same time, the general population in Kerala had a seroprevalence of 42% as per the ICMR serological survey report.[16]

The seroconversion rate has been reported to range widely after the first dose of the COVID-19 vaccine, that is, from 11% to 87.5% in patients with cancer.[17] Most of the data for our study were collected during the first three months of the study, which overlapped with the period when COVID-19 vaccines had just become available in India, and there was an upsurge in vaccine hesitancy; there was also the issue of non-availability of vaccines during the initial phase (April–June 2021) of the nationwide roll-out of COVID-19 vaccination,[18] and therefore, none of our patients had received the COVID-19 vaccine during the period of the study. An exploratory analysis of the rate of vaccine hesitancy for COVID-19 vaccines in India appears to be clustered around 60%.[1920]

The low seroprevalence of SARS-CoV-2 antibodies may indicate a lack of exposure to SARS- CoV-2 and hence the absence of immunity against SARS-CoV-2. This could be because of the very stringent Infection Control practices adopted by the patients and the Oncology Department. We found that 77% of the patients with cancer were worried about contracting COVID-19 infection, which would have prompted them to be cautious and raise their guard against COVID-19. A few of them even deferred their anti-cancer treatment for fear of getting the infection from the health care settings. A decrease in the number of patients with cancer who received cancer-directed therapy during the COVID-19 pandemic has been noted in other studies as well.[212223242526] Additionally, patients with cancer and those receiving cancer-directed therapy may not mount an adequate immune response against SARS-CoV-2.[17] It may be reasonable to assume that asymptomatic patients with cancer may not develop detectable antibody responses and may remain seronegative, even after receiving the COVID-19 vaccine.[11] Patients with hematological malignancies have been reported to have a higher frequency of manifesting symptomatic COVID-19 infection but a significantly lower likelihood of seroconversion.[27] The German Robert Koch Institute estimated the seroprevalence of COVID-19 in Germany to be 7.8% in March 2021.[28] An Austrian study in March–June 2020 also reported a seroprevalence of 3.6% among oncological patients.[4] However, contrary to this earlier line of thought, recent studies indicate that the SARS-CoV-2-specific IgG antibody response does not differ between patients with cancer and healthy subjects.[17] The seroconversion rate of a cohort of patients with cancer was 91%, which was nearly identical to that of the general population, which is reassuring that most patients with cancer were able to mount an immune response to SARS-CoV-2. Given this evidence, we assume that the low seroprevalence in our study may have been the result of a low exposure to the virus as patients with cancer and their caregivers probably made greater efforts to protect themselves from COVID-19 as compared to the general public.

A meta-analysis of COVID-19 infection in patients with cancer revealed a higher risk of mortality (Odds Ratio, 3.23), a severe disease rate (Odds Ratio, 3.91), intensive care unit admission (Odds Ratio, 3.10), and mechanical ventilation (Odds Ratio, 4.8); thus, patients with cancer who develop COVID-19 are at a higher risk of complications.[29] In view of the rising number of cases in Kerala as of August 27, 2021[3] and the low seroprevalence of SARS-CoV-2 antibodies in patients with cancer, we advocate that this cohort of vulnerable patients must take adequate infection control precautions at all times. The hospitals must provide full supportive care for immunosuppressed patients to minimize the risk of infection.

We found that the only factor that significantly affected the SARS-CoV-2 seropralence rate was age; younger patients had higher rates of seropositivity as compared to older patients. On the other hand, sex, alcohol use, smoking, and a history of COVID-19 symptoms did not have any association with seroprevalence. We found that 31% of our patients were taking supplements such as vitamin C, vitamin D, and zinc. This could be a part of their treatment where multi-vitamins are prescribed routinely as “immunity boosters” to help fight against COVID-19, although there are no scientific data to back this.

The COVID-19 pandemic had a major impact on the general treatment patterns and cancer care.[30313233] The exploratory part of our study revealed that some patients had suffered income loss affecting their treatment. Travel restrictions made it difficult to seek follow-up care;[34] some feared contracting COVID-19, and therefore, they deferred their cancer treatment. Although some of the guidelines have advocated the implementation of telemedicine consultations,[19] the importance of facilitating routine hospital visits for check-ups and laboratory investigations cannot be undermined.[35]

Although the incidence of asymptomatic cases of COVID-19 (particularly after the advent of vaccination) varies widely, there is a consensus that the disease can be spread by asymptomatic persons as well.[36] Despite a gradual withdrawal of strict measures of containment all over India, our study suggests that there is a continued need for implementing strict safety measures in oncology outpatient departments and wards to prevent the uncontrolled spread of COVID-19 among the patients with cancer.[11] Our study showed a seroprevalence of 11%, which is comparable to what have been resported by other studies performed in the early phases of the pandemic.[17]

The limitations of our study were that our results represent the seroprevalence situtation after the first wave of the COVID-19 pandemic. As this was early in the pandemic and the uptake of COVID-19 vaccination was poor then, the seropositivity rate is likely to be higher if tested now. Additionally, the seropositivity rate that we found cannot be assumed to be the seroprevalence in the general population of patients with cancer as ours is only one among the many cancer care centers across Kerala. The SARS-CoV-2 antibodies may also wane with time, which may complicate the interpretation of seroprevalence data.

CONCLUSION

Low seroprevalence of SARS-CoV-2 IgG antibodies in patients with cancer is a matter of concern. This is a proxy indicator that many patients with cancer are still vulnerable to COVID-19 infection. There is a continuing need for implementing strict safety measures in oncology care centers and to encourage widespread COVID-19 vaccination in order to prevent the uncontrolled spread of COVID-19 among patients with cancer.

Data sharing statement

De-identified data and additional documents (statistical analysis plan) can be shared for a period of I year after publication on e-mail request to the corresponding author: Dr. Sangeetha Jithin, Email Id: [email protected]

Author contributions

Conception or design of the work: GG, SMV, MRJ, GMC, AS; data collection: FMS, SMV, MRJ; data analysis and interpretation: SMV; drafting the article: SMV; critical revision of the article: GG, SMV, GMC, AS, FMS, MRJ; final approval of the version to be published: all authors; accountable for all aspects of the work: all authors

Financial support and sponsorship

Believers Church Medical College funded the study.

Conflicts of interest

There are no conflicts of interest.

STUDY PROTOCOL SERO-PREVALENCE OF SARS- COV-2 IGG ANTIBODY IN CANCER PATIENTS OF A TERTIARY CARE CENTRE IN CENTRAL KERALA

INTRODUCTION

  • We are nine months into the Covid 19 pandemic since the first reported case in Kerala on January 30, 2020.
  • patients with malignancies might be among the most threatened patient populations since most of them are heavily immunosuppressed due to their underlying disease, their treatment or both.(1) Thus, they are highly susceptible to severe complications if infected with SARS-CoV-2 and mortality is 6% in patients with cancer.
  • Serological tests detecting IgG antibodies against SARS-CoV-2 are easy to perform and could also reduce the heterogeneity of RT-PCR, where infections can be missed early or in the late phase of the disease.
  • More importantly, a serological test could capture previous asymptomatic infections and thereby help to assess the immune status of a cohort of patients.
  • The SARS CoV-2 sero-positivity in patients with cancer has not been investigated so far in Kerala. The antibody response rates against SARS-CoV-2 in patients with cancer receiving anticancer therapies may be less pronounced.
  • If the prevalence of SARS CoV-2 IgG antibody is low, there is a continued need for strict safety measures at cancer centers to prevent uncontrolled viral spread among oncological healthcare professionals and patients with cancer.

OBJECTIVES

  • To detect the sero-prevalence of SARS CoV-2 IgG antibodies in cancer patients attending the BCMCH, Oncology department.
  • To explore the factors associated with presence/absence of SARS CoV-2 IgG antibodies

METHODS

  • STUDY DESIGN- The present study is a mixed retrospective/prospective cohort study with the enrolment date used to collect retrospective data and start the prospective sero-prevalence.
  • STUDY SETTING – Oncology Department, Believers Church Medical College
  • STUDY POPULATION- All patients with cancer attending the Oncology OPD and IPD between Nov 20, 2020 and July 2021.
  • SAMPLING PROCEDURE- All patients attending the Oncology Dept in the abovementioned time period after satisfying the inclusion and exclusion criteria.

INCLUSION CRITERIA:

  • Patient must have a prior or current diagnosis of cancer (solid tumor or hematological malignancy)
  • Age>/= 18 years

EXCLUSION CRITERIA

  • Patient not willing to provide informed consent.
  • Patient with co-existing Auto-immune disease
  • Patient who takes Covid vaccine as and when it comes.
  • HIV positive
  • Prior renal transplant
  • Patients on immune- suppressive drugs for conditions other than cancer

DATA COLLECTION- Patients participating in the study will be asked to sign an informed consent and fill in a structured questionnaire. Data regarding basic demographic parameters (age, gender and profession), travel history in the last 4 weeks, place of residence, known contact with a COVID-19-positive person, the environment of contact with a COVID-19-positive person, positive SARS-CoV-2 test in the past, the necessity of inpatient treatment, experienced symptoms, the necessity of quarantine and about their general experience of COVID-19 pandemic. Other details regarding the symptoms of Covid 19, type of cancer and the mode of treatment- Immunotherapy, chemotherapy, Targeted therapy or their combinations will be filled by the junior resident doctor posted in the department.

SARS-CoV-2 testing: 3 mL of peripheral venous blood will be collected from each participant.

IgG Antibodies against SARS-CoV-2 will be detected using the VITROS Anti-SARS-CoV-2 IgG test- which is an Immunometric test. The VITROS Anti-SARS-CoV-2 IgG test is recommended for use under the Food and Drug Administration's Emergency Use Authorization. This test will also give a IgG titre.- High/Low.

PLAN OF ANALYSIS- Statistical analysis will be performed using the SPSS v. 20 software package. Continuous variables will be presented as median and range. Categorical variables will be summarized using percentages and counts. Association between demographic variables and the presence of IgG antibodies will be tested by Chi-square test of association.

ETHICAL IMPLICATIONS- The study will be conducted after obtaining clearance by the IRB, BCMCH. Patients will be admitted to the study based on their written informed consent.

INTERVIEW SCHEDULE INTERVIEW SCHEDULE

  1. Patient No.-
  2. Age-
  3. Gender-
  4. Occupation -
  5. The primary site of cancer -
  6. Duration of cancer –
  7. Presence of metastasis- Yes/No
  8. Stage of cancer- …………….
  9. Taking treatment- yes/No
  10. Type of treatment-
    1. Radiation, Chemo, Chemo + Radio, Immunotherapy
  11. No. of chemotherapies taken- Time since last chemotherapy
  12. Have you taken radiotherapy- Yes/No
    1. If yes, time since last radiation-
  13. Any surgeries in the past- Yes/No
    1. If yes, time since last surgery-
  14. On palliative care- yes/No
  15. Any co-morbidities – HTN, DM, COPD, Others- mention………………….
  16. Alcoholic- present/past/NO
  17. Smoker- present/past/NO
  18. Have you had symptoms of Covid 19 in the past 3 months-
    1. Fever, Sore-throat, Loose stools, Myalgia, Anosmia, Loss of taste
  19. Have you been tested for Covid 19 in the past 3 months- Yes/No. (Test used-……)
    1. If yes- Positive/Negative
  20. Were you treated as an in-patient for Covid 19?
  21. Were you quarantined for Covid 19?
  22. Do you have a travel history in the last 3 months- Yes/No.
    1. If yes, where?
  23. Have you contacted any known case of Covid in the last 3 months- Yes/No.
    1. If so- environment of contact- home/others- specify
  24. Do you take any other food supplements- vit C, Zinc, Vit-D to boost your immunity? Yes/No
  25. What do you think about the need of quarantining people exposed to Covid 19?
  26. What was your experience in relation to your disease after the advent of Covid 19?

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Keywords:

Cancer; coronavirus; COVID-19; IgG; India; Kerala; seroprevalence

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