Keywords
COVID-19. Health-care workers, Infection Prevention and Control, seroconversion, transmission
This article is included in the Emerging Diseases and Outbreaks gateway.
COVID-19. Health-care workers, Infection Prevention and Control, seroconversion, transmission
Healthcare workers are at the heart of a global crisis such as the COVID-19 pandemic. So far thousands of healthcare workers; including doctors and other healthcare workers have succumbed to COVID-19 in India. The virus traces back to 31st December 2019; when it was first discovered and later renamed as SARS-CoV-2 by the International Committee on Taxonomy of Viruses. At present, the strains prevalent are the alpha, beta, gamma, delta and omicron variants which are of notable importance.1 Coronaviruses transmits from one host to another host, either by an aerosol, fomite or via faecal-oral route.1 Globally, till January 2022, there have been nearly 5,614,909 confirmed deaths and more than 352,165,853 confirmed cases due to the pandemic.2
India is second in line with the highest number of COVID-19 cases in the world with 39,543,328 cases and 489,896 deaths to date; just behind the United States of America and ahead of Brazil.3 The nucleus of the strategic amalgamation of all policies and stratagem, the national capital, stirs a discrete figure.4 The second wave, in April-May of 2021, saw an increase in the number of cases and deaths mostly in a phasedwise manner; weaning and waxing off after a sudden short and high peak.
If there is even the slightest breakdown in personal protection, health care providers providing COVID-19 care are at elevated risk of infection. Patients' clinical treatment and the execution of effective Infection Prevention and Control (IPC) procedures in health care facilities are both responsibilities of health personnel.5 Aside from the increased psychological strain caused by increased patient care and a lack of empathy, their overall well-being is a pressing concern. From line listing through diagnosis, treatment, rehabilitation, home visits, and prevention, the health workforce must be always on the front lines. Financial insecurity, violence, the rage of impacted families, and state mishandling all contribute to the misery.6
Several advisories and directives have been updated by the Emergency Medical Relief Division of the Ministry of Health and Family Welfare, for managing Health care workers who are a valuable and scarce resource. They cannot be spared from being quarantined and treated in isolation. As a result, hospital mechanisms for activating the Hospital Infection Control Committee (HICC), as well as nodal officers assigned to respond to Health Associated Infections (HAIs), must strictly follow the guidelines as updated and made available on the Ministry of Health & Family Welfare (MoHFW) website.7,8
Despite multiple studies in the field, there is considerable ambiguity among healthcare personnel due to a lack of concrete knowledge and its dissemination regarding the risk of transmission, the location of the mutation, vaccination efficacy, and political measures for COVID-19 and its variants.9 Understanding the factors associated with the transmission of infection amongst healthcare workers could provide valuable input for the development of suitable prevention strategies.
Hence the objectives of this study were:
This was a prospective cohort study conducted over seven months, from December 2020 to June 2021. This period covered India’s intense second wave of the COVID-19 pandemic.
The study was conducted among the health care workers of two tertiary health care institutes selected by purposive sampling. The first hospital was a government health facility, Lok Nayak Hospital in Central Delhi, which served as a dedicated COVID-19 tertiary care hospital for severe cases of COVID-19, with over 2000 beds and more than 1400 doctors and nurses providing care to COVID-19 patients. The second, Hakeem Abdul Hameed Centenary (HAHC) Hospital, is a trust hospital located in Southeast Delhi. It is a 200 bedded COVID-19 Care Hospital and has 1050 registered healthcare workers. The study population included all the health personnel who were working in this hospital and had come in contact or been exposed recently to a COVID-19 patient while providing them treatment and care.
Inclusion criteria
All HCW participating in the clinical management of a laboratory-confirmed COVID-19 case or having any of the following exposures with a COVID-19 case
• Close contact (within 1 m) to a patient of COVID-19
• exposed to infected patient's blood or body fluids,
• exposed to infected patient's used materials, devices, or equipment,
• contact with the environmental surface around the infected patient including his/her bed, table, wheelchair, ward corridor etc.
They were enrolled irrespective of their use of Personal Protection Equipment (PPE), any symptoms, or vaccination status.
Exclusion criteria
This study provides information on the extent of COVID-19 infection among health workers and its risk factors. According to a study by Korth et al.10 in Germany, the estimated prevalence of SARS-CoV-2 in high- and low-risk HCWs was estimated to be 5.4% and 1.2%, respectively.9 The data reported by this study was used to calculate the sample size by OpenEpi Calculator Version 3.01. At 95% confidence level, 80% power, assuming a ratio of unexposed and exposed to be 1 (since exposure could not be determined in those using PPE) and expecting infection in the exposed group to be 5.4% and unexposed group to be 1.2%, the sample size was calculated to be 566 using the Fleiss formula. Furthermore, accounting for a 20% loss to follow-up, the effective sample size was 738. Thus, a total of 817 subjects were enrolled in the study.
The duty roster of all healthcare workers deployed in the COVID-19 wards of two tertiary care hospitals was extracted from the administrative office. Thereafter a random sample of HCWs was chosen from this list and assessed for eligibility. Those who fit the inclusion criteria were approached to provide written informed consent. At baseline, a questionnaire was administered by the researcher covering socio-demographic information, IPC training and adherence along with details of the type of exposure with the COVID-19 patient. The health care providers were also observed on their adherence to IPC protocols. With the launch of the vaccination drive in January 2021, details of vaccination were also enquired into. The completed questionnaire was entered in a Microsoft Excel sheet and checked by a supervisor against the hard copy for accuracy of data entry. The participants were provided with a symptom diary to note the development of any symptoms during the 21 days follow-up period. Regular follow up was done telephonically to ensure compliance. The end-line visit was scheduled at 22-31 (preferably 28 days) days from the first visit, for the collection of the symptom diary and end-line form. Serum samples were collected at baseline and at end-line to check for the presence of COVID-19 antibodies. The serum samples were tested for antibodies against COVID-19 using the WANTAI serological testing kit. It is a semi-quantitative kit and a value of above 1 was considered as positive.
2-3 ml of blood was collected by venipuncture from all healthcare workers who were enrolled and provided written informed consent. The first sample was taken at enrollment, which was the baseline sample. If the sample tested negative for anti-SARS COV2 antibodies, a second sample was collected after 21 days. The paired samples testing protocol helped in the detection of asymptomatic carriers and understanding the pattern of seroconversion. Appropriate PPE was worn during sample collection and all the staff were well trained in safe specimen handling practices and spill decontamination protocols.
The sample collected appropriately was labelled and the blood vial was allowed to stand upright for 30 minutes at room temperature followed by centrifugation at 2500 rpm for five minutes. The samples were then sent to the testing laboratory after placing the vials in a carrier box in an upright position. Before accepting, the samples were checked for appropriate labelling, correct test request, sample adequacy, absence of leakage and haemolysis. The received samples were then centrifuged again and their serum separated in fresh labelled microcentrifuge tubes/cryo-vials and stored at -20°C before testing.
Wantai SARS-CoV-2-Ab ELISA kit (Lot no.: NCOA20200902) detects total antibodies against the SARS-CoV-2 virus and is based on the principle of two-step incubation antigen “sandwich” enzyme immunoassay. Briefly, 100 ml of the patient’s serum is added to polystyrene microwell strips pre-coated with recombinant SARS-CoV-2 antigen. Three wells are marked as negative calibrators and two wells as positive calibrators. 50 ml of negative and positive calibrator are added to respective wells and the plate is incubated at 37°C for 30 minutes. Post incubation the wells are washed five times with diluted wash buffer. 100 μl of HRP-Conjugate is then added to each well and the plate is incubated at 37°C for 30 minutes. The wells are washed again five times and 50 μl of Chromogen Solution A and then 50 μl of Chromogen Solution B is added into each well. The plate is then incubated at 37°C for 15 minutes in the dark. Each well receives 50 μl of Stop Solution, which is gently mixed. Absorbance is measured using PR4100 microplate reader, Bio-Rad, USA (dual filter) with reference wavelength at 600~650 nm. The cut-off value (C.O.) was calculated as C. O = Nc + 0.16 (Nc = the mean absorbance value for three negative calibrators). The tested serum samples were stored at -80°C with proper labelling.11
Negative results were reported for specimens with absorbance (A) less than the Cut-off value, which meant that no SARS-CoV-2 antibodies were detected with WANTAI SARS-CoV-2 Ab ELISA (A/C.O. < 1). Specimens with absorbance equal to or greater than the cut-off value were considered positive, which indicated that SARS-CoV-2 antibodies were detected using WANTAI SARS-CoV-2 Ab ELISA A/C.O. ≥ 1). The reports were shared with the principal investigator electronically and all the study participants were provided with a copy of their results and were counselled accordingly.
Seropositivity: For this study, we considered all the enrolled subjects who were positive (A/C.O. >1) for SARS-CoV-2 antibodies, detected with the WANTAI SARS-CoV-2 Ab ELISA kit at baseline. This included all those who were positive due to prior COVID-19 infection or because of vaccination against COVID-19.
Seroconversion: For this study, we considered all the enrolled subjects who were negative (A/C.O. < 1) for SARS-CoV-2 antibodies, detected with the WANTAI SARS-CoV-2 Ab ELISA kit at baseline but subsequently tested positive in the end line serum sample collected between 22-31 (preferably 28 days).
Secondary infection rate: Those HCW who were enrolled after a recent exposure with a COVID-19 patient AND confirmed for new infections of COVID-19, assessed through serological assays on paired samples, divided by susceptible contacts (total enrolled HCW). Due to the limitation of our study, it would be the same as the seroconversion rate.
These healthcare workers included medical staff like doctors, nurses, paramedical staff (which includes physiotherapists, occupational therapists and other allied health professionals, General Duty Assistants, housekeeping staff, security staff) students of medical, nursing and paramedical sciences and other front office staff who were directly involved in patient care.
The forms were verified for consistency and completeness. Collected data was entered and coded appropriately and later cleaned for any possible errors in Microsoft Excel. For analysis, SPSS (version 26) was used. The frequency tests were performed after determining clear values for the outcomes. Categorical data was presented as percentages (%). Descriptive analysis (time, place, and person) provided preliminary insight into the clinical spectrum and course of COVID-19 among health workers. Pearson’s chi-square and bivariate logistic regression were done to evaluate the independent associations of multiple factors. All tests were performed at a 5% level of significance, and hence a p-value of less than 0.05 (p-value < 0.05) was taken as a significant association.
Ethical considerations for doing the study were undertaken and all norms of confidentiality, autonomy, beneficence, and consent were taken care of. The study started after approval by the Research Project Advisory Committee (RPAC) and Institutional Ethics committee (IEC) of both Hamdard Institute of Medical Sciences and Research (HIMSR/IEC/004/2020/Dated: 01/09/2020) and Maulana Azad Medical College (F.1/IEC/MAMC/(79/07/2020/No. 203). Other necessary permissions from the hospital and medical colleges were obtained. Written informed consent in English/Hindi was obtained from each participant before their enrolment in the study.
All personnel involved in the study were trained in infection prevention and control procedures (standard, contact, droplet, and airborne precautions, as described by the World Health Organization (WHO) technical guidelines).8 Procedures included proper hand hygiene and the correct use of medical or respiratory face masks.
Confidentiality was maintained by assigning a study identification number by the investigation team for the labelling of questionnaires and clinical specimens. The linking of this identification number to individuals was performed by the investigation team and will not be disclosed elsewhere. The data has been shared with the funding agency WHO, which also provided support for data analysis. The shared data only included the study identification number without any personally identifiable information.
A total of 1210 HCWs were contacted of whom 817 were recruited in this study as per the inclusion criteria. All the participants were interviewed and blood sampling was done for serology at the baseline visit. Out of the 817, 384 were included at the end line serology assessment. The selection of participants and loss to follow up are highlighted in Figure 1.
The study had a roughly equal distribution of male and female participants, with a majority of them belonging to the 31-60 years age group. We had a good representation of doctors, nurses, and paramedics with the majority of them working in high-risk areas where the risk of transmission of COVID-19 was high such as COVID wards, Intensive Care Unit (ICU), testing areas etc. The COVID vaccination drive in India was launched during the study period in a phased manner, prioritizing the vaccination of HCW and frontline workers. Hence, about 50% of the participants were either partially or fully vaccinated. The participant characteristics have been shown in Table 1.
Table 2 presents a summary of the results relating to IPC training and the attitudes towards IPC practices, as reported by various categories of HCWs. On comparing the training received for IPC, most healthcare workers, in all categories; doctors, nurses and paramedics, received less than 2 hours of IPC training and amongst them, nurses were seen to have the highest proportion. 26.8% of nurses had not received any IPC training in the past. Hand hygiene measures as recommended during their IPC training were practiced by the majority of HCWs of all categories, with paramedics (100) (98.0%) showing best adherence, followed by nurses (90.1%) and doctors (84.5 %). An interesting finding was that among the three categories of HCWs, almost all paramedics reported that they always followed hand hygiene as prescribed. However, doctors (84.5%) and nurses (90.1%) seemed to have fallen short in adhering to the prescribed hand hygiene measures at appropriate moments such as before and after touching a patient, their surroundings, or their body fluids. Maximum HCWs (99.5%; 99.8%; 97.1%) reported that they always wore their PPE appropriately and had a regular availability of PPE in the hospital setting.
At baseline, the serology of all HCWs was assessed, as shown in Figure 2. The presence of COVID-19 antibodies was either due to a previous infection or vaccination. The highest proportion was found amongst nurses followed by doctors and paramedics. After 22-31 days, at the end line serology, a positive seroconversion was observed in 53(14.1%) HCWs who were negative at the time of baseline sampling. Further, we analyzed the relation between seroconversion and vaccination status of the individuals and found them to be significantly associated with each other as shown in Figure 3. A positive seroconversion was noted most (29.8%) among the completely vaccinated group. Among those who were not vaccinated, seroconversion was observed amongst 9.9% of the participants.
In this study, we assessed the association of IPC attitudes amongst HCWs with their baseline serology status as seen in Table 3. For analysis, we classified the use of various IPC attitudes into dichotomous variables as adequate and inadequate. We found that among those that received IPC training, 45.5% (285) were negative and 54.5% (341) showed a positive result. Among those who reported that they wore PPE appropriately 45.9% (363) had a negative result and 54.1% (428) showed positive serology. None of the measures was found to have any significant association with serology, however, using appropriate PPE was shown to have a protective effect on preventing infection as seen by negative baseline serology but was not statistically significant.
We also assessed the association between IPC attitudes and seroconversion (Table 4), we found that those who had received training had a higher odd of seroconversion as compared to those who did not, this was however not statistically significant. It was seen that those who adhered to hand hygiene practices adequately had a lower odd of seroconversion although none of the measures was significant. Our study found that those who followed IPC standards had higher odds of seroconversion, in contrast to those who did not.
Further, as shown in Table 5, on assessing the seroconversion based on the type of exposure a healthcare worker had, we found that seroconversion was maximum among participants who had close contact (within one meter) of a COVID 19 patient (17.5%) or those who had a face-to-face exposure (34.4%). Those with contact with patient materials showed a statistically significant association with fewer patients showing seroconversion. However, HCWs who had contact with the surroundings of an infected patient seemed to show a higher odd of seroconversion even though it wasn’t found to be statistically significant. This could be due to the perception that infection cannot be acquired by contact with the surroundings and hence a laxity in the hand hygiene measures employed. Analyzing the kind of PPE used we found that the use of masks and gloves were protective in preventing infection. While the use of gowns/coveralls/headcover or shoe cover didn’t show any protective effect. The association of the type of contact and the kind of PPE used on seroconversion has been shown in Table 6. None of the measures was found to be statistically significant however the protection conferred by the use of masks, face shields and gloves were better in comparison to that of other PPE measures.
This study was conducted to assess the Infection Prevention and Control measures amongst various categories of healthcare workers during the COVID-19 pandemic. To evaluate its effectiveness in preventing human-to-human transmission among recently exposed healthcare workers, we measured their seroconversion, which has been used as a proxy indicator for secondary infection in this study. We collected information about the exposure to COVID-19 infection and the IPC measures taken by them, along with the serological testing at baseline and after 3-4 weeks. This was further supported by a daily symptom diary. The launch of the vaccination campaign and the disastrous second wave of COVID-19 in New Delhi, coincided with the data collection period of this study. Therefore, the results need to be appreciated keeping in mind that approximately 50% of study participants received at least one dose of the vaccine. Due to vaccination, several individuals were positive at their baseline serology, hence as per the protocol, they had to be excluded (47.1%) at the beginning of the study. Further, we had a drop-out rate of 10.7%. Despite a considerable loss in the number of participants, the socio-demographic characteristics amongst the participants at baseline and end-line were very similar, thus making the groups relatively comparable.
In our study, we found a higher proportion of individuals of 31-60 years, as this age group comprises the working-age group. This distribution was also seen in other similar studies conducted amongst healthcare workers.12,13 Also, most of the HCWs above the age of 60 were asked to provide telehealth services to prevent them from getting infected, hence were not exposed to COVID-19 patients. We had a higher participation from non-physician healthcare workers, a majority being nurses. This could be due to either lack of time amongst physicians to participate in the study or, most of them having had previous COVID-19 infection or being vaccinated and hence excluded at baseline. We found that only 3/4th of the healthcare workers had been trained in Infection Prevention and Control measures. This could be due to new HCWs being recruited/hired to handle the surge in cases and not having had the opportunity to attend training. Tabah et al found a similar pattern with about 83% of their staff having adequate training, but desiring additional training for better compliance.13
An unusual finding was that the attitude towards IPC measures was found to be better amongst non-physicians such as nurses and paramedics as compared to doctors. This was despite doctors having received better training as compared to a quarter of the nursing staff not being trained in IPC measures. In contrast to our findings, a study among Bangladeshi HCWs found no difference in knowledge amongst physician and non-physician HCWs, however, they found, that physicians showed a better attitude towards IPC practices.14 A systematic review however uncovered a similar pattern, wherein the doctors showed poorer compliance as compared to nurses in following hand hygiene measures.15 Further, the attitude towards hand hygiene measures of the paramedical staff was seen to be the best, despite the finding that 1/4th of them did not know what the standard IPC precautions were. The WHO recommends 5 moments of hand hygiene to prevent the spread of hospital-acquired infections. However, in our study, we found that the hand hygiene measures showed a decreasing trend in compliance to the moments, depending on the risk of exposure and based on the nature of contact.16 The attitude towards ensuring hand hygiene was seen to be the highest after touching body fluids and was seen to be the least before touching a patient or after touching their surroundings. Although the adherence to wearing PPE was best amongst the paramedic staff, the availability amongst them seemed to be the lowest. Considering the rationale use of PPE in a scenario of shortage of PPEs during the surge of the pandemic, doctors and nurses were given greater priority over paramedics. Incorporating IPC training in the curricula of medical, nursing and paramedic students and conducting refresher training courses on IPC measures are essential to ensure better compliance, especially in settings such as a medical college where the staff are constantly changing.15,17 Adherence to IPC measures doesn’t happen naturally. Thus a multifaceted approach targeted to improve compliance, achieved through training, followed by observation and feedback is pivotal in improving adherence to IPC practices.15 Apart from training, building and promoting an IPC resilient system requires input from IPC professionals, thus building a career path in facilitating a behaviour change among HCWs at the state and national levels.17,18 Ensuring adequate supplies of PPE, sanitizers and handwashing stations, placed at easily visible and accessible places, could enhance the utilization of these resources.18
The chances of secondary infection were seen to be significantly higher among those with face-to-face exposure (p = 0.039), contact with patient body fluid fluids (p = 0.014), or patient materials (p < 0.001). This was surprising considering that these routes of transmission are less commonly recognized yet showed significant risk of infection. A laxity in ensuring hand hygiene practices and other IPC measures could have led to easy transmissibility. Further, the tendency of people to touch the infected mask or inappropriate doffing measures could be a plausible explanation.19 The more commonly known routes of transmission such as aerosolizing procedures or direct contact close to 1 meter of the patient, did not show any significant infections. Better awareness of these well-established routes of transmission could have warranted adequate IPC practices. Recent researches on identifying the routes of transmission for COVID-19 have disproved the airborne route of transmission and claimed a lower chance of transmission via the contact route.20,21 Thus, this could further explain the lower rates found in our study. Higher transmission from contact with surroundings could also imply poor sanitization of the patient surroundings. Hence, healthcare establishments should emphasize the importance of sanitizing surfaces as they act as fomites for transmission of several hospital-acquired infections.21,22 We cannot dismiss the possibility of contracting an infection from settings outside the workplace, such as the home or during lunch breaks. It is quite common for HCWs to take breaks together where they do not adhere to practices of physical distancing or wearing a mask.12 Thus ensuring reduction in other congregate settings and promoting hand hygiene and disinfection of surfaces in settings outside the workplace is also essential.23
Good PPE practices and an alert mind, have been proven tools to prevent hospital-acquired infections.22 In our study, we had a similar finding, where appropriate use of masks and other elements of personal protection was seen to have a lower odd of secondary infection. Of all the types of PPE used, the use of masks was found to be most effective in decreasing transmission of infection. Similar results have been found in other studies where it was reported that the seropositivity among those wearing any type of mask (10.9%; 95% CI: 10.1%–11.6%) was significantly lower than for those without (17.5%; 95% CI: 16.0%–19.2%).24 Considering, the dearth of availability of PPE, promoting its rational use is crucial. Thus, while masks, gloves and hand hygiene practices are key components in any setting, other types of PPE such as shoe cover, head cover, goggles etc. can be reserved for high-risk areas. The mere availability of resources doesn’t guarantee its utilization, and if utilized then its appropriate utilization. Thus, demonstration of using PPE by trained infection control professionals could impress upon the HCWs the appropriate methods of usage and disposal.
This study was not without limitations. One of the biggest challenges we faced was the launch of the COVID-19 vaccination drive among healthcare workers. Although it was a much-awaited relief, it could have considerably confounded the findings of this study. It was not possible to differentiate between the seropositivity developed due to vaccination or due to secondary infection. The drawback of not using RT-PCR as a diagnostic tool for secondary infection was greatly felt. The use of RAT/RT-PCR could have enabled us in differentiating the true secondary infections from theseropositives which were due to COVID-19 vaccination. Finally, the IPC measures adopted were self-reported, hence the underlying fear of interviewer bias cannot be overlooked, especially amongst the paramedical staff who might have been apprehensive from fear of disciplinary action if the truth were told.
In conclusion, strengthening IPC practices is essential in and to the entire community. Healthcare workers being very much a part of the community need to ensure the appropriate use of personal protection to prevent contracting any disease and transmitting it to the community and vice versa. In view of the new knowledge added, rational and appropriate use of PPE and other disinfection practices need to be communicated to the larger audience. Further research on the transmission of COVID-19 in low- and middle-income settings is required.
The data that support the findings of this study are subject to certain data-sharing restrictions. If any researcher is interested in finding out more about this study or wishes to collaborate with us, kindly send an email stating your intentions to the corresponding author. Due permission will be sought from WHO thereafter, and communicated likewise to the interested researchers.
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Is the work clearly and accurately presented and does it cite the current literature?
Partly
Is the study design appropriate and is the work technically sound?
Partly
Are sufficient details of methods and analysis provided to allow replication by others?
Yes
If applicable, is the statistical analysis and its interpretation appropriate?
Partly
Are all the source data underlying the results available to ensure full reproducibility?
No
Are the conclusions drawn adequately supported by the results?
Partly
Competing Interests: No competing interests were disclosed.
Reviewer Expertise: epidemiology, geriatics
Is the work clearly and accurately presented and does it cite the current literature?
Yes
Is the study design appropriate and is the work technically sound?
Yes
Are sufficient details of methods and analysis provided to allow replication by others?
Yes
If applicable, is the statistical analysis and its interpretation appropriate?
Yes
Are all the source data underlying the results available to ensure full reproducibility?
Yes
Are the conclusions drawn adequately supported by the results?
Yes
References
1. Paul E, Alzaydani Asiri I, Al-Hakami A, Chandramoorthy H, et al.: Healthcare workers’ perspectives on healthcare-associated infections and infection control practices: a video-reflexive ethnography study in the Asir region of Saudi Arabia. Antimicrobial Resistance & Infection Control. 2020; 9 (1). Publisher Full TextCompeting Interests: No competing interests were disclosed.
Reviewer Expertise: Primary health care, medical education, health systems research
Alongside their report, reviewers assign a status to the article:
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Provide sufficient details of any financial or non-financial competing interests to enable users to assess whether your comments might lead a reasonable person to question your impartiality. Consider the following examples, but note that this is not an exhaustive list:
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