From a cluster of patients with viral pneumonia at a wet market of Wuhan, China, emerged one of the biggest pandemics of our era, the coronavirus disease 2019 (COVID-19) virus. From its origin in December 2019, this virus has rapidly encircled the globe, infecting over 110 million people and claiming up to 2.5 million lives worldwide to date. The most affected countries include the USA, Brazil, and India. India accounts for 2.5 crore total cases and 2.7 lakh deaths due to COVID-19. ¹

WHO reported that over 14% of the total COVID-19 cases account for HCWs and has reached even 35% in some countries.

In India, more than 15,000 HCWs have been affected and over 800 health care workers have succumbed to COVID-19 according to the Indian Medical Association (IMA) records.

India’s health infrastructure has only 76 doctors for every 1 lakh population, which adds to the health care burden in the face of this pandemic. ²

While health care systems and equipment can be boosted in a pandemic, the same cannot be done for health care personnel, which makes them a precious resource. Thus, protecting the health care personnel becomes paramount. However, with the increasing patient burden, the second wave of cases, shortage of staff, limited isolation facilities, and personal protective equipment we found more and more HCWs being ensnared by this disease. This posed a difficult problem for the health care community and society as a whole. The only protection that the HCWs have is infection control measures to prevent them from contracting this virus. A rapid review also confirmed that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), like other coronavirus infections, is a burden on the HCW, and the use of personal protective equipment (PPE) and infection control training is associated with decreased risk. ³

We conducted a case-control retrospective study, to assess the risk factors that HCWs were exposed to in a tertiary care hospital treating COVID-19 patients. We attempted to assess why some HCWs contracted COVID-19 while others did not. We intended to investigate specific risk factors for COVID-19 transmission among HCWs in a tertiary care university hospital. We also decided to stratify risk factors among Heath care workers based on their exposure, precautions taken, breach in infection control precautions, and prophylaxis used.

We found that despite using the conventional infection control precautions as per the Ministry of Health and Family Welfare (MoHFW), there were some interesting findings in the study that helped us review and contextualize the infection control policies based on available resources. These factors could also aid in shielding the HCWs from the next wave of the pandemic by refining and strengthening the infection control policies in individual health care facilities.

For this case-control study, a total of 116 HCWs working in Kasturba Hospital, Manipal (South India) were recruited from all clinical departments involved in the care of COVID-19 patients between July 2020 to September 2020 (3 months). Among these 50% were cases and 50% were controls in 1:1 ratio. Both cases and controls were between the age of 20 to 60 years.

Cases were defined as symptomatic HCWs working in our hospital who tested positive for COVID-19 by real time reverse transcription polymerase chain reaction (RT-PCR) using the TRU PCR kit by KILPEST’s [Blackbio]. Controls were defined as HCWs who did not develop symptoms and did not test positive for COVID-19.

All 116 patients (57 cases and 59 controls) filled up a detailed questionnaire (after consenting) regarding demographics, details of their work profile, exposure details, details of precautions used, breach of infection control precautions, and Hydroxychloroquine (HCQs) prophylaxis. ^{5 , 6} Cases were asked for details of their COVID illness as well.

The details of work profile included the areas that the participants were exposed to in the hospital as frontline HCWs, the duration of exposure as number of days per week and number of hours per day and exposure to high-risk COVID areas such as the COVID intensive care units (ICU). The exposure details included details of COVID-19 exposure during collection of throat swab, intubation, handling and transport of respiratory secretions and exposure to high-risk activities such as surgical procedures on COVID-19 patients. Details of personal protective equipment used by HCWs such as face mask, gloves, face shield, hospital gown, scrubs, shoe covers and practise of hand hygiene were collected. Breach of these precautions in terms of omission of use or improper/intermittent use were also included. During data collection, the participants were asked to provide accurate information and assured of their anonymity. Hence potential bias such as improper reporting of breach in infection control precautions were also minimized.

The collected data was analysed using the SPSS for Windows version 22.0, RRID: SCR_002865 (SPSS, Inc., Chicago, IL). The variables were summarized using frequency and percentage. A Chi-square test was used to determine the association between the risk factors for COVID-19 transmission among healthcare workers (HCWs) and the dependant variable (case/control). The variables which were found to be significantly associated were subjected to multivariable logistic regression. Adjusted odds ratio with 95% confidence interval is reported. p-value <0.05 represents statistical significance.

The recruited HCWs (n = 116) were equally distributed into cases and controls in a 1:1 ratio. All the 116 participants who were approached for the study were found to be eligible and consented to participate in the study. All the participants completed the entire questionnaire required for the study. Table 1 shows the baseline characteristic of all the recruits.

The maximum representation was between the age of 20–30 years (74%) followed by recruits between 31–40 years (26%). There were 64 males and 52 females among the study population. The HCWsincluded in the study were medical interns (46%), post-graduates (22%), medical staff (21%), and nurses (11%) who were involved in treating patients with COVID-19. Only 10% of the recruits had associated co-morbidities.

The areas of work among both cases and controls were the emergency area (28%), COVID intensive care (51%), and COVID ward (21%). The duration of exposure was mostly more than 6 hours (66%) followed by 3-6 hours (39%). A majority of the recruits also reported working for 7 days of the week (49% cases and 59% controls) while 40% of all recruits clocked 3-6 days a week.

Exposure to patients in the COVID intensive care was equal (50%) among both cases and controls. Table 2 indicates the comparison between cases and controls based on their exposure to COVID-19 infection at work.

Involvement in taking a throat swab for the COVID test also was almost similar among the cases and the controls. Though they had a similar exposure of work in an intensive care setting, only around 10% of cases and controls were involved in intubating a COVID suspect or a COVID positive patient. None of the recruits were involved in endotracheal sample collection for a COVID suspect/COVID positive patient. Only 12% of cases and controls were involved in the collection/transportation of blood/urine for a COVID suspect or COVID positive patient.

Surgical procedures including tracheostomy, emergency orthopedic and general surgery procedures, cesarean sections on a COVID suspect/positive patient saw a significant 28% cases in attendance compared to only 13% among controls (p=0.05). Table 3 compares the cases and controls based on the infection control precautions used. It was noted that an equal number of cases and controls wore a mask at all times during patient contact.

However, only 15% of the cases and controls were non-compliant with the use of gloves during patient contact. In addition to masks and gloves, HCWswere provided with face shields during patient contact. However, only 56% of the cases wore the face shield compared to 71% among the controls (p=0.09). Also, hospital gowns were provided toHCWs. Interestingly, only 47% of cases used this provision compared to 71% of the control population (p=0.009). Similarly, only 49% of cases wore scrubs compared to 67% controls (p=0.04). The use of shoe covers was similar among cases and controls with only half of the recruits regularly making use of them. All recruits performed hand hygiene following doffing after patient contact. There was no significant difference in the breach of infection control precautions among cases and controls. Table 4 compares the breach in infection control precautions and prophylaxis used between cases and controls.

A majority of the recruits did not report improper use of PPE or making mistakes while implementing infection control precautions. Though some of the recruits (38% cases and 34% controls) stayed in the same duty room with another HCW without masks, this data was similar among both cases and controls. Consumption of food within a meter of another health care worker also did not show a significant difference among cases (64%) and controls (50%). Half of the cases and controls reported failure to maintain safe social distance from another healthcare worker.

Hydroxychloroquine prophylaxis was taken by 17% cases and 25% controls. However, only 5 cases and 7 controls took the HCQ prophylaxis for the entire 8 weeks.

Among the cases, most of the recruits tested positive in July 2020 and had mild severity of COVID illness. Ten cases reported the spread of the COVID illness to their primary contacts.

The COVID pandemic that broke out from the confines of China reached our district in South India by February 2020. However, the first HCW contracted COVID only in July 2020 with medical intern testing positive for COVID by RT-PCR. This five-month delay could be attributed to the stringent infection control precautions in place at our hospital. However, when the first case was detected among a HCW despite all the precautions, the initial question was whether it was a hospital-acquired or a community-acquired infection. Over the subsequent weeks, several other HCW contracted COVID thereby confirming the possibility of a hospital-acquired spread. This led us to revisit the infection control policies and re-evaluate the risk factors that the HCW are exposed to while treating COVID patients.

The volunteers in the study had a male: female ratio of 1.2:1 with 64 men and 52 women participants. This correlated with the findings in other Indian studies as well. ⁴ The age distribution among the cases and controls showed a predominant population between the age of 20–30 years (74%) followed by 30–40 years (23%). The age distribution did not follow a Gaussian pattern. This could be due to the hospital policy to protect older individuals with co-morbidities from COVID exposure by not allowing them on the front line. The age distribution is reflected in the type of health care worker included in the study as well. A majority of the recruits were interns and post-graduates followed by staff doctors and nurses. As the study population leaned towards the younger age group, 90% of them did not have associated co-morbidities. Table 1 shows the demographic profile of the cases and controls in the study.

In a large Indian study done on 18,000 HCW, it was noted that the median age was in the range of 18–40 years. ⁴ A case-control study done on HCW in North India, using a data portal to obtain exposure details among HCW fighting COVID-19, showed a mean age of 34 years with cases being slightly older than controls. ⁵ This younger age group resonates with the similar finding in our study and the trend of the younger HCWs manning the front lines was likely a strategy to deter increased morbidity and mortality among HCWs.

Evaluation of the details of their work profile showed a significant association between duration of exposure and contracting the COVID illness. The HCW who had >6 hours of work in the COVID area seemed more likely to contract the disease as shown among the 67% cases vs the 46% controls (p=0.02). However, the number of days at work did not seem to have a significant bearing on contracting the COVID disease.

In a study done in Turkey on over 50 HCWs involved in COVID care, it was found that the positivity rates among the HCWs who worked in frontline positions were higher (RR=2.449, CI=1.06, p=0.027) than those who were not in frontline positions. ⁶ At this point, it is important to note that it is difficult to ascertain whether COVID infection in a HCW is hospital-acquired or community-acquired. However, owing to the cluster of cases following the index case among HCWs in our facility, the infection is more likely to be hospital-acquired rather than acquired from the community. A modeling study by Temime et al. found that R0 for Covid-19 (i.e. ability to transmit the infection to other people) was higher for HCWs compared to the general public as they have prolonged contact with infected individuals. ⁷ This further corroborates the assumption that the COVID-19 illness in the HCWscould be hospital-acquired rather than community-acquired.

The study showed similar exposure of both cases and controls to the COVID intensive care facility. Though only a few of the cases and controls were involved in high-risk procedures like the collection of throat swabs or intubation of a COVID suspect/positive patient, it did not predispose them to develop the disease. This could be because all precautions are taken stringently for high-risk procedures such as these and the risk of breach of infection control precautions is low. Though there is conflicting literature regarding the risk of transmission during high-risk procedures like intubation, most of the evidence suggested no or low rates of transmission during these procedures. A study by Van Doremalen also implicated aerosols generated during high-risk procedures as an important factor in the mode of virus transmission among HCWs. ⁸ An international registry study (INTUBATE COVID), included over 1700 clinicians who performed intubation on COVID patients, and only a mere 3% developed COVID. ⁶ Another study from Wuhan, China on 420 HCWs who were involved in intubation reported no transmission at all. ⁹

Incidentally, exposure in the operating room to a COVID suspect/positive patient during surgical procedures indicated a significant risk for cases (28%) compared to controls (13%). SARS-CoV-2 shows high infectivity in the hospital setting as it has been isolated from sputum, nasopharynx, oropharynx, stool, blood, & conjunctiva. ^{10 – 12} This could be attributed to prolonged duration of exposure in closed spaces of an operation theatre, aerosol generation during intubation/airway suctioning during the administration of anesthesia, or even surgical smoke produced during laparoscopy. ¹³

Usage of face shields was found to offer significant protection against COVID to HCWs. It was noted that only 56% of cases used face shields compared to 71% controls (p=0.09). WHO has included face shields as a part of standard PPE for COVID, to protect against aerosol generation. ¹⁴ However, some HCWs prefer using eye goggles over face shields. This has shown an increased risk of COVID transmission in our study. It is possible that using a face shield decreases accidental touching of the face compared to eye goggles.

Our study also noted a significant association between the use of gowns and protection against COVID. Gowns or coveralls are provided as a part of the standard PPE in keeping with the WHO guidelines. ¹⁴ However, our study noted less transmission risk among HCWs who used gowns compared to coveralls. Almost 71% of controls used gowns compared to 47% of cases who used coveralls instead. No study has compared the effectiveness of gowns and coveralls in reducing the transmission of the virus to HCWs. The only difference between the gown and the coverall is their design. Coveralls are designed to cover the entire body including the back and the legs. They also allow ease of movement. However, the zipper of the coverall may pose a risk if it is not covered by a flap as it can compromise barrier protection. They also generate more heat stress compared to gowns making it uncomfortable for HCWs to spend long hours in the PPE (especially during hot and humid months in South India). Also, coveralls are harder to don/doff and most HCWs are not familiar with its usage as gowns were more commonly used during the pre-COVID times. Gowns, on the other hand, offer complete protection to the front of the body which is more exposed to infection during patient care. Though it allows limited movement, it is comfortable during long duty hours and is also easy to doff carefully. ¹⁵

It was also noted that the use of scrubs decreased the risk of transmission of COVID. Scrubs were used in only 49% of cases compared to 67% of the controls (p=0.04). Scrubs are beneficial compared to regular clothes as they allow for adequate microbial decontamination. Domestic laundering of regular clothes worn to the hospital is of concern due to lack of control and monitoring of decontamination thereby providing a route for pathogens to enter the clinical environment. This minor but significant association is of importance during this pandemic to prevent transmission via clothes as fomites. ¹⁶

The Turkish study on HCWs reported an increased risk of transmission due to a breach of infection control precautions such as staying in a duty room without a mask with another HCW or eating meals together. ⁶ However, our study did not show an increased risk of transmission due to these breaches in protocol. It should be noted that our study did not evaluate other possible avenues of infection among HCWs like commuting in a vehicle together or social interaction, etc.

The use of HCQs as prophylaxis was also evaluated in our study but it did not show any significant difference in the outcome. This could be because most of the recruits who took the HCQ prophylaxis were not compliant with it and less than 10% completed the entire course for 8 weeks. This is in conjunction with the results of a Cochrane database review ¹⁷ done on randomized control trials which showed no efficacy of HCQ in the prevention of COVID-19 infection. In another Indian study, it was noted that HCQ prophylaxis played no role in the prevention of COVID-19. ⁴ Multiple systematic reviews also concluded that there is no pertinent data to support the use of HCQ outside that of research. ^{18 , 19} Also, there is lack of clinical data to support its efficacy and adverse effects like prolongation of QTc. Further, the use of HCQ seems to be counter-productive as it tends to instil a false sense of protection.

A major limitation in our study was that it was a voluntary questionnaire-based study. Though the study was performed on health workers who included doctors, interns, nurses, and residents, there was a poor representation among the nurses as reflected in the limited number of nurses who participated in the study. This resulted in a skewed representation of theHCWs. Also, details of vaccination could not be collected from all the participants as many of them regarded sharing this detail as an invasion of their privacy. This detail could have helped us better understand the interplay between the risk factors that HCWsare exposed to and the benefit offered by vaccination.

We found that, in the face of this unprecedented pandemic, prevention is the goal to avert a health care crisis. In this regard, the frontline workers must be protected and equipped in every way to fight the battle ahead. With the recent increase in COVID cases, it becomes important to consolidate our resources and refine our infection control policies to shield us from the impending wave of pandemics. Small steps like shorter shifts and rotating HCWsthrough various areas of exposure with lesser risk may reduce the risk of contracting the infection. The provision of scrubs, which undergo industrial cleaning should be advocated for all HCWs. Use of gowns and face shields over the coveralls and eye goggles as a part of the PPE may also contribute to the mitigation of COVID-19 infection amongHCWs. Such changes as these will go a long way in strengthening our defenses at the frontline.

An informed written consent was obtained from all participants.

CAS and SV conceptualized the study. NB was involved in drafting the protocol and ethical clearance. AV and RN were involved with the initial planning data collection and data analysis. NB also contributed to the data processing and analysis. CAS, SV and NB were involved in preparing the draft and editing the final manuscript.