The impact of the COVID-19 pandemic on healthcare workers (HCWs) has been immense according to data from China,Reference Tang, Tang and Chen1–Reference Xiang, Jin and Wang3 Europe,Reference Xiang, Li and Yang2 and the United States, where the CDC reported 91,267 COVID-19 cases and 501 deaths as of June 23, 2020.4 In Spain, as of June 25, 2020, ~52,500 cases in HCWs have been reported, accounting for >20% of the total cases in the general population.5
Different factors facilitated the rapid spread of the infection in hospital settings, such as the transient unavailability of personal protective equipment (PPE)Reference Mandrola6 and the initial assumption that the main transmission route of the virus was only by droplets.Reference Lewis7 These facts delayed the generalized used of surgical masks inside hospitals.Reference Liang, Gao and Cheng8 Northeast of Madrid has been one of the most severely affected regions, with a cumulative incidence of 1,300 cases per 100,000 inhabitants in our health area (Alcalá de Henares)9 and a mortality rate of 27% among patients that were attended at our emergency department.Reference Pérez-Tanoira, Pérez-García and Romanyk10
The Ethics Committee of Hospital Universitario Príncipe de Asturias (Madrid) approved the study (protocol number: no. COVID-HUPA).
In this study, we aimed (1) to assess the prevalence of infection among hospital workers, (2) to describe the different groups of infected workers, and (3) to assess the risk factors that were associated with SARS-CoV-2 infection in our setting.
Material and methods
Population and study period
We performed a study from March 5, 2020, to May 30, 2020, among workers from our hospital: 490 beds and almost 3,100 hired workers. To evaluate the impact of SARS-CoV-2 pandemic in our hospital, we recorded the number of daily cases by polymerase chain reaction (PCR), differentiating those belonging to hospital workers. The study was performed in 2 periods. During the first period (March and April), PCR was performed in nasopharyngeal exudate for all hospital workers who presented symptoms of SARS-CoV-2 infection and were attended by the occupational health department. During the second period (May), all remaining workers were studied by serology (IgM and IgG antibodies), including asymptomatic workers and symptomatic workers that were negative by PCR.
All workers with a previously confirmed diagnosis of COVID-19 by PCR were not tested using serology. The serologic test was performed using finger-prick blood, and results were immediately reported by the Occupational Health practitioners. Workers were informed about the results and its interpretation. All workers with positive IgM antibodies were additionally studied using PCR. A case of SARS-CoV-2 infection was defined for those workers who presented a positive PCR or serologic test.
Clinical and occupational data
Demographic and clinical data, professional category, and epidemiological data were extracted from the database of the Occupational Health Service. Demographic and clinical characteristics included age, gender, comorbidities (ie, smoker, hypertension, diabetes, cardiovascular disease, chronic obstructive pulmonary disease–COPD, pregnancy and immunosuppression) and clinical features for symptomatic workers (ie, symptoms and disease severity). Hospital workers were categorized as HCWs (including medical staff, nursing, technical specialist, auxiliary nursing care technician and hospital porters) and nHCWs (including kitchen personnel and administrative staff).
Epidemiological data included reported use of PPE, the participation in aerosol generating procedures (AGP) and previous risk contacts with COVID-19 patients, coworkers, or relatives, and type of contact (close or casual contact, according to standardized protocols).11 Briefly, a close contact was defined for any individual who had contact with a case from 48 hours before the onset of symptoms until case isolation (ie, providing care to the case without adequate protection measures or being in the same place that a confirmed case, such as cohabiting or visits, at a distance of <2 m for >15 minutes). On the other hand, casual contact was defined for those individuals that had been in the same closed space with a symptomatic case, without meeting criteria for close contact.11
Diagnostic methods
Molecular techniques
Diagnosis of SARS-CoV-2 infection by PCR was based on the detection of the E, N, ORF1ab, or RdRP genes. RNA amplification was made using 2 real-time PCR platforms: VIASURE SARS-CoV-2 Real-Time PCR Detection Kit (Certest Biotech, Zaragoza, Spain) and Allplex 2019-nCoV assay (Seegene, Seoul, South Korea). All equipment was used according to the manufacturer’s instructions for both the handling and the interpretation of the results.
Serology
For the seroprevalence study, we used the AllTest COVID-19 IgG/IgM kit (AllTest Biotech, Hangzhou, China). This test consists of a qualitative membrane-based immunoassay (immunochromatography or lateral flow immunoassay, LFA) for the detection of IgG and IgM antibodies against SARS-CoV-2 in whole blood, serum, or plasma samples. This LFA was previously validated in our hospital showing a specificity of 100% and a sensitivity of 88% from 14 days after the onset of symptoms.Reference Pérez-García, Pérez-Tanoira and Romanyk12 We used 20 µL of finger-prick whole blood obtained for these tests.
Statistical analysis
Continuous variables were expressed as median and interquartile range (IQR) and categorical variables as proportions. For the interpretation of serology, we considered a positive result for samples in which IgG, IgM, or both were detected. Comparisons between groups were made using the Mann-Whitney U test for continuous variables and the 2-tailed Fisher exact test for categorical variables. Comparisons for demographical and clinical date were calculated using the Kruskal-Wallis test for continuous variables and the 2-tailed Fisher exact test for categorical variables using the noninfected individual’s category as a reference. P values were corrected for multiple comparisons using the Bonferroni procedure. For these comparisons, P ≤ .05 was considered significant.
Logistic regression analysis was performed to establish which variables were associated with SARS-CoV-2 infection, for the following variables: type of hospital worker (HCW vs nHCW), professional category (using medical staff as a reference), type of contact (close vs casual), use of PPE, performance of AGP, contact with COVID-19 patients, contact with hospital coworkers, and contact with relatives. A multivariate logistic regression test was adjusted by the most significant covariates, which were selected using a stepwise method (forward). Results for regression analysis were expressed as odds ratios (ORs), and 95% confidence intervals (95% CIs) were calculated for each risk factor using the Wald approximation method. Statistical analyses were performed using Stata/IC version 13.1 software (StataCorp, College Station, TX).
Results
Impact of SARS-CoV-2 pandemic and results of the diagnostic techniques
Figure 1 shows the impact of the pandemic from March 5, 2020, to May 5, 2020, in our hospital. During this period, the clinical microbiology department performed >6,000 PCR assays, and 2,397 cases of SARS-CoV-2 infection were diagnosed using this method. During the first 2 weeks, 1,883 new cases of SARS-CoV-2 infection were detected, and 477 (25.3%) of these were hospital workers. Management of COVID-19 patients was conducted following protocols established by our government (Supplementary Table 1 online).
Fig. 1. Impact of SARS-CoV-2 pandemic in our hospital. This figure shows only the cases of SARS-CoV-2 infection diagnosed by polymerase chain reaction (PCR). Each case represents a new diagnosis as duplicates in the PCR tests were eliminated for this analysis.
The main results of the study are summarized in Figure 2. Briefly, our hospital had 3,066 workers at the beginning of the study. However, 103 workers could not be enrolled, so they were excluded from the analysis, for a final study population of 2,963 workers. Moreover, 1,092 (36.8%) workers presented symptoms compatible with COVID-19, of whom 539 (49.4%) were positive for SARS-CoV-2 by PCR. Among symptomatic workers with negative PCR results (553 workers, 50.6% of symptomatic population), 197 (35.6%) had a positive result in the subsequent serologic test. Regarding the remaining 1,871 asymptomatic workers, serology was positive for 345 of them (18.4% of asymptomatic workers, accounting for 31.9% of total SARS-CoV-2 infections). Regarding the results of serology, 2,424 tests were performed,and 542 (22.4%) were positive. The vast majority of positive workers (487, 89.9%) were positive only for IgG antibodies; 40 (7.4%) were positive for both IgM and IgG antibodies; and 15 (2.8%) were positive only for IgM. All 55 workers with positive IgM tests underwent a SARS-CoV-2 PCR test to exclude active infection and these results were negative for all of them. Taking into account the results of both PCR and serology, 1,081 hospital workers (36.5%) of our institution had evidence of infection by SARS-CoV-2.
Fig. 2. Results of the study on hospital workers. In total, 103 workers could not be included in the survey and, therefore, where excluded from the analysis: 31 workers had symptoms of COVID-19 but without serologic test performed after a negative PCR; 10 symptomatic workers had no PCR or serology test performed; 62 asymptomatic workers had no serology test.
Characteristics of the different groups of infected workers
Workers without evidence of SARS-CoV-2 infection presented some differences from those who became infected (Table 1). No differences were detected in gender, pregnancy, or immunosuppression between any of the 3 groups of infected workers and the noninfected group. Compared with noninfected workers, symptomatic workers with positive PCR tests were older; they were less frequently smokers; and they more frequently presented comorbidities such as hypertension, diabetes, COPD, or immunosuppression (Table 1). Symptomatic workers with negative PCR and positive serology tests were older and more frequently presented hypertension and COPD than noninfected individuals. Finally, asymptomatic workers with positive serology tests presented fewer differences in comorbidities compared with noninfected individuals, who showed differences only in smoking habit (Table 1).
Table 1. Characteristics of the Different Groups of Infected Workersa
Note. P value, level of significance; IQR, interquartile range; COPD, chronic obstructive pulmonary disease.
a Statistics: Values are expressed as median (IQR) and absolute count (percentage). P values were calculated using the 2-tailed Fisher exact test for categorical variables and the Kruskal-Wallis test for continuous variables using the noninfected individual’s category as reference and were corrected for multiple comparisons using the Bonferroni procedure. Significant differences are shown in bold.
Regarding symptomatic workers, Supplementary Table 2 (online) summarizes the comparisons between those positive by PCR or serology. Clinical courses were similar for both groups, but those symptomatic workers with positive PCR results presented slightly higher percentages of fever (>38°C) and headache and notably higher percentages of anosmia and ageusia (Supplementary Table 2). Symptomatic workers with positive PCR tests had higher rates of hospital admission, but they did not have worse outcomes; pneumonia and ICU admission rates were almost the same for both subgroups. None of the workers died from COVID-19, and at the end of this study all who had been admitted to the hospital had already been discharged.
Impact of SARS-CoV-2 infection on different workers
The Distribution of COVID-19 cases is summarized in Table 2. Among the 2,614 HCWs, 977 (37.4%) became infected. Regarding nHCWs (349 workers), 104 (29.8%) were infected by SARS-CoV-2 and the difference in percentages of infection between HCW and nHCW was statistically significant (P = .006). In the group of HCWs, the most affected professional categories were hospital porters (83 cases, 44.9%), followed by nurses (340 cases, 39.6%) and auxiliary nursing care technicians. Regarding nHCWs, kitchen personnel were the most affected category (26 cases, 33.3%), followed by administrative staff (59 cases, 30.3%).
Table 2. Infection Rates by Professional Categories
a This category included mainly physiotherapists, psychologists and midwives.
b This category included maintenance personnel, engineers and cleaning personnel.
Risk factors associated with SARS-CoV-2 infection
The results of the logistic regression analysis of risk factors associated with infection are summarized in Table 3. Univariate analysis showed that type of hospital worker (ie, HCW), professional category (ie, hospital porters) and performance of AGP were significantly associated with infection, whereas the type of contact (close vs casual) was not statistically associated with infection. The use of PPE was a protective factor against infection (OR, 0.62; 95% CI, 0.48–0.079; P < .001). Recommended PPE for care of COVID-19 patients in the methods is summarized at the end of Table 3. Regarding previous reported contacts, contact with COVID-19 patients was more strongly associated with SARS-CoV-2 infection (OR, 5.10; 95% CI, 4.30–6.06; P < .001) than other reported contacts.
Table 3. Risk Factors Associated With SARS-CoV-2 Infection in Our Workers
Note. HCW, healthcare worker; nHCW, nonhealthcare worker; PPE, personal protective equipment; AGP, aerosol-generating procedure; P value, level of significance; OR, odds ratio; 95% CI, 95% confidence interval.
a Results for regression analysis are expressed as odds ratios (ORs). The 95% confidence intervals were calculated for each risk factor using the Wald approximation method. Significant differences are shown in bold. Multivariate analysis results show the most significant covariates, which were selected by a stepwise method (forward).
b This category included mainly physiotherapists, psychologists and midwives.
c This category included maintenance personnel, engineers and cleaning personnel.
d Recommended PPE for care of COVID-19 patients consisted of disposable medical caps, FFP2 masks, disposable medical protective clothing (waterproof), disposable gloves and protective goggles or protective screens. When an AGP was necessary, the involved workers wore FFP3 masks.
In the multivariate analysis, only the use of PPE (protective: OR, 0.56; 95% CI, 0.44–0.72; P < .001) and previous contact with COVID-19 patients (risk factor: OR, 1.69; 95% CI, 1.28–2.24; P < .001) were independent factors associated with SARS-CoV-2 infection, whereas type of contact (close vs casual) did not reach statistical significance (P = .081).
Discussion
Our study shows that our institution has suffered a huge impact of the COVID-19 pandemic; more than one-third of our workers have been infected with SARS-CoV-2. We found statistically significant differences in the rates of infection between HCWs and nHCWs. The use of PPE and a previous contact with COVID-19 patients were independent factors that were associated with SARS-CoV-2 infection.
The disparity in infection prevalence in hospital workers across Europe is high. For instance, in a German tertiary-care hospital located in an area with little impact of the pandemic, the prevalence of infected HCWs was only 1.6%.Reference Korth, Wilde and Dolff13 In another study carried out in a hospital specialized in infectious diseases in Naples, the prevalence was 3.4%.Reference Fusco, Pisaturo and Iodice14 Finally, another group of researchers in Brussels reported 12.6% infection at their institution.Reference Martin, Montesinos and Dauby15 In Spain, it is estimated that ~5% of the general population has antibodies against SARS-CoV-2 and in Madrid, this percentage increases to 11%.Reference Pollán, Pérez-Gómez and Pastor-Barriuso16 Regarding data of infections in HCWs in Spain, 2 different studies have been published. On the one hand, the study of Folgueira et alReference Folgueira, Munoz-Ruiperez, Alonso-Lopez and Delgado17 was performed only using RT-PCR and showed that 11.6% of all hospital workers had a PCR test positive for SARS-CoV-2. On the other hand, García-Basteiro et alReference Garcia-Basteiro, Moncunill and Tortajada18 also reported an 11.2% infection prevalence combining PCR and serology tests. In our hospital, combining PCR in symptomatic personnel and serology screening in both symptomatic and asymptomatic workers, we reached a prevalence of SARS-CoV-2 infection of 36.5%. These results contrast with those of other Spanish studies that show a prevalence 3 times lower. However, our results are from one of the most affected communities of Spain (Alcalá de Henares, Madrid), which had a cumulative incidence of 1,300 cases per 100,000 inhabitants as of June 28, 2020.9 Additionally, the rate of infection in hospital workers increased in parallel to the number of infected patients (Fig. 1).
This high rate of infection could reflect also the problem associated with the lack of proper PPE at the beginning of the pandemic,Reference Mandrola6 the initial recommendations against the generalized use of face masks,Reference Lewis7,Reference Liang, Gao and Cheng8 and/or the probable silent dispersion of the virus in the society and the hospital long before the first cases were detected by molecular methods.
This explanation is in line with our findings; in multivariate analysis, the use of PPE was an independent protective factor for SARS-CoV-2 infection (OR, 0.56; 95% CI, 0.44–0.72; P< .001). This finding also reflects the need to provide adequate PPEs to hospital workers to control the spread of the pandemic in this environment.
We found a high rate of false-negative results of PCR in symptomatic workers who later developed a serological response to SARS-CoV-2 (35.6%). This difference between analytical and clinical sensitivity of PCRs is widely known and has previously been described.Reference Woloshin, Patel and Kesselheim19 Another study performed at our institution showed that almost 90% of 63 clinical COVID-19 pneumonias, which tested negative by PCR for SARS-CoV-2, could be diagnosed through a rapid test detecting IgG and IgM antibodies.Reference Pérez-García, Pérez-Tanoira and Romanyk12 Our results reinforce the need to use tests complementary to PCR, such as serology, for initial diagnosis of SARS-CoV-2 infection.Reference Pan, Li and Yang20,Reference Quattrone, Vabanesi and Borghini21
Our study also points out the great problem posed by individuals with asymptomatic infection: in our hospital up to 31.9% of infections in workers were asymptomatic. As a consequence, for future epidemic waves, screening should cover all personnel, not just symptomatic individuals because those with asymptomatic infections also spread the virus.Reference Rivett, Sridhar and Sparkes22
We observed different infection rates between HCWs (37.4%) and nHCWs (29.8%). As expected, nurses, auxiliary nursing-care technicians, and medical staff presented higher rates of infection among HCWs (39.6%, 39.0%, and 34.7%, respectively), reflecting their close contact with COVID-19 patients. However, the most affected professional category in our institution were hospital porters (44.9%). There is some debate about whether hospital porters could be considered HCWs or nHCWs. However, beyond formal considerations, in our opinion, the work of hospital porters frequently involves contact with patients at short distance. This may explain why hospital porters were the most affected professional category in our hospital and indicates that they should be considered at-risk personnel who require adequate PPE. At the beginning of the pandemic in Wuhan, other researchers established that infections among HCWs occurred mainly in low-contagion areas, which supported the need for routine screening to detect asymptomatic carriers.Reference Lai, Wang and Qin23 Our results are in line with these findings—they reflect the need for screening in all professional categories in addition to that classically recognized to be at risk (nurses and physicians) as well as the importance of establishing an adequate workflow to interrupt nosocomial transmission routes.
Our study has some limitations. First, it was a retrospective analysis conducted in a single hospital. Consequently, we could not present data about the kind of PPE that was employed or the existence of possible breaches in PPE use. Further prospective multicenter studies are necessary to reinforce our findings. Second, our serologic results are based on the use of a lateral flow immunoassay (All Test COVID-19 IgG/IgM). The usefulness of this kind of test has been questioned due to a lack of official performance validations.Reference Krammer and Simon24 However, recently published studies have shown that these point-of-care tests could be a suitable option for seroepidemiological studies.Reference Pollán, Pérez-Gómez and Pastor-Barriuso16 Furthermore, we previously performed a validation of the test using 100 pre-pandemic sera and 90 serum samples from patients with positive PCR for SARS-CoV-2, and we found a specificity of 100% and a sensitivity of 88% from 14 days after the onset of symptoms. Thus, we concluded that this serologic test was reliable to diagnose SARS-CoV-2 infection and could be used for the seroprevalence study.Reference Pérez-García, Pérez-Tanoira and Romanyk12 However, some techniques based on ELISA or chemiluminescence could present sensitivities of almost 100%,Reference Padoan, Cosma, Sciacovelli, Faggian and Plebani25 and a second seroprevalence study with these techniques in our institution could yield interesting findings.
Despite these limitations, to the best of our knowledge, our study constitutes one of the largest cohorts regarding SARS-CoV-2 infection among hospital workers. Moreover, it was carried out on the entire hospital staff and provides relevant data about symptoms, comorbidities, infected professional categories, use of PPE, as well as contact investigation in one of the institutions that have been most affected by the pandemic.
Hospital workers are the first-line workforce for clinical care of COVID-19 patients; therefore, their security at work must be ensured to warrant the success facing the SARS-CoV-2 pandemic.26 During the first phase of the pandemic, the availability of PPE was quite limited in most European countries, and many hospital workers were supplied with equipment that might not meet protection standards. Adequate provision of PPE and individual support in terms of rest, family, and psychological support must be ensured by the hospital management.26,Reference Jin, Huang and Wang27 The danger of a second wave is real, and hospitals should establish a preparedness plan to minimize the impact of this highly contagious disease to protect their most valuable asset—their workers.Reference Barranco and Ventura28
Acknowledgments
We want to thank all workers of the Hospital Universitario Príncipe de Asturias for their enormous work, effort and dedication facing this pandemic during these difficult months.
Financial support
We did not received any specific grant from funding agencies in the public, commercial, or not-for-profit sectors for this research.
Conflicts of interest
The authors declare that they have no conflicts of interest.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2020.1303
Open access
