COVID-19 Reinfection in Healthcare Workers: An Original Comprehensive Longitudinal Study

doi:10.21203/rs.3.rs-3596390/v1

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Research Article

COVID-19 Reinfection in Healthcare Workers: An Original Comprehensive Longitudinal Study

https://doi.org/10.21203/rs.3.rs-3596390/v1

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Background

The ongoing evolution of SARS-CoV-2 has perpetuated the global prevalence of coronavirus disease 2019 (COVID-19) and the emergence of new cases. Healthcare workers (HCWs), given their heightened exposure to infected individuals, remain particularly susceptible to COVID-19 recurrence. The primary objective of this investigation was to explore the occupational risk factors contributing to COVID-19 recurrence among HCWs.

Methods

This longitudinal study was carried out in a specialized teaching hospital located in Tehran, Iran, approximately 20 months after the onset of the pandemic. HCWs were administered an online questionnaire specifically tailored to elicit information about their history of COVID-19 infections. Prediction modeling employed the use of generalized estimation equations.

Results

The study encompassed 601 HCWs, predominantly characterized by their female representation (60.2%), age bracket between 18 and 29 years (47.4%), and a notable absence of preexisting medical conditions or comorbidities (56.2%). This study revealed notable SARS-CoV-2 recurrence among HCWs, with 15% experiencing reinfection. Vaccination status had a significant influence on reinfection rates, precipitating a noteworthy reduction from 9.0% prevaccination to 1.4% post-initial dose and 5.0% following the second dose. In a comparative analysis, nurses exhibited more than a twofold increased risk of recurrence when juxtaposed against physicians and other HCWs. Furthermore, employment within a COVID-19 ward emerged as a substantial risk factor for reinfection. After adjusting for relevant risk factors within our predictive model, only occupation and working in COVID-19 wards emerged as statistically significant predictors in heightening the risk of reinfection.

Conclusion

This research underscores the escalated susceptibility of nurses, particularly those serving in COVID-19 wards. These findings have critical implications for the implementation of targeted interventions and enhanced infection control measures designed to safeguard HCWs effectively. Subsequent investigations should concentrate on larger prospective studies, delving further into the risk factors associated with SARS-CoV-2 recurrence, thereby enabling the refinement of preventive strategies for this high-risk demographic.

SARS-CoV-2

COVID-19

healthcare workers

reinfection

recurrence

risk factors

vaccination

pandemic

public health

occupational risk

What is known about this topic

SARS-CoV-2 mutations contribute to reinfections, prolonging the pandemic. However, the role of exposure in the reinfection of healthcare workers is controversial.

What this article adds

Vaccination significantly reduces the reinfection rate. Exposure to COVID-19 cases plays a crucial role in reinfection risk. Among HCWs, occupation is a strong predictor of reinfection, while nurses are at the highest risk of reinfection.

Since the emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the prevailing expectation has been that recovery from coronavirus disease 2019 (COVID-19) would confer immunity. However, SARS-CoV-2 has exhibited a propensity for mutations, resulting in the emergence of distinct strains, each characterized by region-specific genetic variations (1). This trait poses a challenge to the immune system's ability to recognize the virus. Consequently, the first documented case of recurrent COVID-19 involved a 33-year-old immunocompetent male who contracted a genetically distinct variant 142 days after his initial infection, despite testing negative twice during that period (2). The ongoing mutational activity of SARS-CoV-2 underscores the potential for the emergence of novel variants, significantly impacting disease transmission, severity, and the medical community's capacity to diagnose, manage, prevent, and control the landscape of infection (3).

The investigation of reinfection holds significant implications for various reasons. First, it provides crucial insights into the durability of immunity following natural infection or vaccination. This is pivotal for assessing future protection against infection and determining the need for booster shots to sustain continuous immunity (4). It enables the evaluation of vaccine efficacy, thereby informing the development of optimal vaccination strategies (5). Furthermore, reinfection studies yield vital insights that inform evidence-based decisions in public health, such as vaccine distribution, scheduling, and preventive measures such as mask-wearing and social distancing (6). Last, understanding the role of reinfection contributes to the assessment of the combined impact of naturally acquired immunity and vaccination in achieving herd immunity, a critical factor in controlling the spread of infectious diseases within populations (7).

The susceptibility to reinfection is influenced by various factors, including vaccination status (5), the emergence of new variants such as the Omicron Variant (8), the severity of the initial infection (8), the presence of comorbidities (5), and age (5, 8). Nevertheless, even after considering other risk variables, frontline healthcare workers (HCWs) exhibit a COVID-19 infection rate at least three times higher than that of the general population (9). The susceptibility of healthcare workers to reinfection can vary depending on multiple factors, such as age, comorbidity status, workplace environment, occupation type, and vaccination status (4, 5, 10).

Healthcare workers play a pivotal role in providing direct patient care, including disease spread, promoting vaccination, responding to emergencies, advancing medical knowledge, advocating for public health, and enhancing healthcare outcomes. Therefore, it is imperative to establish practical strategies and precautions to safeguard their well-being. This study aims to assess the recurrence rate of self-reported COVID-19 among HCWs and explore potential risk factors contributing to a higher likelihood of reinfection.

Study Design and Participants

In this retrospective longitudinal study, we investigated the prevalence of COVID-19 recurrence and potential associated risk factors among healthcare workers (HCWs) from February 2019 to October 2021 utilizing a structured checklist. All HCWs employed at the Hazrat Rasool Medical Center, a referral hospital with 800 beds located in Tehran, Iran, featuring multiple dedicated COVID-19 wards during the pandemic, were included in this study. Exclusion criteria consisted of individuals who declined to provide informed consent, those with incomplete or unreliable responses on the checklist, or those who could not recall specific details regarding their COVID-19 history.

Data Collection and Checklist Development

To comprehensively capture essential information concerning participants' COVID-19 history and potential reinfection occurrences during the study period, a team of specialized professionals designed a structured checklist founded on established guidelines and scholarly references. This comprehensive checklist encompassed diverse sections, including demographic particulars, SARS-CoV-2 vaccination status, prior COVID-19 diagnoses, pertinent medical histories, utilization of personal protective equipment (PPE), and familial COVID-19 histories. Additionally, specific queries were integrated to evaluate symptoms associated with the initial infection and potential reinfection episodes. All questions employed a multiple-choice format to mitigate response errors. The checklist was administered electronically through a secure online survey platform utilizing various social media channels between October and March 2021. It was recurrently shared within social media groups to maximize the number of respondents.

Study Variables and Outcomes

Participant identities were safeguarded through the allocation of unique ID numbers. Key study variables included age, gender, blood group, past medical history, smoking and alcohol consumption habits, occupation, workplace location, duration of employment in a week, educational background, family medical history, and vaccination status. Study outcomes encompassed the determination of the prevalence of SARS-CoV-2 recurrence among HCWs and the identification of predictors associated with recurrence.

COVID-19 Diagnosis and Recurrence Definition

COVID-19 diagnoses were established based on a physician's assessment using a combination of symptoms, serology tests, chest CT scans, and/or polymerase chain reaction (PCR) tests. SARS-CoV-2 recurrence was defined as the occurrence of two or more SARS-CoV-2 infections, irrespective of the time interval between these episodes. The occupational categorization included nurses, physicians, clinical staff, and nonclinical staff. Physicians consisted of specialists, residents, and interns. Clinical staff comprised individuals working in clinical wards or engaging in direct patient interactions, while nonclinical staff encompassed medical students and other personnel.

Statistical Analysis

The dataset was structured longitudinally based on vaccination dose status. Descriptive statistics were employed to present study variables as frequencies (percentages), and chi-square and Fisher’s exact tests were utilized for analysis. Subsequently, a multivariable generalized estimation equation (GEE) was implemented to predict potential risk factors for reinfection. Vaccination status was treated as a within-subject variable with an autoregressive order 1 (AR1) correlation structure. Variables were selected through a backward selection process, retaining those with p values ≤ 0.1 in the multivariable model. Data analysis was executed using IBM SPSS Statistics version 26 and STATA software version 17 (StataCorp. LLC, US).

Ethics and Consent

This study received approval from the Iran University of Medical Sciences Ethics Committee (IR.IUMS.FMD.REC.1401.034). Informed consent was diligently obtained from all participants before their engagement in the survey. The study strictly adhered to the principles outlined in the Declaration of Helsinki and other pertinent ethical guidelines.

A total of 601 healthcare workers (HCWs) were included in this study, and their baseline characteristics are summarized in Table 1 (see the end of the document). The majority of participants were female (60.2%), with approximately half falling within the age range of 18 to 29 years (47.4%). Among the participants, 338 individuals (56.2%) reported no underlying medical conditions. Comorbidities were distributed as follows: 14 participants (2.3%) had diabetes mellitus, 23 participants (3.8%) had hypertension, nine participants (1.5%) had cardiovascular disorders, 31 participants (5.2%) had asthma, and four participants (0.7%) had chronic obstructive pulmonary disease. Current smokers accounted for 33 individuals (5.5%). In terms of occupation, 35.1% were physicians, 19.6% were nurses, while the remaining participants (45.3%) encompassed clinical and nonclinical staff members and students. Additionally, 8.2% of participants were employed in COVID-19 wards. Regarding vaccination status, 17 participants (2.8%) had not received any vaccines, while 20 participants (3.3%) had received only the first dose of the vaccine. The most frequently administered vaccines were Sputnik (36.8%) and AstraZeneca (30.4%). Other vaccines included Sinopharm, Pfizer, Bharat, Barkat, and Razi. Notably, a total of 90 reinfection episodes were detected (15.0%), involving 72 individuals (11.98%). Specifically, 54 participants (9.0%) experienced reinfection before vaccination, eight participants (1.4%) after the first vaccine dose, and 28 participants (5.0%) after the second dose. Significant differences were observed in occupation categories (p = 0.03) and types of masks used (p = 0.01) between the reinfected and nonreinfected groups. No significant differences were found in baseline characteristics between the two groups. Additionally, variables including blood group, smoking status, alcohol use, work duration, usage of different kinds of personal protective equipment (PPE) (except kind of mask usage, p = 0.01), familial history of COVID-19, and vaccine brand were assessed, revealing no significant differences between the two groups.

Table 1

Baseline characteristics of the participants and association between risk factors and recurrence ^a.
Characteristics	Total(n = 601)	Participants with reinfection(n = 72)	Participants without reinfection(n = 529)	p value ^b
Age group				0.88
18–29 yr	285(47.4)	35(48.6)	250(47.3)
30–39 yr	153(25.5)	17(23.6)	136(25.7)
40–49 yr	109(18.1)	14(19.4)	95(18.0)
50–59 yr	47(7.8)	6(8.3)	41(7.8)
≥ 60 yr	7(1.2)	0(0)	7(1.3)
Sex				0.72
Male	239(39.8)	30(41.7)	209(39.5)
Female	362(60.2)	42(58.3)	320(60.5)
Blood group				0.43
A+	187(31.1)	25(34.7)	162(30.6)
A-	18(3)	3(4.2)	15(2.8)
B+	112(18.6)	10(13.9)	102(19.3)
B-	14(2.3)	2(2.8)	12(2.3)
O+	181(30.1)	24(33.3)	157(29.7)
O-	28(4.7)	2(2.8)	26(4.9)
AB+	44(7.3)	2(2.8)	42(7.9)
AB-	6(1)	2(2.8)	4(0.8)
Medical condition
Diabetes mellitus	14(2.3)	3(4.2)	11(2.1)	0.27
Hypertension	23(3.8)	2(2.8)	21(4.0)	1.00
Cardiovascular disorders	9(1.5)	1(1.4)	8(1.5)	1.00
Asthma	31(5.2)	4(5.6)	27(5.1)	0.78
Chronic obstructive pulmonary disease	4(0.7)	1(1.4)	3(0.6)	0.40
Smoker	33(5.5)	2(2.8)	31(5.9)	0.14
Alcohol use	21(3.5)	2(2.8)	19(3.6)	1.00
< 14 g	19(3.2)	1(3.6)	18(3.1)	0.99
14–28 g	1(0.2)	0(0)	1(0.2)
> 28 g	1(0.2)	0(0)	1(0.2)
Occupation				0.03
Physician	211(35.1)	19(26.4)	192(36.3)
Nurse	118(19.6)	23(31.9)	95(18.0)
Clinical staff ^c	212(35.3)	25(34.7)	187(35.3)
Nonclinical staff ^d	60(10)	5(6.9)	55(10.4)
Work in clinical ward				0.15
Covid-19 ward	49(8.2)	9(12.5)	40(7.6)
Non-Covid-19 ward	428(71.2)	53(73.6)	375(70.9)
Work duration				0.57
< 30 h	148(24.6)	14(19.4)	134(25.3)
30–50 h	271(45.1)	32(44.4)	239(45.2)
> 50 h	165(27.5)	23(31.9)	142(26.8)
Education				0.12
Student	162(27)	22(30.6)	140(26.5)
Diploma and underdiploma	49(8.2)	8(11.1)	41(7.8)
Upper-diploma, BSc, MSc	196(32.6)	27(37.5)	169(31.9)
GP, PhD, and higher levels	189(31.4)	14(19.4)	175(33.1)
Personal protective equipment (PPE)
Kind of mask				0.01
Cloth mask	13(2.2)	2(2.8)	11(2.1)
Surgery mask	200(33.3)	28(38.9)	172(32.5)
2 surgery masks	97(16.1)	9(12.5)	88(16.6)
N95	96(16)	17(23.6)	79(14.9)
N95 + surgery mask	54(9)	10(13.9)	44(8.3)
Gloves				0.34
None	139(23.1)	23(31.9)	116(21.9)
Latex	317(52.7)	34(47.2)	283(53.5)
Plastic	52(8.7)	4(5.6)	48(9.1)
Both	33(5.5)	3(4.2)	30(5.7)
Eye protection				0.67
none	328(54.6)	36(50.0)	292(55.2)
Glass	83(13.8)	9(12.5)	74(14.0)
Shield	124(20.6)	16(22.2)	108(20.4)
both	19(3.2)	4(5.6)	15(2.8)
Gown	252(41.9)	33(45.8)	219(41.4)	0.41
Family history
Hospitalization in relatives	125(20.8)	17(23.6)	108(20.4)	0.82
Death in relatives	76(12.6)	12(16.7)	64(12.1)	0.54
Vaccine brand				0.90
None	17(2.8)	3(4.2)	14(2.6)
Sputnik	221(36.8)	28(38.9)	193(36.5)
Sinopharm	102(17)	13(18.0)	89(16.8)
Asterazeneca	183(30.4)	20(27.8)	163(30.8)
Other ^e	78(13)	8(11.1)	70(13.3)
BSc: bachelor of science; MSc: master of science; GP: general practitioner; PhD: doctor of philosophy. ^a Categorical variables are presented as numbers (%). ^b p ≤ 0.05 considered significant. ^c Including externs. ^d Including medical students.

A multivariable generalized estimation equation (GEE) analysis was conducted. In unadjusted analysis, a significant association was observed between vaccination status (OR, 0.14, 95% CI, 0.07 to 0.27; p < 0.001 for the period after the first vaccine dose, and OR, 0.49, 95% CI, 0.31 to 0.78; p < 0.01 for the period after the second dose) and being a nurse (OR, 2.17, 95% CI, 1.19 to 3.97; p = 0.01) with COVID-19 reinfection. After adjusting for confounding factors, the analysis indicated that vaccination status (OR, 0.16, 95% CI, 0.08 to 0.32; p < 0.001 for the period after the first dose, and OR, 0.59, 95% CI, 0.36 to 0.95; p = 0.03 for the period after the second dose), being a nurse (OR, 2.33, 95% CI, 1.15 to 4.74; p = 0.02), and working in the COVID-19 ward (OR, 2.04, 95% CI, 1.04 to 4.02; p = 0.04) were identified as potential predictors of COVID-19 reinfection (see Table 2). This analysis indicates that nurses and clinical staff, in the second instance, have more than a twofold risk of COVID-19 recurrence compared to physicians.

Table 2

Prediction of recurrence, GEE multivariable analysis.
Variables	Unadjusted		Adjusted
Variables	OR (95% CI)	p value ^a	OR (95% CI)	p value ^a
Vaccination status
Before vaccination	1.00	1.00	1.00	1.00
After the first dose	0.14(0.07–0.27)	< 0.001	0.16(0.08–0.32)	< 0.001
After the second dose	0.49(0.31–0.78)	< 0.01	0.59(0.36–0.95)	0.03
Male	1.18(0.75–1.86)	0.48	1.70(0.96–3.02)	0.07
Occupation
Physician	1.00	1.00	1.00	1.00
Nurse	2.17(1.19–3.97)	0.01	2.33(1.15–4.74)	0.02
Clinical staff	1.25(0.69–2.24)	0.46	1.16(0.60–2.24)	0.66
Nonclinical staff	1.44(0.47–2.78)	0.76	0.83(0.24–2.87)	0.77
Work in covid-19 ward	1.83(0.94–3.58)	0.08	2.04(1.04–4.02)	0.04
OR: odds ratio; 95% CI: 95% confidence interval ^a p ≤ 0.05 considered significant.

The objective of this study was to evaluate the prevalence of SARS-CoV-2 reinfection among healthcare workers (HCWs) and determine the factors influencing their susceptibility to reinfection. Our findings indicate that occupational factors play a significant role in the likelihood of reinfection, while specific baseline characteristics may also contribute to the risk of COVID-19 reinfection.

High Prevalence of SARS-CoV-2 Recurrence Among Healthcare Workers

Our investigation revealed a COVID-19 recurrence rate of 15%, signifying a substantial rate of recurrence in Iran. In comparison, prior studies have reported varying reinfection rates among HCWs, ranging from 5.94–20.57%, with notable differences potentially arising from variations in diagnostic certainty and the inclusion of probable cases (11–15). The criteria used to define recurrence or reinfection based on the time interval between positive SARS-CoV-2 tests may also contribute to these disparities. The recurrence rate of SARS-CoV-2 was reported to be 20.57% among HCWs in the Rivelli A. study (7). However, the reinfection rate was reported as 5.94% (7). Vaezi A. et al. identified 6.3% reinfection among seronegative healthcare workers in Iran in 2021 (16). This study was conducted in October 2020, when the third peak in Iran started; in contrast, our study contains five peaks of the COVID-19 pandemic in Iran. Alebouyeh M. et al. estimated a reinfection rate of 13.7% in HCWs, which is in line with our results in the same juncture (17).

Significant reduction in the recurrence rate after vaccination

Our analysis highlights a significant reduction in the rate of SARS-CoV-2 recurrence, declining from 9.0% before vaccination to 1.4% after the first vaccine dose and 5.0% after the second dose. The lower recurrence after the first dose compared to the second dose can be attributed to the short period between the first and second doses, which was approximately one to three months. This decline is in line with previous research. For instance, Hall V. et al. demonstrated a significant reduction in the crude incidence rate of reinfection from 2.25 reinfections/10,000 person-days at risk for unvaccinated individuals to 0.43 after the first dose and 0.4 reinfections/10,000 person-days at risk after the second dose of vaccination with Pfizer-BioNTech (18). Similarly, Malhotra S. et al. and Ozdemir Y. E. et al. reported a lower incidence rate of reinfection among fully vaccinated individuals (5, 19). Ozdemir Y. E. et al. suggested that individuals remain susceptible to reinfection without vaccination, especially three months after the initial infection (19).

Heightened Risk of Reinfection Among Nurses

Our study reveals that nurses face more than a twofold increased risk of COVID-19 recurrence compared to physicians and other healthcare workers. Additionally, working in a COVID-19 ward emerged as a significant risk factor for reinfection. This underscores the strong connection between exposure to SARS-CoV-2 and the subsequent risk of reinfection. Previous research by Nguyen L. H. et al. supports the notion that SARS-CoV-2 exposure significantly increases the risk of infection, with frontline HCWs being 12 times more likely to contract the virus than the general population (20). In contrast, Leidi A. et al. did not find significant differences in reinfection risk between occupational groups (21). However, Ramos W. et al. reported a higher risk of reinfection among those with direct contact with COVID-19 cases in their work environment. They also found that physicians and nurses had a higher risk of hospitalization compared to other HCWs (15). In addition, physicians and nurses, in the second degree, were at higher risk of hospitalization than other HCWs (15). Studies by Pople D. et al. and Costa LGVD. Et al. further confirmed the elevated risk of SARS-CoV-2 infection among HCWs with greater exposure to COVID-19 cases (4, 22). It seems that more exposure to COVID-19 cases and occupations with the most exposure are at the highest risk of reinfection, which supports our findings.

Impact of Baseline Characteristics and PPE Usage

Our study did not identify significant associations between baseline characteristics, including age, sex, blood group, underlying diseases, smoking, alcohol consumption, family history of COVID-19, and education, and the risk of COVID-19 recurrence. Likewise, we did not observe significant differences in the types of masks used as part of personal protective equipment (PPE) concerning the risk of reinfection. These findings align with several studies that have not established correlations between reinfection risk in healthcare workers and age (17, 22), blood group (17), gender (22, 23), underlying disease (22, 23), smoking (22), and PPE usage (22). However, other investigations have suggested potential risk factors for reinfection, such as age (5, 8), immunosuppressed conditions (22), underlying disease (17), and type A blood group (23).

Strength and Limitations

This study's strengths lie in its comprehensive data collection, covering a wide range of demographic, vaccination, occupation, workplace, and relevant factors. The utilization of generalized estimation equation (GEE) analysis enhances the robustness of our findings, offering valuable insights into healthcare policies and strategies. However, limitations include potential recall bias and accuracy concerns associated with self-reported data, as well as potential selection bias due to the voluntary nature of participation. Future research should consider more extensive prospective studies with definitive diagnostic testing to build upon these findings.

In conclusion, our study underscores the heightened risk of SARS-CoV-2 reinfection among male nurses working in COVID-19 wards with direct exposure to cases. This emphasizes the need for targeted interventions, including tailored infection control measures, to safeguard healthcare workers in these roles.

SARS-CoV-2

Severe Acute Respiratory Syndrome Coronavirus 2

COVID-19

Coronavirus Disease 2019

HCW

Healthcare Worker

PPE

Personal Protective Equipment

CT scan

Computed Tomography scan

PCR

Polymerase Chain Reaction

GEE

Generalized Estimation Equation, AR1:Autoregressive Order 1.

Ethics approval and consent to participate

Consent for publication

Not applicable

Availability of data and materials

The datasets generated and/or analyzed during the current study are not publicly available due to participant confidentiality policies and laws but are available from the corresponding author upon reasonable request.

Competing interests

The authors declare that they have no competing interests

Funding

The Iran University of Medical Sciences (IUMS) supported this research financially.

Authors' contributions

YK contributed significantly to the study design, questionnaire development, data acquisition, data production, analysis, and data interpretation and took the lead in writing the initial and final drafts of the manuscript. AA played a role in data acquisition, data production, and analysis and contributed to the initial draft of the manuscript. SAYA analyzed and interpreted the dataset. TR, SK, NN, and SS facilitated questionnaire distribution and data acquisition. HRB played a crucial role in shaping the study design, questionnaire development, analysis, interpretation, and revision of the manuscript. AG played a significant role in shaping the study design, questionnaire development, data acquisition, data production, and manuscript revision. All the authors have read and approved the final manuscript.

Declaration of AI-assisted technologies in the writing process

While preparing this work, the author used ChatGPT-3.5 to enhance readability and fluency. After using this tool, the author reviewed and edited the content as needed and took full responsibility for the publication's content.

Acknowledgment

The authors would like to thank the staff of the Rasool Akram Medical Complex for their contribution to data collection.

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No competing interests reported.

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COVID-19 Reinfection in Healthcare Workers: An Original Comprehensive Longitudinal Study

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Abstract

Background

Methods

Results

Conclusion

Capsule summary

Introduction

Methods

Study Design and Participants

Data Collection and Checklist Development

Study Variables and Outcomes

COVID-19 Diagnosis and Recurrence Definition

Statistical Analysis

Ethics and Consent

Results

Discussion

High Prevalence of SARS-CoV-2 Recurrence Among Healthcare Workers

Significant reduction in the recurrence rate after vaccination

Heightened Risk of Reinfection Among Nurses

Impact of Baseline Characteristics and PPE Usage

Strength and Limitations

Conclusion

Abbreviations

Declarations

References

Additional Declarations

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