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Longitudinal analysis of risk factors associated with severe acute respiratory coronavirus virus 2 (SARS-CoV-2) infection among hemodialysis patients and healthcare personnel in outpatient hemodialysis centers

Published online by Cambridge University Press:  21 July 2022

Sumanth Gandra*
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Tingting Li
Affiliation:
Division of Nephrology, Washington University School of Medicine, St Louis, Missouri
Kimberly A. Reske
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Kate Peacock
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Karl G. Hock
Affiliation:
Department of Pathology and Immunology, Washington University School of Medicine, St Louis, Missouri
Silvana Bommarito
Affiliation:
Division of Nephrology, Washington University School of Medicine, St Louis, Missouri
Candace Miller
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Henry Stewart
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Na Le Dang
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Christopher W. Farnsworth
Affiliation:
Department of Pathology and Immunology, Washington University School of Medicine, St Louis, Missouri
Margaret A. Olsen
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Jennie H. Kwon
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
David K. Warren
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
Victoria J. Fraser
Affiliation:
Division of Infectious Diseases, Washington University School of Medicine, St Louis, Missouri
*
Author for correspondence: Sumanth Gandra MD, MPH, Division of Infectious Diseases, Department of Medicine, Washington University School of Medicine, Campus Box 8051, 4523 Clayton Ave, St Louis, MO63110. E-mail: gandras@wustl.edu

Abstract

In this prospective, longitudinal study, we examined the risk factors for severe acute respiratory coronavirus virus 2 (SARS-CoV-2) infection among a cohort of chronic hemodialysis (HD) patients and healthcare personnel (HCPs) over a 6-month period. The risk of SARS-CoV-2 infection among HD patients and HCPs was consistently associated with a household member having SARS-CoV-2 infection.

Type
Concise Communication
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
© The Author(s), 2022. Published by Cambridge University Press on behalf of The Society for Healthcare Epidemiology of America

Patients with end-stage renal disease (ESRD) on chronic hemodialysis (HD) are at increased risk of severe disease and death from severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection. Reference Ng, Hirsch and Wanchoo1 Despite vaccination, chronic HD patients are at risk for breakthrough SARS-CoV-2 infection due to attenuated Reference Anand, Montez-Rath and Han2,Reference Van Praet, Reynders and De Bacquer3 and receding immunological response to vaccines. Reference Anand, Montez-Rath and Han4Reference Bell, Campbell and Lambourg6 Several studies have examined the risk factors associated with SARS-CoV-2 infection among chronic HD patients; however, these were cross-sectional studies without longitudinal follow-up data. Reference Hsu, Weiner and Aweh7Reference Rincón, Moreso and López-Herradón10 Longitudinal data are valuable for identifying modifiable risk factors and devising strategies to prevent SARS-CoV-2 infection among HD patients. In this prospective, longitudinal study, we examined the risk factors for SARS-CoV-2 infection among a cohort of chronic HD patients and healthcare personnel (HCP) working in 3 outpatient HD units over a 6-month period.

Methods

This study was conducted in 3 outpatient HD units at the Washington University School of Medicine (WUSM) in St Louis, Missouri, and it was approved by the WU Human Research Protection Office. Adult patients on in-center HD and dialysis-center HCP were enrolled after giving informed consent, as described previously. Reference Gandra, Li and Reske11 A survey was administered either electronically or in-person at 3 different times (September 2020, December 2020, and March 2021) to patients and HCP to assess their household characteristics, personal behaviors and prevention activities, SARS-CoV-2 exposures, and history of SARS-CoV-2 infection since March 1, 2020.

Blood was also collected at these 3 times to assess SARS-CoV-2 infection status. Previous SARS-CoV-2 infection was assessed using the Abbott SARS-CoV-2 IgG serologic assay that targets the viral nucleocapsid protein (Abbott, Abbott Park, IL). The resulting unit for the SARS-CoV-2 IgG assay is the index (ie, signal/calibrator or S/C). An S/C value ≥1.40 was considered positive.

Electronic medical records of patients were reviewed at each survey and blood draw to obtain relevant clinical information, including dates of SARS-CoV-2 PCR test(s), hospitalizations due to SARS-CoV-2 infection, and symptoms. Comorbid conditions were reviewed at enrollment. The electronic medical records of HCP were not reviewed. All data were entered into a REDCap database.

We defined a SARS-CoV-2 case as having either a history of positive PCR test documented in the medical record or a positive IgG nucleocapsid serology result prior to each survey. For HCP, we only considered positive IgG serology to define a SARS-CoV-2 case because we did not review HCP medical records. Univariate analyses of patient characteristics among SARS-CoV-2 cases and noncases were performed using the Fisher exact test or the χ Reference Anand, Montez-Rath and Han2 test for categorical variables and the Mann Whitney U test for continuous variables. Statistical analyses were performed using SAS version 9.4 software (SAS Institute, Cary, NC), and P < .05 was considered statistically significant.

Results

Among the 3 HD units, 227 patients and 39 HCP were enrolled in the study (Fig. 1 and Supplementary Tables 1 and 2). At baseline, 22 (9.7%) of 227 patients had evidence of prior SARS-CoV-2 infection and none of the HCP had a SARS-CoV-2 infection. At the 3-month follow-up, 20 (10.6%) of 187 patients and 4 (15.2%) of 33 HCP had SARS-CoV-2 infection between the baseline and the 3-month follow-up. At the 6-month follow-up, 9 (5.8%) of 156 patients and 4 (16%) of 25 HCP had SARS-CoV-2 infection between the 3- and 6-month follow-ups. The cumulative incidence of SARS-CoV-2 infection among HD patients was 22.9% (52 of 227), which was 52 (26.5%) of 196 but excluding those lost to follow-up. The cumulative incidence of SARS-CoV-2 infection among HCP was 20.5% (8 of 39), which was 8 (25.8%) of 31 but excluding those lost to follow-up.

Fig. 1. Distribution of SARS-CoV-2 infection cases among HD patients and HCPs at baseline, 3 months and 6 months.

The baseline univariate analyses of risk factors associated with SARS-CoV-2 infection were published previously. Reference Gandra, Li and Reske11 In the analysis of the 3-month and 6-month surveys, SARS-CoV-2–infected cases were significantly more likely to have had a household family member with SARS-CoV-2 infection (3-month survey, 40% vs 4.2%; P ≤ .001; 6-month survey, 11.1% vs 2.8%; P = .029) and to have had a household family member asked to quarantine because of exposure to SARS-CoV-2 (6-month survey, 33.3% vs 2.1%; P ≤ .001) (Table 1). Additionally, for the 3-month survey, SARS-CoV-2–infected patients reported significantly less adherence to social distancing outside the dialysis units (50% vs 81.4%; P ≤ .004). The only risk factors for SARS-CoV-2 infection identified among HCP were household exposure (3-month survey, 80% vs 14.3%, P = .009; and 6-month survey, 75% vs 4.8%; P = .007) and having a household member instructed to quarantine (6-month survey, 100% vs 0%, P ≤ .001) (data not shown).

Table 1. Univariate Analysis of Characteristics of HD Patients Who Tested Positive or Negative for SARS-CoV-2 Infection at the 3-Month and 6-Month Follow-Up

Note. ND, not determined; BMI, body mass index; ESRD, end-stage renal disease; PKD, polycystic kidney disease; CAD, coronary artery disease; CVA, cerebrovascular accident; HF, heart failure; HD, hemodialysis; IQR, interquartile range.

a Defined as a positive PCR and/or serology for SARS-CoV-2.

b Other etiologies include glomerulonephritis, lupus nephritis, PKD, other.

c Other comorbidities include active malignancy, cirrhosis, current smoker, HIV, lung disease.

d Restricted to patients who reported attended a gathering with <10 people, a visit to a health facility or a visit to a public location.

Potential transmission events in the HD centers were examined (Supplementary Fig. 1). Most cases did not appear to be temporally or spatially related to any other SARS-CoV-2 cases. One shift at facility A had 3 positive patients who reported generally sitting in the same pod; 1 patient had a positive PCR result in November and 2 additional patients were IgG positive in December without any known SARS-CoV-2 exposures.

Discussion

Studies examining risk factors associated with SARS-CoV-2 infection among chronic HD patients and HCP working in HD units using repeated surveys are lacking. In our prior publication, several risk factors at baseline were associated with SARS-CoV-2 infection, including SARS-CoV-2 infection among immediate family members or friends, residence in a long-term care facility, poor adherence to face mask use, and travel outside the local metropolitan area. Reference Gandra, Li and Reske11 However, in the subsequent surveys, the only risk factor that remained associated with SARS-CoV-2 infection among chronic HD patients was having a household member with SARS-CoV-2 infection. Among HCP, the only risk factor associated with SARS-CoV-2 infection was having a household member with SARS-CoV-2 infection.

There appeared to be no patient-to-patient or patient-to-staff transmission in the dialysis units; however, we did not perform whole-genome sequencing to confirm this. In one facility, 2 patients were identified as IgG positive in without known SARS-CoV-2 exposures in the month after an infected patient was dialyzed in the same pod. Because it is not known when the 2 IgG-positive patients were exposed to SARS-CoV-2, no clear relationship between these cases could be discerned. The 3 HD units implemented the Centers for Disease Control and Prevention (CDC) SARS-CoV-2 infection prevention measures in March 2020. 12 Previous studies reported that implementation of infection prevention measures (eg, a universal mask policy) in HD units were associated with reduced risk of SARS-CoV-2 infection. Reference Caplin, Ashby and McCafferty9,Reference Biedunkiewicz, Tylicki, Puchalska-Reglińska and Dębska-Ślizień13 Our results are consistent with a previous study Reference Caplin, Ashby and McCafferty9 indicating that when recommended infection prevention measures are used in HD units, the risk of SARS-CoV-2 infection is dependent on exposures from contacts in patient homes, especially when the community burden of SARS-CoV-2 is high.

Our study had several limitations. Due to the small number of cases, we could not perform multivariate analysis to identify independent risk factors for SARS-CoV-2 infection. Survey responses may be subject to recall bias. Finally, our study was performed when most patients had not received the SARS-CoV-2 vaccine (only 33% of patients had received at least 1 dose of vaccine at the 6-month survey) and prior to the emergence of the SARS-CoV-2 o(omicron) variant. Thus, our results may not be generalizable to new SARS-CoV-2 variants that emerged after the study period or among vaccinated chronic HD patients.

In this longitudinal survey study in 3 outpatient HD units that implemented CDC SARS-CoV-2 infection prevention measures, the risk of SARS-CoV-2 infection among HD patients and HCPs was consistently associated with a household member having SARS-CoV-2 infection.

Supplementary material

For supplementary material accompanying this paper visit https://doi.org/10.1017/ash.2022.269

Acknowledgments

Financial support

This study was funded by the CDC Epicenters Program (grant no. 6 U54CK000482-04). The REDCap database is supported by the NIH Clinical and Translational Science Award (CTSA grant no. UL1 TR000448) and the Siteman Comprehensive Cancer Center and NCI Cancer Center (grant no. P30 CA091842). J.H.K. is supported by the National Institute of Allergy and Infectious Diseases (grant no. 1K23AI137321-01A1).

Conflicts of interest

M.A.O. received grant funding from Pfizer in the past 3 years and worked as consultant to Pfizer not related to COVID-19. All other authors have no relevant disclosures.

Footnotes

a

Authors of equal contribution.

b

Authors of equal contribution.

References

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Figure 0

Fig. 1. Distribution of SARS-CoV-2 infection cases among HD patients and HCPs at baseline, 3 months and 6 months.

Figure 1

Table 1. Univariate Analysis of Characteristics of HD Patients Who Tested Positive or Negative for SARS-CoV-2 Infection at the 3-Month and 6-Month Follow-Up

Supplementary material: PDF

Gandra et al. supplementary material

Tables S1-S2 and Figure S1

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