As of September 6, 2020, there were nearly 27 million confirmed cases of coronavirus disease 2019 (COVID-19) worldwide, with >870,000 deaths. From mid-March through May 2020, New York City was the epicenter of the United States outbreak.
As the pandemic continued, information regarding the effects of COVID-19 on patients on dialysis became available.1,2 Generally, patients on dialysis have high rates of hospitalizations and mortality for cardiovascular and infectious causes,3 with infections the second most common cause of death.4 In the setting of COVID-19, patients on dialysis have specific risk factors associated with this highly contagious pathogen: older age3 and high prevalence rates of diabetes mellitus and hypertension, all of which are associated with worse outcomes in COVID-19.1,2,5 Studies thus far have not described the natural history, spectrum of disease, or effects of COVID-19 on patients on dialysis.
In this article, we report the experience of a small dialysis organization in the New York City and Long Island region from March 8, 2020 to April 20, 2020. A surveillance program identified patients on dialysis with suspected or confirmed COVID-19 by screening at every dialysis encounter, providing the opportunity to explore the challenges related to social determinants of health, particularly race or ethnicity and immigration status.
Methods
Atlantic Dialysis Management Services, LLC (ADMS), a regional small dialysis organization operating 13 facilities in New York City and Long Island, initiated a prospective Centers for Disease Control and Prevention–guided program to screen patients on dialysis for signs and symptoms of COVID-19 as well as ascertain known unprotected exposure (no mask on at least one person) to a person with symptoms or confirmed COVID-19 diagnosis. Positively screened patients on dialysis were referred for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) testing, hospitalization, or both and were considered persons under investigation (PUIs). PUIs were followed for symptom changes, hospitalization, death, and results of COVID-19 testing (Supplemental Figure 1). Asymptomatic PUIs or those negative for COVID-19 were considered COVID-19–negative. PUIs who tested positive, had signs and symptoms consistent with COVID-19, or both were considered COVID-19–positive or COVID-19–symptomatic patients.
We obtained demographic information from the facilities’ electronic health records. Patients on dialysis without Social Security numbers were considered undocumented residents.6
Statistical analysis focused on the PUI cohort. Chi-squared tests compared demographic characteristics between COVID-19–positive/symptomatic and COVID-19–negative groups. Focusing on the COVID-19–positive/symptomatic cohort, we explored how demographic characteristics and comorbidities were associated with hospitalization and mortality as outcomes (using bivariate Firth penalized logistic regressions because of the limited number of patients). We used Stata 14 (StataCorp 2014) for all analyses.
Results and Discussion
Among our study population of 2178 patients on dialysis, we found a 14% prevalence of COVID-19–positive/symptomatic patients, much higher than the 2.6% prevalence in the general New York City population.5 There were 408 PUIs; 306 PUIs (75%) were COVID-19-positive/symptomatic, and 244 of the latter (79.7%) had confirmed positive COVID-19 tests, an incidence of 112 per 1000 (Supplemental Figure 1). Given overall rates of COVID-19 of 25 per 1000 for New York City and 28 per 1000 for the New York City borough of Queens,5 it is apparent that New York City patients on dialysis were at higher risk of community exposure to COVID-19. The most common signs and symptoms of COVID-19 in the study population were fever (44%), cough (28%), and weakness or fatigue (20%), similar to those found in a recent study of ESKD admissions at a New York City medical center.1
Compared with COVID-19–negative patients, COVID-19–positive/symptomatic patients had considerably higher odds of death and hospitalization and marginally higher odds of emergency department visits (Supplemental Table 1). Demographic characteristics and specific residence were similar for both groups (Supplemental Table 2).
COVID-19–positive/symptomatic patients were more likely to be men and Black or Hispanic; their average age was 64 years, and their time on dialysis was longer compared with the total ADMS population of patients on dialysis (Supplemental Table 3). Of the 306 COVID-19–positive/symptomatic patients, 135 (44%) resided in Queens, comprising 15% of the 880 ADMS patients on dialysis in Queens (Supplemental Table 3). Of the 104 ADMS patients on dialysis in Manhattan, 24 (23%) were COVID-19 positive/symptomatic (a higher rate than in Queens and other locations), but more than half the patients on dialysis in the Manhattan facilities were from nursing homes.
Of the cohort of COVID-19–positive/symptomatic patients, 178 (58%) were hospitalized, 8% of the total ADMS population (Table 1). Patients residing in Queens had significantly increased odds of hospitalization (odds ratio [OR], 2.39; 95% confidence interval [95% CI], 1.01 to 5.69) (Table 2). The increased odds likely reflects the high population density of Queens.7
Table 1.
Demographic characteristics and comorbidities of the total ESKD population, of the total COVID-19 (those positive for SARS-CoV-2 RNA and those presumed to be positive on the basis of case presentation and symptoms) cohort, and by outcome
| COVID-19 (+/S) Patients, n=306 | Hospitalized COVID-19 (+/S) Patients, n=178 | COVID-19 (−) Patients, n=102 | Died COVID-19 (+/S) Patients, n=85 | Total ADMS Patients, n=2178 | |
|---|---|---|---|---|---|
| Age, yr, n (%) | |||||
| 18–44 | 30 (10) | 18 (10) | 13 (13) | 3 (4) | 221 (10) |
| 45–54 | 44 (14) | 28 (16) | 19 (19) | 4 (5) | 323 (15) |
| 55–64 | 73 (24) | 39 (22) | 27 (26) | 17 (20) | 569 (26) |
| 65–74 | 87 (28) | 46 (26) | 23 (23) | 26 (31) | 559 (26) |
| Over 75 | 72 (24) | 47 (26) | 21 (21) | 35 (41) | 508 (23) |
| Average age, yr | 64±13.5 | 64±12.6 | 61±14.8 | 70±11.9 | 63±14.0 |
| ESKD vintage, yr | 4.5±4.0 | 4.8±4.4 | 3.7±3.1 | 5.5±4.4 | 3.8±6.0 |
| Men, n (%) | 192 (63) | 106 (60) | 61 (60) | 57 (67) | 1299 (60) |
| Race, n (%) | |||||
| White | 31 (10) | 23 (13) | 11 (11) | 8 (9) | 234 (11) |
| Black | 117 (38) | 67 (38) | 45 (44) | 33 (39) | 749 (34) |
| Asian | 39 (13) | 20 (11) | 12 (12) | 13 (15) | 221 (10) |
| Hispanic | 113 (37) | 67 (38) | 29 (28) | 28 (33) | 537 (25) |
| Comorbid conditions, n (%) | |||||
| Diabetes | 110 (36) | 87 (49) | 43 (42) | 43 (51) | 1418 (65) |
| Hypertension | 115 (38) | 86 (48) | 43 (42) | 38 (45) | 1309 (60) |
| CHF | 30 (10) | 25 (14) | 13 (13) | 18 (21) | 207 (10) |
| CAD | 15 (5) | 24 (13) | 3 (3) | 15 (18) | 293 (13) |
| Location | |||||
| Brooklyn | 92 (30) | 52 (29) | 33 (3) | 28 (33) | 634 (29) |
| Queens | 135 (44) | 84 (47) | 51 (50) | 34 (40) | 880 (40) |
| Bronx | 30 (10) | 17 (10) | 9 (9) | 10 (12) | 293 (13) |
| Nassau and Suffolk Counties | 24 (8) | 15 (8) | 7 (7) | 8 (9) | 201 (9) |
| Manhattan | 24 (8) | 10 (6) | 2 (2) | 4 (5) | 104 (5) |
| Treatment modality, n (%) | |||||
| Peritoneal dialysis | 2 (0.6) | 2 (1) | 2 (2) | 1 (1) | |
| Home hemodialysis | 1 (0.3) | 1 (0.6) | |||
| Death, n (%) | 85 (28) | 48 (25) | 0 |
Hospitalized/died includes all patients in the PUI group who were hospitalized or died, and total ADMS indicates prevalent patients on dialysis at all facilities. COVID-19 (+/S), all individuals tested positive for SARS-CoV-2 RNA and those presumed to be positive on the basis of case presentation and symptoms. CHF, congestive heart failure; CAD, coronary artery disease.
Table 2.
Risk factors for hospitalization and death in the COVID-19 (those positive for SARS-CoV-2 RNA and those presumed to be positive on the basis of case presentation and symptoms) cohort
| Hospitalization | Death | |||
|---|---|---|---|---|
| OR (95% CI) | P Value | OR (95% CI) | P Value | |
| Borough/City | ||||
| Manhattan | 1 | 1 | ||
| Queens | 2.39 (1.01 to 5.69) | 0.05 | 1.64 (0.55 to 4.86) | 0.37 |
| Brooklyn | 1.79 (0.73 to 4.38) | 0.28 | 2.01 (0.66 to 6.12) | 0.22 |
| Bronx | 1.79 (0.62 to 5.19) | 0.20 | 2.33 (0.66 to 8.25) | 0.19 |
| Long Island | 1.64 (0.52 to 5.15) | 0.39 | 1.79 (0.46 to 7.03) | 0.40 |
| Sex | ||||
| Women | 1 | 1 | ||
| Men | 0.72 (0.45 to 1.16) | 0.18 | 1.29 (0.76 to 2.17) | 0.34 |
| Race/ethnicity | ||||
| White | 1 | 1 | ||
| Black | 0.47 (0.20 to 1.13) | 0.91 | 1.08 (0.45 to 2.61) | 0.86 |
| Hispanic | 0.51 (0.21 to 1.22) | 0.13 | 0.95 (0.39 to 2.32) | 0.92 |
| Asian | 0.38 (0.14 to 1.03) | 0.06 | 1.40 (0.51 to 3.91) | 0.51 |
| Multiracial or other | 0.36 (0.03 to 3.97) | 0.41 | 2.76 (0.25 to 30.33) | 0.40 |
| Social Security number | ||||
| Yes | 1 | 1 | ||
| No | 0.96 (0.54 to 1.68) | 0.89 | 2.34 (1.31 to 4.18) | 0.004a |
| Age, yr | ||||
| 18–44 | 1 | 1 | ||
| 45–54 | 1.17 (0.46 to 2.99) | 0.75 | 0.87 (0.20 to 3.82) | 0.86 |
| 55–64 | 0.77 (0.33 to 1.81) | 0.55 | 2.43 (0.71 to 8.37) | 0.16 |
| 65–74 | 0.76 (0.33 to 1.74) | 0.51 | 3.38 (1.02 to 11.26) | 0.05a |
| 75 or older | 1.26 (0.53 to 2.99) | 0.60 | 7.44 (2.23 to 24.78) | 0.001a |
| ESKD vintage, yr | 0.97 (0.92 to 1.03) | 0.31 | 1.1 (1.01 to 1.14) | 0.01a |
| Diabetes | ||||
| No | 1 | 1 | ||
| Yes | 1.27 (0.80 to 2.00) | 0.31 | 1.26 (0.77 to 2.07) | 0.36 |
| Hypertension | ||||
| No | 1 | 1 | ||
| Yes | 0.91 (0.58 to 1.43) | 0.67 | 0.77 (0.47 to 1.28) | 0.32 |
| CHF | ||||
| No | 1 | 1 | ||
| Yes | 0.79 (0.42 to 1.46) | 0.45 | 1.78 (0.94 to 3.41) | 0.08 |
| CAD | ||||
| No | 1 | 1 | ||
| Yes | 0.71 (0.38 to 1.32) | 0.28 | 1.28 (0.66 to 2.49) | 0.46 |
Results from univariate Firth penalized logistic regressions with hospitalization and death as outcomes, and demographic variables and comorbidities as explanatory variables. The nonadjusted OR and the 95% CI are indicated for each outcome. CHF, congestive heart failure; CAD, coronary artery disease.
Statistically significant.
Among the COVID-19–positive/symptomatic patient cohort, 85 deaths (28%) occurred, representing 4% of the total ADMS population (Table 1). Patients who died were older (70 [SD, 11.9] years old), had a longer ESKD duration (5.5 [SD, 4.4] years), and were disproportionately men (Table 1). Mortality was associated with age >65 years and longer ESKD duration, with a 10% increase for each additional year on dialysis (Table 2). The proportion of deaths among hospitalized patients was not significantly different from that of patients who were not hospitalized (26.8% versus 28.9%, respectively; chi square =0.13; P=0.71), suggesting that at-home mortality occurred.
Although minorities were less likely to be hospitalized compared with non-Hispanic Whites (Table 2), the difference was not significant. Asians had the lowest hospitalization rate. This finding, in addition to the high proportion of deaths in nonhospitalized COVID-19–positive/symptomatic patients, suggests there may be disparities in seeking acute care. Alternatively, it may represent a higher risk of sudden death in ESKD3 related to COVID-19 infection.2 Exploring the relationship between race and other demographic factors and mortality among COVID-19–positive/symptomatic patients will be an important avenue of study.
Undocumented patients on dialysis had twice the odds of dying (Table 2). Immigrants, especially undocumented individuals, tend to have lower-paying jobs and thus often share households to make ends meet, which likely increased their exposure to SARS-CoV-2. Moreover, although undocumented patients on dialysis were younger (chi square =22.1; P<0.001), they also had longer duration of ESKD (Kruskal–Wallis test; P<0.01). When adding Social Security numbers to the multivariate model including ESKD duration and age, ESKD duration was no longer significant (adjusted OR, 1.06; 95% CI, 0.99 to 1.13; P=0.09). This indicates that Social Security number or immigration status and age were more significant risk factors of death than ESKD duration and that undocumented status in the COVID-19–positive/symptomatic patient population was associated with greater mortality, despite younger age. Queens is home to a large immigrant and undocumented population from diverse areas, ranging from Asia to South America.8 Being undocumented is associated with lower socioeconomic status and a lack of education and health insurance, reflecting social determinants of health associated with poorer health outcomes.6 These barriers, in addition to fear of discovery by authorities and loss of work, often compound health disparities for this population.9 It is possible that delayed acute care as well as disparities in chronic health care influenced mortality.
We did not find other demographic variables to be associated significantly with mortality but observed some trends. Among COVID-19–positive/symptomatic patients, Asians were disproportionately more likely to die and have lower hospitalization rates compared with non-Hispanic whites (Tables 1 and 2). Men were less likely than women to be hospitalized (OR, 0.72; 95% CI, 0.45 to 1.16) and more likely to die (OR, 1.29; 95% CI, 0.76 to 2.17) (Table 2).
Strengths of this analysis are real-time detection and disease risk mitigation. Our sample size is larger than those of previous studies and more diverse with respect to ethnicity, race, and socioeconomic status.1,2 We were also able to trace out-of-hospital deaths.
Limitations of the study include electronic medical record data being subject to inaccurate entry and unavailability of details about location and cause of death. In areas with population densities that differ from those of the areas we studied, findings and outcomes may vary. In addition, limited access to SARS-CoV-2 PCR diagnostic testing in New York City at the time of the study resulted in the authors’ decision to present results as COVID-19–positive/symptomatic patients on the basis of the high pretest probability of COVID-19. This raises the possibility of misclassification bias, and known limitations of SARS-CoV-2 PCR sensitivity also increased the possibility of false-negative findings.
ESKD duration is represented as total years since first dialysis treatment and does not account for nondialysis periods. Only a very small proportion of PUIs in our study used home dialysis, and results cannot be generalized to this population.
In the COVID-19 pandemic, person-to-person exposure in densely populated cities has been key in explaining the devastating effects.10 Patients on dialysis receiving outpatient hemodialysis must leave their home multiple times per week, regardless of stay-at-home orders. As a result, they face increased infection risk because of exposure to others, whether on mass transportation, through shared transportation rides, or in facility waiting rooms. Population density and related socioeconomic factors may be key to understanding disease transmission among this patient population.
Disclosures
G. Coritsidis is a salaried director of the Broadway dialysis unit, the data of which are included in the paper as one of the 13 units. G. Coritsidis reports personal fees from Atlantic Dialysis Management Services, LLC during the conduct of the study. All remaining authors have nothing to disclose.
Funding
None.
Supplementary Material
Acknowledgments
The authors acknowledge Mr. Harrison Cosentino (Department of Information Technology, Atlantic Dialysis Management Services, LLC) for his assistance in data collection.
Dr. Premila Bhat, Dr. George Coritsidis, and Mr. Steven Weiss conceptualized and designed the study; Dr. J. Ganesh Bhat and Mr. Steven Weiss were responsible for data acquisition; Dr. Maria del Pilar Fernandez was responsible for data analysis; Dr. J. Ganesh Bhat, Dr. Premila Bhat, Dr. George Coritsidis, Dr. Maria del Pilar Fernandez, and Mr. Steven Weiss were responsible for interpretation of data; Dr. Premila Bhat, Dr. George Coritsidis, Dr. Maria del Pilar Fernandez, and Mr. Steven Weiss were responsible for tables and the figure; and Dr. J. Ganesh Bhat, Dr. Premila Bhat, Dr. George Coritsidis, Dr. Maria del Pilar Fernandez, and Mr. Steven Weiss drafted and revised the paper and approved the final version of the manuscript.
Footnotes
Published online ahead of print. Publication date available at www.jasn.org.
Supplemental Material
This article contains the following supplemental material online at http://jasn.asnjournals.org/lookup/suppl/doi:10.1681/ASN.2020070932/-/DCSupplemental.
Supplemental Figure 1. Categorization of patients.
Supplemental Table 1. Nonadjusted odds of death, hospitalization, and ED visit of the PUI cohort by COVID-19 infection status.
Supplemental Table 2. Demographic characteristics of the PUI population.
Supplemental Table 3. Demographic characteristics of the total ESKD population.
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