Key Points
We studied the effect of coronavirus disease 2019 (COVID-19) on the 30-day postdischarge outcomes of patients with end-stage kidney disease who are on dialysis.
During the first postdischarge week, patients on dialysis who were hospitalized with COVID-19 were more likely to experience readmission and death.
After the first week, there was no marked difference in the risks of readmission and death between patients with COVID-19 and those without.
Keywords: dialysis, aftercare, COVID-19, patient discharge, SARS-CoV-2, United States
Visual Abstract
Abstract
Background
Recent investigations have shown that, on average, patients hospitalized with coronavirus disease 2019 (COVID-19) have a poorer postdischarge prognosis than those hospitalized without COVID-19, but this effect remains unclear among patients with end-stage kidney disease (ESKD) who are on dialysis.
Methods
Leveraging a national ESKD patient claims database administered by the US Centers for Medicare and Medicaid Services, we conducted a retrospective cohort study that characterized the effects of in-hospital COVID-19 on all-cause unplanned readmission and death within 30 days of discharge for patients on dialysis. Included in this study were 436,745 live acute-care hospital discharges of 222,154 Medicare beneficiaries on dialysis from 7871 Medicare-certified dialysis facilities between January 1 and October 31, 2020. Adjusting for patient demographics, clinical characteristics, and prevalent comorbidities, we fit facility-stratified Cox cause-specific hazard models with two interval-specific (1–7 and 8–30 days after hospital discharge) effects of in-hospital COVID-19 and effects of prehospitalization COVID-19.
Results
The hazard ratios due to in-hospital COVID-19 over the first 7 days after discharge were 95% CI, 1.53 to 1.65 for readmission and 95% CI, 1.38 to 1.70 for death, both with P<0.001. For the remaining 23 days, the hazard ratios were 95% CI, 0.89 to 0.96 and 95% CI, 0.86 to 1.07, with P<0.001 and P=0.50, respectively. Effects of prehospitalization COVID-19 were mostly nonsignificant.
Conclusions
In-hospital COVID-19 had an adverse effect on both postdischarge readmission and death over the first week. With the surviving patients having COVID-19 substantially selected from those hospitalized, in-hospital COVID-19 was associated with lower rates of readmission and death starting from the second week.
Introduction
Since late 2019, the outbreak of coronavirus disease 2019 (COVID-19), the disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has exerted a profound effect on hospitalization and postdischarge outcomes in the United States (1–3) and in other viral epicenters across the world (4–7). As the confirmed cases and associated hospitalizations of COVID-19 surged in the initial stage of the pandemic (8,9), US hospitals limited their outpatient capacity and elective procedures (1,10), leveraged telemedicine for nonurgent visits (11,12), and reallocated medical resources toward treating patients with COVID-19 in response to government mitigation orders (13,14). Restricted access to health services and the fear of contagion contributed to deferred hospital admissions and poorer outcomes after discharge for patients with chronic illness, including ESKD (15–18).
Due to immune dysfunction (19), elevated comorbidity burden (20), and frequent contact with health care providers, patients with ESKD who are on dialysis constitute a vulnerable group with higher risks of SARS-CoV-2 infection and COVID-19-associated hospitalization and death than the general population, according to several early reports from China and Europe (21–24). This evidence was further corroborated by investigations on patients with ESKD in the United States, with study samples mostly limited to regional hospital or dialysis center networks (25–29). The literature has been recently enriched with studies focusing on postdischarge readmission and death for hospitalized patients with COVID-19 from statewide or nationwide health care systems in the United States (2,3,30–32). However, the effect of COVID-19 on the postdischarge prognosis of patients with ESKD who are on dialysis, presumably significant given the associated complications (33,34), remains underexplored.
Using an extensive national ESKD patient claims database administered by the US Centers for Medicare and Medicaid Services (CMS), the objective of this study was to characterize the effect of COVID-19 on postdischarge readmission and death among Medicare beneficiaries on kidney dialysis. In particular, we sought to examine whether the COVID-19 effect varied with time after hospital discharge. The study grew out of a CMS-designated investigation of the influence of COVID-19 on dialysis facility profiling according to the standardized readmission ratio, a quality measure that has been used by CMS in various quality initiatives (35,36). In addition to informing discharge decision making for patients on dialysis who have COVID-19, the study suggests ways one could adjust for COVID-19 in devising quality measures.
Materials and Methods
Data Sources and Study Population
The data in this retrospective cohort study were derived from the CMS clinical and administrative database, primarily on the basis of the Renal Management Information System, CROWNWeb facility-reported clinical and administrative data (including Forms CMS-2728, CMS-2746, and CMS-2744, and patient-tracking data), the Medicare Enrollment Database, and Medicare claims data. Included in this study were 436,745 live acute-care hospital discharges of 222,154 Medicare beneficiaries on dialysis from 7871 Medicare-certified dialysis facilities between January 1 and October 31, 2020. Discharges from non–acute-care hospitals, discharges with in-hospital death, and discharges with discharge-day outcomes were excluded from the analysis, along with other administrative exclusions (Figure 1).
Figure 1.
Study population. About 5.1% of the 436,745 live hospital discharges from acute care hospitals were associated with in-hospital COVID-19. Discharges from non–acute-care hospitals included discharges from cancer, rehabilitation, psychiatric, or long-term care hospitals. Administrative exclusions included discharges against medical advice, discharges associated with unknown dialysis facilities, discharges after >365 days of hospitalization, discharges after a patient’s 12th hospitalization within a year, and discharges of patients who were no longer actively on dialysis (e.g., discontinued dialysis, recovery, or loss to follow-up). Outcomes on discharge day included unplanned readmission, death, and planned readmission. COVID-19, coronavirus disease 2019.
Identification of COVID-19 Diagnosis
Information on in-hospital and prehospitalization COVID-19 diagnosis was identified from Medicare inpatient, outpatient, skilled nursing facility, home health agency, hospice, and physician/supplier claims (for Medicare Advantage patients only inpatient claims were available), along with ESKD medical evidence reports for Medicare entitlement and/or patient registration (Form CMS-2728). An in-hospital COVID-19 diagnosis was confirmed if the patient’s inpatient or physician/supplier claim associated with the inpatient stay had either of the two diagnosis codes of the International Classification of Diseases, Tenth Revision (ICD-10): B97.29 (since February 20, 2020) or U07.1 (from April 1, 2020 onward); a prehospitalization COVID-19 diagnosis was confirmed if the patient had any Medicare claim carrying the ICD-10 code B97.29 or U07.1 (3, 37).
Outcomes
Outcomes of primary interest were all-cause unplanned acute-care-hospital readmission and death within 30 days of hospital discharge. Unless otherwise stated, a readmission hereafter refers to an unplanned readmission to an acute-care hospital.
Baseline Characteristics
In addition to in-hospital and prehospitalization COVID-19 diagnoses, we also considered as baseline characteristics patient demographics and clinical characteristics, including age (≤24, 25–44, 45–59, 60–74, and ≥75), sex (female or male), race (Black, White, and other), body mass index (<18.5, 18.5–24.9, 25–29.9, ≥30 kg/m2), hospitalization status (planned versus unplanned), discharge status (discharged to home with self-care; home with medical care; a hospice; a skilled nursing facility; or other health care facility, including rehabilitation hospital, psychiatric hospital, nursing home, or any other long-term care hospital), Medicare Advantage enrollment status, ESKD vintage (<1, 1–2, 2–3, 3–6, >6 years), length of hospitalization (in quartiles), nursing home status, and diabetes as the cause of ESKD. Using ICD-10 diagnosis codes aggregated to comorbidity groups defined by the Agency for Healthcare Research and Quality Clinical Classifications Software (38), we collected data on 53 prevalent comorbidities using inpatient claims from 2019 and 2020.
Exploratory Data Analysis
We examined baseline characteristics of the 436,745 hospital discharges by in-hospital COVID-19 status (Table 1, Supplemental Table 1). To explore the outcomes, we first compared the variations across calendar time of postdischarge readmission and death between discharges with and without in-hospital COVID-19 (Figure 2). Thirty-day rates of readmission and death were calculated on a rolling basis from March 17 to October 15 of 2019 and 2020 (with 2019 as the reference group). To describe the distribution of postdischarge outcomes, we calculated the counts and proportions of unplanned readmissions, deaths, and planned readmissions across postdischarge intervals by in-hospital COVID-19 status (Table 2). In addition, we plotted the unadjusted hazard curves of readmission and death over the 30-day follow-up period, stratified by in-hospital COVID-19 status (Figure 3). On each postdischarge day, the unadjusted hazard of readmission (or death) was defined as the number of readmissions (or deaths) occurring over that day divided by the number of discharges at risk for readmission (or death) at the beginning of that day.
Table 1.
Baseline characteristics of discharges with or without in-hospital COVID-19
| Baseline Characteristic | n (%)a | P Valueb | Discharges with In-Hospital COVID-19, %c | |
|---|---|---|---|---|
| In-Hospital COVID-19 (N=22,149) | No In-Hospital COVID-19 (N=414,596) | |||
| Sex | ||||
| Male | 11,958 (54) | 220,361 (53) | 0.02 | 5 |
| Female | 10,191 (46) | 194,235 (47) | 5 | |
| Age, yr | ||||
| ≤24 | 67 (0.4) | 2313 (0.6) | <0.001 | 3 |
| 25–44 | 1711 (8) | 38,791 (9) | 4 | |
| 45–59 | 5238 (24) | 95,291 (23) | 5 | |
| 60–74 | 9832 (44) | 176,926 (43) | 5 | |
| ≥75 | 5301 (24) | 101,275 (24) | 5 | |
| Race | ||||
| White | 11,523 (52) | 250,553 (60) | <0.001 | 4 |
| Black | 9303 (42) | 140,053 (34) | 6 | |
| Other | 1323 (6) | 23,990 (6) | 5 | |
| Time since previous COVID-19 d | ||||
| No previous COVID-19 | 14,602 (66) | 401,173 (97) | <0.001 | 4 |
| 1–7 | 4844 (22) | 2357 (0.6) | 67 | |
| 8–14 | 1084 (5) | 1296 (0.3) | 46 | |
| 15–21 | 588 (3) | 1124 (0.3) | 34 | |
| 22–28 | 329 (2) | 902 (0.2) | 27 | |
| >28 | 702 (3) | 7744 (2) | 8 | |
| Planned hospitalization | 337 (2) | 40,170 (10) | <0.001 | 0.8 |
| Discharge destination | ||||
| Home with self-care | 9391 (42) | 224,302 (54) | <0.001 | 4 |
| Home with medical care | 4378 (20) | 102,330 (25) | 4 | |
| Hospice | 543 (2) | 6774 (2) | 7 | |
| Skilled nursing facility | 6961 (31) | 70,993 (17) | 9 | |
| Othere | 876 (4) | 10,197 (3) | 8 | |
| ESKD vintage, yr | ||||
| <1 | 3467 (16) | 84,562 (20) | <0.001 | 4 |
| 1–2 | 3048 (14) | 58,824 (14) | 5 | |
| 2–3 | 2748 (12) | 51,052 (12) | 5 | |
| 3–6 | 6151 (28) | 107,693 (26) | 5 | |
| >6 | 6735 (30) | 112,465 (27) | 6 | |
| Nursing home stay in 2019, d | ||||
| 0 | 14,139 (64) | 306,524 (74) | <0.001 | 4 |
| 1–89 | 3646 (17) | 73,621 (18) | 5 | |
| ≥90 | 4364 (20) | 34,451 (8) | 11 | |
| Length of hospitalization | ||||
| Quartile 1 | 2688 (12) | 99,235 (24) | <0.001 | 3 |
| Quartile 2 | 4720 (21) | 121,599 (29) | 4 | |
| Quartile 3 | 5675 (26) | 98,136 (24) | 6 | |
| Quartile 4 | 9066 (41) | 95,626 (23) | 9 | |
The summary of other baseline characteristics is available in Supplemental Table 1. COVID-19, coronavirus disease 2019.
Listed are counts (percentages in parentheses) of discharges with the specified characteristic from the groups with and without COVID-19.
Listed are P values from chi-squared tests.
Shown are the percentages of discharges with in-hospital COVID-19.
Refers to time since the most recent positive COVID-19 diagnosis before the corresponding hospitalization, with 0 day being no previous COVID-19.
Refers to a rehabilitation hospital, psychiatric hospital, nursing home, or any other long-term care hospital.
Figure 2.
Calendar variation of the unplanned readmission and death rates among discharges with and without in-hospital COVID-19 from March 17 to October 15, 2020. The monthly rate of readmission among discharges with COVID-19 was initially lower, but then became higher than the rate among discharges without COVID-19. The monthly rate of death among COVID-19 discharges remained higher than the rate among discharges without COVID-19. Monthly rates of readmission (or death) and their 95% CIs were calculated on a rolling basis. For comparison, rates and confidence intervals over the same period of 2019 were also presented.
Table 2.
Distribution of postdischarge outcomes with or without in-hospital COVID-19
| Outcome | n (%) | |||||
|---|---|---|---|---|---|---|
| Days after Discharge | Total | |||||
| 1–3 | 4–7 | 8–14 | 15–21 | 22–30 | ||
| In-hospital COVID-19 (N=22,149) | ||||||
| Unplanned readmission | 1731 (8) | 1631 (7) | 1551 (7) | 1140 (5) | 930 (4) | 6983 (32) |
| Death | 424 (2) | 261 (1) | 204 (0.9) | 116 (0.6) | 95 (0.4) | 1100 (5) |
| Planned readmission | 40 (0.2) | 40 (0.2) | 73 (0.3) | 67 (0.3) | 64 (0.3) | 284 (1) |
| Total | 2195 (10) | 1932 (9) | 1828 (8) | 1323 (6) | 1089 (5) | 8367 (38) |
| No in-hospital COVID-19 (N=414,596) | ||||||
| Unplanned readmission | 18,777 (5) | 23,667 (6) | 32,080 (8) | 23,745 (6) | 22,631 (6) | 120,900 (29) |
| Death | 4195 (1) | 2901 (0.7) | 3095 (0.7) | 2052 (0.5) | 1987 (0.5) | 14,230 (3) |
| Planned readmission | 1594 (0.4) | 2068 (0.5) | 2900 (0.7) | 2346 (0.6) | 2356 (0.6) | 11,264 (3) |
| Total | 24,566 (6) | 28,636 (7) | 38,075 (9) | 28,143 (7) | 26,974 (7) | 146,394 (35) |
Percentages (in parentheses) are with respect to the total number of discharges with or without in-hospital COVID-19. Within 30 days of discharge, 13,782 (62%) out of the 22,149 discharges with COVID-19 had no outcomes, whereas 268,202 (65%) out of the 414,596 discharges without COVID-19 had no outcomes. COVID-19, coronavirus disease 2019.
Figure 3.
Unadjusted cause-specific hazard curves of unplanned readmission and death from January 1 to October 31, 2020. The differences in the hazard of readmission and death between discharges with COVID-19 and those withoutwere substantial for the first 7 days, but shrank to non-significance afterwards. On each postdischarge day, the unadjusted hazard of readmission (or death) was defined as the number of readmissions (or deaths) occurring over that day divided by the number of discharges at risk for readmission (or death) at the beginning of that day. w/, with; w/o, without.
Cause-Specific Hazard Modeling
Postdischarge readmission and death can be treated as two distinct event types (i.e., competing risks) with observation continuing until their first occurrence or 30 days, whichever is first. In this case, a Cox relative risks model for cause-specific hazards can be used and allows separate estimation of hazard ratios (HRs) for both risks (39). Moreover, as a preliminary check on whether the effect of in-hospital COVID-19 was time dependent, we tested the proportional hazards assumption using a well-established software package in survival analysis (40). This test suggested the COVID-19 effects did not remain constant over time, as was also suggested by the hazard plot (Figure 3). To account for the temporal variation of COVID-19 effects on postdischarge readmission and death, we fitted stratified Cox cause-specific hazard models, each of which included two interval-specific (1–7 days and 8–30 days) relative risks due to in-hospital COVID-19 diagnosis. In the analysis, discharges were matched through dialysis facility stratification, and the COVID-19 effect was allowed to be time dependent for each competing risk. Where appropriate, the time to hospital admission from the most recent prehospitalization COVID-19 diagnosis was also included in the model, as were other baseline characteristics. HRs of readmission and death for baseline characteristics, 95% CIs, and associated P values were calculated (Table 3, Supplemental Table 2). We also fitted the Cox cause-specific hazard models for readmission and death to a more homogeneous subsample of only discharges to home (Supplemental Table 3). To examine the calendar variation of COVID-19 effect, we fitted the same models to the study population, except that calendar indicators and their interactions with in-hospital COVID-19 were also included (Supplemental Table 4).
Table 3.
Effects of baseline characteristics on unplanned readmission and death after discharge day
| Baseline Characteristic | Readmission | Death | ||
|---|---|---|---|---|
| Hazard Ratio (95% Confidence Interval) | P Value | Hazard Ratio (95% Confidence Interval) | P Value | |
| In-hospital COVID-19, d | ||||
| No in-hospital COVID-19 (reference) | — | — | — | — |
| Effect in 1–7 | 1.59 (1.53,1.65) | <0.001 | 1.53 (1.38,1.70) | <0.001 |
| Effect in 8–30 | 0.92 (0.89,0.96) | <0.001 | 0.96 (0.86,1.07) | 0.50 |
| Time since previous COVID-19a, d | ||||
| No previous COVID-19 (reference) | — | — | — | — |
| 1–7 | 0.98 (0.94 to 1.03) | 0.40 | 0.83 (0.73 to 0.94) | 0.004 |
| 8–14 | 0.91 (0.85 to 0.98) | 0.01 | 0.87 (0.71 to 1.07) | 0.20 |
| 15–21 | 0.91 (0.83 to 0.98) | 0.02 | 0.85 (0.66 to 1.10) | 0.20 |
| 22–28 | 0.97 (0.88 to 1.06) | 0.50 | 0.85 (0.64 to 1.13) | 0.30 |
| >28 | 0.99 (0.95 to 1.02) | 0.50 | 0.74 (0.65 to 0.85) | <0.001 |
| Sex | ||||
| Male (reference) | — | — | — | — |
| Female | 1.01 (1.00 to 1.02) | 0.05 | 0.84 (0.81 to 0.87) | <0.001 |
| Age, yr | ||||
| ≤24 | 1.45 (1.34 to 1.58) | <0.001 | 0.65 (0.35 to 1.19) | 0.20 |
| 25–44 | 1.18 (1.16 to 1.21) | <0.001 | 0.78 (0.70 to 0.88) | <0.001 |
| 45–59 (reference) | — | — | — | — |
| 60–74 | 0.98 (0.97 to 1.00) | 0.03 | 1.30 (1.23 to 1.38) | <0.001 |
| ≥75 | 0.99 (0.97 to 1.01) | 0.30 | 2.02 (1.90 to 2.16) | <0.001 |
| Race | ||||
| White (reference) | — | — | — | — |
| Black | 0.97 (0.96 to 0.99) | <0.001 | 0.82 (0.78 to 0.86) | <0.001 |
| Other | 0.99 (0.96 to 1.02) | 0.30 | 0.84 (0.77 to 0.93) | <0.001 |
| Planned hospitalization | 0.92 (0.90 to 0.94) | <0.001 | 0.74 (0.68 to 0.79) | <0.001 |
| Discharge destination | ||||
| Home with self-care (reference) | — | — | — | — |
| Home with medical care | 1.11 (1.09 to 1.13) | <0.001 | 1.42 (1.34 to 1.50) | <0.001 |
| Hospice | 0.75 (0.70 to 0.81) | <0.001 | 73.04 (68.65 to 77.70) | <0.001 |
| Skilled nursing facility | 1.18 (1.15 to 1.20) | <0.001 | 2.49 (2.34 to 2.64) | <0.001 |
| Otherb | 1.26 (1.22 to 1.31) | <0.001 | 2.95 (2.67 to 3.25) | <0.001 |
HRs, 95% CIs and P values for other baseline characteristics are available in Supplemental Table 2. HR, hazard ratio; COVID-19, coronavirus disease 2019.
Refers to time since the most recent positive COVID-19 diagnosis before the corresponding hospitalization.
Refers to a rehabilitation hospital, psychiatric hospital, nursing home, or any other long-term care hospital.
All analyses were conducted in SAS 9.4 (SAS Institute Inc., Cary, NC) and R version 3.6.3 (R Foundation for Statistical Computing, Vienna, Austria). Statistical significance was defined as P<0.05. This study was exempted from approval by the institutional review board at the University of Michigan.
Results
Baseline Characteristics
Of the 436,745 live hospital discharges between January 1 and October 31, 2020, 5% had an in-hospital COVID-19 diagnosis, whereas 95% did not (Table 1). The sex distribution was similar in the two groups, with slightly more men in the COVID-19 discharges. Age distributions were also similar in the two groups, although patients at least 45 years old were slightly more common in the COVID-19 group (92% versus 90%). Of discharges from Black patients, 6% had in-hospital COVID-19, compared with 4% of White patients. Among the 22,149 discharges with in-hospital COVID-19, 7547 (34%) had a COVID-19 diagnosis before the corresponding hospitalization; in comparison, of the 414,596 discharges without in-hospital COVID-19, 13,423 (3%) had a COVID-19 diagnosis before the hospitalization. As expected, only a few (337 or 2%) discharges with in-hospital COVID-19 resulted from a planned hospitalization, whereas 40,170 (10%) discharges with no in-hospital COVID-19 followed a planned hospitalization. Compared with discharges without an in-hospital COVID-19 diagnosis, discharges with in-hospital COVID-19 were more likely to involve patients with a longer ESKD vintage, having >90 days of nursing home stay, or longer hospital stay before discharge. Finally, discharges with in-hospital COVID-19 were less likely to be discharges to home with either self or medical care (P<0.001).
Calendar Variations of Readmission and Death
The rate of readmission for discharges with in-hospital COVID-19 was increasing and became significantly higher than the rate for discharges without in-hospital COVID-19 after May, 2020 (Figure 2). In addition, the readmission rate in the 2020 group without in-hospital COVID-19 was initially lower than the 2019 rate before May, and then tracked closely with the 2019 rate through October. The rate of death for discharges with in-hospital COVID-19 was decreasing and remained higher than the rate for discharges without in-hospital COVID-19. As expected, death rates of the 2020 groups were significantly higher than the 2019 death rate. The differences in readmission and death rates between the two 2020 groups were further examined in a Cox cause-specific hazard model (Supplemental Table 4).
Postdischarge Variations of Readmission and Death
When analyzing the 154,761 discharges with a 30-day outcome (unplanned readmission, death, or planned readmission) by in-hospital COVID-19 status and five postdischarge intervals, we observed, over the first 7 days, that the proportions for readmission and death were substantially higher in the COVID-19 group than those in the non–COVID-19 group (Table 2). After the first week, the non–COVID-19 cohort surpassed the COVID-19 cohort in readmission until the last day of follow-up, whereas the difference in the proportion of death between the two groups became less pronounced. This evidence suggests the effect of in-hospital COVID-19 on postdischarge outcomes varied with time since discharge.
To advance the analysis with a competing-risk approach, we plotted the unadjusted cause-specific hazard curves of readmission and death against days after discharge (Figure 3). The hazard curves for discharges with in-hospital COVID-19 were significantly higher than those for discharges without in-hospital COVID-19 within the first 7 days of discharge. After approximately the first week, the hazard difference between the COVID-19 and non–COVID-19 groups became less marked. In addition, the hazard curve of readmission for COVID-19 discharges mostly lay below the curve for non–COVID-19 discharges after the first week. These findings, along with the preliminary test of the proportional hazards assumption (P<0.001), further corroborated the time dependence of the postdischarge effect of in-hospital COVID-19.
Effects of COVID-19 Diagnosis
On the basis of the shape of the unadjusted cause-specific hazard curves, we introduced two interval-specific effects of in-hospital COVID-19 into the Cox cause-specific hazard models (Table 3). In-hospital COVID-19 was associated with a substantial increase in the rate of readmissions over the first 7 days of discharge, with an HR of 1.59 (95% CI, 1.53 to 1.65; P<0.001), but, after the first week, was associated with a slightly reduced risk, with an HR of 0.92 (95% CI, 0.89 to 0.96; P<0.001). Similar to readmission, COVID-19 led to an increased risk of death (HR, 1.53; 95% CI, 1.38 to 1.70; P<0.001) during the first week, but this risk was smaller and nonsignificant (HR, 0.96; 95% CI, 0.86 to 1.07; P=0.50) over the rest of the 30-day period. A sensitivity analysis using only discharges to home showed similar effects of in-hospital COVID-19 diagnosis (Supplemental Table 3). These effects changed only slightly in a supplementary analysis where discharges in January and February of 2020 were removed from the sample. When calendar indicators and their interactions with in-hospital COVID-19 were included in the model (Supplemental Table 4), in-hospital COVID-19 was associated with an increased risk of readmission and a decreased risk of death over time.
Different from in-hospital COVID-19 diagnosis, prehospitalization COVID-19 did not exert a strong nor consistent effect on postdischarge readmission. The five interval-specific HRs of prehospitalization COVID-19 fell between 0.91 and 1, and only two (8–14 days and 15–21 days since the most recent COVID-19 diagnosis) of the five effects were significant (P=0.01 and [95% CI, 0.85 to 0.98] P=0.02 [95% CI, 0.83 to 0.98], respectively). The five HRs for postdischarge death were consistently <0.88, with two effects being significantly different from one (HRs of 0.83 [95% CI, 0.73 to 0.94] and 0.74 [95% CI, 0.65 to 0.85] for 1–7 days and >28 days since the most recent COVID-19 diagnosis, with P=0.004 and P<0.001, respectively). Similarly, the sensitivity analysis using only home discharges did not support significant and consistent effects of prehospitalization COVID-19. Breaking down the interval-specific HRs of prehospitalization COVID-19 by in-hospital COVID-19 status (not shown here) did not yield significantly different HRs between discharge groups with and without in-hospital COVID-19.
Demographics, Discharge Status, and Planned Hospitalization
There was limited evidence of sex and racial differences in readmission, with the HRs very close to one. Discharges from patients <45 years were more likely to be followed by a 30-day readmission than those discharges from patients at least 45 years old. In contrast, discharges from patients aged at least 45 years were more likely to be followed by a 30-day death than discharges from patients <45 years. Discharges from women or non-White patients were associated with a lower risk of death than discharges from men or White patients (HRs around 0.83 with P<0.001). The sex and Black-White differences in the risk of readmission were not marked (HRs of 1.01 [95% CI, 1.00 to 1.02] and 0.97 [95% CI, 0.96 to 0.99], respectively), although the HRs were significantly different from one (P=0.05 and P<0.001, respectively). The sensitivity analysis with only home discharges yielded similar results for demographic risk factors (Supplemental Table 3). Using home discharge with self-care as the reference, we observed that discharges to hospice were associated with a substantially increased risk of death but a decreased risk of readmission, compared with discharges to home with self-care. As expected, a planned hospitalization was associated with lower risks of readmission and death after discharge (HRs of 0.92 [95% CI, 0.90 to 0.94] and 0.74 [95% CI, 0.68 to 0.79], respectively, with both P<0.001) than an unplanned hospitalization.
Discussion
Compared with the stable readmission rate in 2019, the lower readmission rates in the 2020 discharge groups before May are in accordance with the shock of the pandemic to the US health care system, and possibly reflect the fear of contagion among patients on dialysis and their caregivers (Figure 2). The substantial difference starting from early June 2020 in the rate of readmission between discharges with and without in-hospital COVID-19, together with the elevated death rate in the 2020 group with in-hospital COVID-19, suggests that patients on dialysis who had in-hospital COVID-19 were associated with higher risks of postdischarge readmission and death than their counterparts without in-hospital COVID-19. In addition, the significantly higher death rate in the 2020 group without in-hospital COVID-19 compared with the 2019 group implies that patients on dialysis had worsened postdischarge survival, perhaps due to reduced medical service capacity and/or deferred care for non–COVID-19 conditions.
The temporal variation of the in-hospital COVID-19 effect on postdischarge readmission and death suggests that a COVID-19 diagnosis during hospitalization initially had a strong adverse influence on postdischarge readmission and survival, but this effect shrank into insignificance after the first week. In-hospital mortality and the high initial postdischarge mortality in the discharge group with in-hospital COVID-19 may have resulted in those patients with in-hospital COVID-19 surviving the first week being somewhat more robust than their counterparts with no in-hospital COVID-19, which led to reduced rates of readmission and death after the first week. However, the net effect of in-hospital COVID-19 over the entire 30-day period is still adverse with higher risks of readmission and death. Similarly, in a previous study using <1500 patients hospitalized with COVID-19 and matched cohorts with pneumonia and heart failure from 132 hospitals of the US Veterans Affairs health care system, the HRs of COVID-19 infection for postdischarge readmission were estimated to be (95% CI, 1.09 to 1.87) and (95% CI, 1.31 to 2.01) for the first 10 days, and (95% CI, 0.36 to 0.74) and (95% CI, 0.41 to 0.74) for the next 10 days (4). Although this study considered a limited sample from the veteran population, the decreasing pattern of HRs is concordant with what we observed from patients with ESKD who are on dialysis.
The 30-day hospital readmission rate has been recognized as an indicator of interprovider care coordination, medical cost-effectiveness, and quality of life for patients on dialysis (41–44). In the midst of the COVID-19 pandemic, the need to study postdischarge readmission and death among patients on dialysis has been even greater. As a group of patients who continually receive treatments at dialysis facilities, patients with ESKD who are on dialysis have encountered an elevated risk of SARS-CoV-2 infection, contributing to overwhelmed inpatient and emergency departments amid a public health emergency. Thus, it has been crucial to take measures to combat the spread of SARS-CoV-2 in dialysis facilities where physical distancing is difficult to practice (45). On the other hand, early reports in areas with high COVID-19 incidence indicated that a nontrivial number of patients without ESKD had AKI and required inpatient dialysis at hospital due to COVID-19 (46, 47). It is possible that this depletion of hospital resources in some cases might have led to early discharges for some patients with ESKD who were on dialysis before they were sufficiently clinically stable, and the strain on health care providers might have impeded typical postdischarge care coordination processes between the hospital and dialysis facility. Our findings will help inform discharge decision making for patients on dialysis who have COVID-19.
In terms of the analytic approach, we treated readmission and death as competing risks and used a stratified Cox cause-specific hazard model with time-varying effects of in-hospital COVID-19, in light of the course of recovery from SARS-CoV-2 infection. Alternatively, the logistic regression model has been used by the CMS in profiling dialysis facilities on the basis of the standardized readmission ratio (35, 36). This approach simplifies the analysis by merely considering whether or not a readmission is observed within 4–30 days of discharge, regardless of the postdischarge time to that readmission. By doing so, only an average effect of a risk factor over the 4- to 30-day period can be characterized. In addition, readmissions and deaths within 3 days of discharge are excluded from the analysis because these readmissions are likely to occur before patients can be reconnected with their respective dialysis facilities. By contrast, this study took a comprehensive and refined analytic framework in that both the time to the occurrence of a readmission or death and the effect variation with time of an in-hospital COVID-19 diagnosis were considered within the entire 30-day period. Because our study was focused on the postdischarge outcomes of patients on dialysis rather than dialysis facility profiling, discharges with 3-day readmissions or deaths were incorporated into the analysis.
Our findings should be interpreted with the following limitations: First, it should be noted that our study population only consisted of live acute-care hospital discharges from January 1 to October 31, 2020. Given the constantly evolving situation of the pandemic, the results shown here are subject to change as treatment and vaccination are becoming more standardized and effective, new virus variants are spreading, and government regulators are adjusting pandemic-related public health mandates. Second, as suggested in early studies (48–50), asymptomatic SARS-CoV-2 infection has been prevalent due to limited sensitivity and accuracy of the diagnostic tests. The under-reporting of confirmed COVID-19 cases among Medicare beneficiaries on dialysis reduced the number of identified inpatients with COVID-19, which may change the observed effects of COVID-19. Third, discharges with in-hospital death accounted for 6% of the original 536,315 discharges. Compared with patients discharged alive, patients deceased in hospital were expected to be greatly affected by COVID-19. Therefore, excluding deceased discharges from the analysis resulted in a less representative sample of patients with milder health conditions. This, in turn, may lead to the discharges from patients with in-hospital COVID-19 diagnosis being more comparable with those discharges without in-hospital COVID-19. Lastly, for patients enrolled in Medicare Advantage, their COVID-19 diagnosis information was only available from inpatient claims. To account for this limitation, we applied the Cox competing risk model to discharges only from Medicare fee-for-service patients without Medicare Advantage (Supplemental Table 5). The effects of risk factors are similar to those including both patients with and without Medicare Advantage (Table 3, Supplemental Table 2).
In conclusion, COVID-19 during hospitalization had an adverse effect on postdischarge readmission and death over the first 7 days of discharge. With the surviving patients having COVID-19 substantially selected from patients hospitalized with COVID-19, the effects of in-hospital COVID-19 became slightly nonadverse after the first week. These results will help inform discharge decision making for patients on dialysis who have COVID-19 and encourage greater attention to coordinated care after discharge. The analytic approach will also be useful for risk adjustment in quality measure development.
Disclosures
X. Ding reports receiving research funding from Bayer HealthCare Pharmaceutical Inc. J. Du reports having ownership interest in Blue Cat Blue Cat LLC. G.W. Gremel reports having ownership interest in CVS. R.A. Hirth reports serving in an advisory or leadership role for the American Journal of Managed Care (as deputy editor of medical care and on the editorial board) and Association of University Programs in Health Administration (on the board of directors). J.D. Kalbfleisch reports serving on the editorial board of Lifetime Data Analysis. J.H. Segal reports serving in an advisory or leadership role for the ESRD Network 11 Medical Review/Executive Committees. All remaining authors have nothing to disclose.
Funding
This study was supported by the CMS, contract numbers 75FCMC18D0041 and 500-2016-00085C.
Acknowledgments
The statements contained in this article are solely those of the authors and do not necessarily reflect the views or policies of the CMS. The authors assume responsibility for the accuracy and completeness of the information contained.
Author Contributions
L. Borowicz was responsible for resources; C. Dahlerus, G.W. Gremel, K. He, R.A. Hirth, J.D. Kalbfleisch, J. Kang, J.M. Messana, J.H. Segal, A. Sen, and W. Wu were responsible for methodology and reviewed and edited the manuscript; C. Dahlerus, K. He, J.D. Kalbfleisch, J.M. Messana, and J.H. Segal were responsible for funding acquisition; X. Ding, A. Eckard, G.W. Gremel, M. Slowey, X. Wang, and W. Wu were responsible for formal analysis and visualization; J. Du was responsible for data curation; J. Du, G.W. Gremel, and H. Gu were responsible for software; B. Frye, H. Gu, T. Nahra, R. Padilla, L. Tong, and K. Wisniewski were responsible for investigation; K. He, J.D. Kalbfleisch, and J.M. Messana conceptualized the study; K. He, J.D. Kalbfleisch, and W. Wu wrote the original draft; and J.H. Segal provided supervision.
Data Sharing Statement
Data cannot be shared to a third-party repository, as required by the CMS.
Supplemental Material
This article contains supplemental material online at https://kidney360.asnjournals.org/lookup/suppl/doi:10.34067/KID.0000242022/-/DCSupplemental.
Baseline characteristics of discharges with or without in-hospital COVID-19 (continued from Table 1). Download Supplemental Table 1, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day (continued from Table 3). Download Supplemental Table 2, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day using home discharges only. Download Supplemental Table 3, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day with calendar effects. Download Supplemental Table 4, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day using Medicare fee-for-service patients only. Download Supplemental Table 5, PDF file, 229 KB (228.9KB, pdf)
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Baseline characteristics of discharges with or without in-hospital COVID-19 (continued from Table 1). Download Supplemental Table 1, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day (continued from Table 3). Download Supplemental Table 2, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day using home discharges only. Download Supplemental Table 3, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day with calendar effects. Download Supplemental Table 4, PDF file, 229 KB (228.9KB, pdf)
Effects of baseline characteristics on unplanned readmission and death after discharge day using Medicare fee-for-service patients only. Download Supplemental Table 5, PDF file, 229 KB (228.9KB, pdf)