Palliative care for patients with chronic kidney disease and severe COVID-19 in Brazil: a retrospective study in a quaternary hospital
Tulio L. Correa1,2
, Mariana Sandoval Terra Campos Guelli1, Ricardo Tavares de Carvalho1
Contributions: (I) Conception and design: TL Correa, RT Carvalho; (II) Administrative support: RT Carvalho; (III) Provision of study materials or patients: RT Carvalho; (IV) Collection and assembly of data: All authors; (V) Data analysis and interpretation: All authors; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.
Background: Patients with chronic kidney disease (CKD) have many special needs in the areas of symptom management, advanced care planning, and end-of-life care. We aimed to evaluate the palliative care (PC) provided to patients with CKD admitted with severe coronavirus disease 2019 (COVID-19) at the Clinics Hospital of the University of Sao Paulo Faculty of Medicine during the first wave of the pandemic.
Methods: A retrospective observational study was conducted in a quaternary hospital. Patients assisted by the PC team with CKD in 2020 were selected according to a protocol for identifying patient at an elevated risk of death who require PC support. The clinical and demographic characteristics, as well as the outcomes, were assessed using electronic records.
Results: A total of 217 patients with CKD were included in the study, of whom 44.2% were admitted to the intensive care unit (ICU). Patients with CKD had an increased relative risk (RR) of death [1.31, 95% confidence interval (CI): 1.12–1.53] but were not assisted by the PC team to a higher degree. Eighty patients with CKD (83.3%) died without being assisted by the PC team. Dialysis treatment and CKD grades were not significantly associated with PC assistance.
Conclusions: Although patients with CKD experienced higher mortality rates, they did not receive PC at a significantly greater frequency and many died without receiving adequate end-of-life care during the COVID-19 pandemic in Brazil.
Keywords: Coronavirus disease 2019 (COVID-19); chronic kidney disease (CKD); nephrology; palliative care (PC); pandemic
Submitted Jul 02, 2024. Accepted for publication Nov 22, 2024. Published online Jan 20, 2025.
doi: 10.21037/apm-24-99
Highlight box
Key findings
• Patients with chronic kidney disease (CKD) had an increased relative risk of death than patients without CKD.
• In our study, patients with CKD were not assisted by the palliative care (PC) team to a higher degree.
• Eighty patients (83.3%) died without being assisted by the PC team.
• Dialysis and CKD grades were not significantly associated with PC assistance.
What is known and what is new?
• Patients with CKD have many special needs in the areas of symptom management, advanced care planning and end-of-life care.
• Our study reported a very low utilization of PC for patients with CKD during the coronavirus disease 2019 (COVID-19) pandemic, although they have worse outcomes.
What is the implication, and what should change now?
• It is crucial to raise attention to this matter due to the importance of PC for patients with CKD, especially for those with higher disease grades. This should be even more crucial during emergency situations, including pandemics.
Introduction
Individuals with chronic illnesses face a heightened risk of severe symptoms and increased mortality associated with coronavirus disease 2019 (COVID-19) (1). It is estimated that around 11% of the Brazilian population has chronic kidney disease (CKD) (2). CKD not only elevates the susceptibility to COVID-19 infection but also heightens the likelihood of progressing to critical disease and death (3). Research indicates that COVID-19 can directly invade kidney cells, causing cell injury and fibrosis (4). Considering the impact of COVID-19 on the kidneys, it is imperative to provide special attention and care to patients with CKD during the pandemic, given their heightened risk of adverse outcomes and the potential neglect of their health needs (5).
In the midst of a pandemic, addressing suffering and aiding in complex decision-making are not just integral aspects of crisis response but also fundamental elements of palliative care (PC) (6). Effective PC involves managing symptoms and prioritizing the psychological, social, and spiritual well-being of patients (7). In humanitarian crises like the COVID-19 pandemic, delivering adequate end-of-life care can be exceptionally challenging (8). Disparities in accessing PC are particularly pronounced in low- and middle-income countries, including Brazil (9). Most of the PC services in the country are located in state capitals and are mainly composed of hospital-level physicians with private funding (10).
Patients with CKD have many special needs in the areas of symptom management, advanced care planning and end-of-life care but are less likely to receive adequate PC than patients with other terminal illness (11). Therefore, this study aimed to describe the PC provided to patients with CKD admitted with COVID-19 to the Clinics Hospital of the University of Sao Paulo Faculty of Medicine during the first wave of the pandemic. We present this article in accordance with the STROBE reporting checklist (available at https://apm.amegroups.com/article/view/10.21037/apm-24-99/rc).
Methods
A retrospective observational study was carried out at the Clinics Hospital of the University of Sao Paulo Faculty of Medicine (HCFMUSP) (12). The HCFMUSP is a prominent quaternary hospital center made up of various health institutes. During the pandemic, the Central Institute of HCFMUSP admitted COVID-19 patients from other institutes. As a quaternary hospital, the criteria for a COVID-19 patient to be transferred to the HCFMUSP was to be a severe case needing advanced care not able to be provided in primary or secondary medical facilities.
The study focused on adults who were hospitalized with a confirmed COVID-19 diagnosis through reverse transcription polymerase chain reaction (RT-PCR) from March to November 2020. Previous comorbidities and CKD diagnosis were verified using electronic medical records and the respective International Classification of Diseases-11 (ICD) code (13). The demographic (age, sex, and place of admission) and clinical (comorbidities, CKD staging, PC screening, PC assistance, and PC unit admission) variables, as well as the outcome (death) were evaluated using electronic medical records.
PC screening
In response to the COVID-19 pandemic, the PC team at HCFMUSP developed a series of actions including a PC protocol (PALI-COVID) for identifying patients at an elevated risk of death who require PC support (14,15).
Individuals were evaluated for PC requirements using The Supportive and Palliative Care Indicators Tool (SPICT-BR) to identify those with a terminal condition and general indicators of poor or deteriorating health (16). This tool includes both general signs of deterioration and specific clinical indicators associated with life-limiting conditions (16). A clinical prediction model was also incorporated to identify those with a higher risk of death: chronic obstructive pulmonary disease (COPD) ≥ three decompensations in 6 months; heart failure with use of inotropic medications or ≥ three decompensations in 6 months; dementia with Clinical Dementia Rating of 3 and/or frequent infections/hospitalizations; metastatic cancer with Karnofsky Performance Status (KPS) Scale ≤40%; cerebrovascular accident sequela and degenerative syndromes with low functionality and/or frequent hospitalizations (15).
Subsequently, patients were categorized into three groups: red group (RG), yellow group (YG), and green group (GG). Patients in the RG did not meet the SPICT or the high risk of death criteria. Patients in the YG met the SPICT criteria but did not meet the high risk of death criteria. For the YG, activating the PC team was left to the medical team’s discretion and was recommended to assist with symptom management, communication challenges, and/or conflicts in decision-making. Patients in the GG met both the SPICT and the high risk of death criteria, and palliative care unit (PCU) referral was indicated. In all groups, a PC consultation team maintained daily communication with other medical teams upon request.
CKD grading
As for the 2012 Kidney Disease: Improving Global Outcomes (KDIGO) classification, CKD is defined as a glomerular filtration rate (GFR) less than 60 mL/min/1.73 m2 or persistent evidence of kidney damage on imaging, biopsy, or urinalysis for longer than 3 months (17).
Estimated glomerular filtration rate (eGFR) has been calculated through the Chronic Kidney Disease Epidemiology Collaboration (CKD-EPI) formula using age, sex, and serum creatinine measured at the time of hospital admission (17). Patients’ medical records were also used to assess current dialysis treatment. Based on the calculated eGFR in mL/min per 1.73 m2, patients were allocated into six groups according to the 2012 KDIGO CKD classification (18):
G1: GFR 90 and above;
G2: GFR 60 to 89;
G3a: GFR 45 to 59;
G3b: GFR 30 to 44;
G4: GFR 15 to 29;
G5: GFR less than 15 or dialysis.
Statistical analyses
Data were projected on an Excel 16.0 spreadsheet and statistical analyses involving the associations of presence of CKD, PC assistance, and CKD grades with categorical variables of interest (such as gender, age group, admission, comorbidities, SPICT criteria, Risk of death, and PALI-COVID group) were performed using Chi-squared test. To estimate the relative risk (RR) of death, the Log-binomial regression model was used. Stata 15 statistical software was used for the statistical analyses, considering a significance level of 5%.
Ethical approval
All methods were conducted under the ethical standards of the Declaration of Helsinki (as revised in 2013). The study was approved by the Research Ethics Committee of the Clinics Hospital, Faculty of Medicine, University of Sao Paulo (CEP/HCFMUSP) under number 31385420.6.0000.0068. This study is a retrospective study based on chart review, and it is exempt from informed consent.
Results
A total of 3,480 patients were included in the study, of which 217 (6.2%) had CKD. The median age was 61 years old; most patients with CKD were males (60.4%) and were admitted to an intensive care unit (ICU) (44.2%) (Table 1). Despite having increased RR of death [1.31, 95% confidence interval (CI): 1.12–1.53], patients with CKD were not assisted by the PC team to a higher degree (P=0.73). Of the 96 (44.2%) patients with CKD who died, 80 (83.3%) were not assisted by the PC team.
Table 1
| Characteristics | CKD | Total (n=3,480) | P value | |
|---|---|---|---|---|
| No (n=3,263) | Yes (n=217) | |||
| Gender | 0.16* | |||
| Female | 1,451 (44.5) | 86 (39.6) | 1,537 (44.2) | |
| Male | 1,812 (55.5) | 131 (60.4) | 1,943 (55.8) | |
| Median age (years) [IQR] | 61 [48–71] | 61 [47–71] | 61 [48–71] | |
| Age (years) | 0.47* | |||
| <20 | 47 (1.4) | 4 (1.8) | 51 (1.5) | |
| 20–59 | 1,463 (44.8) | 107 (49.3) | 1,570 (45.1) | |
| 60–79 | 1,423 (43.6) | 90 (41.5) | 1,513 (43.5) | |
| 80–89 | 281 (8.6) | 15 (6.9) | 296 (8.5) | |
| ≥90 | 49 (1.5) | 1 (0.5) | 50 (1.4) | |
| Elderly (≥60 years) (yes) | 1,753 (53.7) | 106 (48.8) | 1,859 (53.4) | 0.16* |
| Admission | 0.30* | |||
| Wards | 846 (25.9) | 51 (23.5) | 897 (25.8) | |
| Emergency | 895 (27.4) | 70 (32.3) | 965 (27.7) | |
| ICU | 1,522 (46.6) | 96 (44.2) | 1,618 (46.5) | |
| Comorbidities (yes) | ||||
| Hypertension | 1,592 (48.8) | 128 (59.0) | 1,720 (49.4) | <0.001* |
| Diabetes mellitus | 1,029 (31.5) | 81 (37.3) | 1,110 (31.9) | 0.08* |
| Dyslipidemia | 640 (19.6) | 34 (15.7) | 674 (19.4) | 0.15* |
| SPICT criteria (yes) | 857 (26.3) | 88 (40.6) | 945 (27.2) | <0.001* |
| Risk of death (yes) | 317 (9.7) | 32 (14.7) | 349 (10.0) | 0.02* |
| PALI-COVID group, n | 2,815 | 217 | 3,032 | <0.001* |
| Red | 1,987 (70.6) | 128 (59.0) | 2,115 (69.8) | |
| Yellow | 571 (20.3) | 65 (30.0) | 636 (21.0) | |
| Green | 257 (9.1) | 24 (11.0) | 281 (9.2) | |
| Assisted by the PC team (yes) | 278 (8.5) | 17 (7.8) | 295 (8.5) | 0.73* |
| PC unit (yes) | 129 (4.0) | 5 (2.3) | 134 (3.9) | 0.22* |
| Death (yes) | 1,106 (33.9) | 96 (44.2) | 1,202 (34.5) | |
| Relative risk of death (95% CI) | 1 | 1.31 (1.12–1.53) | – | <0.001** |
Data are presented as n (%) unless otherwise specified. This table was reused/adapted from an Open Access article (19) under the terms of the Creative Commons Attribution License 4.0 (CCBY). *, Chi-squared test; **, Log-binomial regression. HCFMUSP, Clinics Hospital, Faculty of Medicine, University of Sao Paulo; COVID-19, coronavirus disease 2019; CKD, chronic kidney disease; IQR, interquartile range; ICU, intensive care unit; SPICT, Supportive and Palliative Care Indicators Tool; PALI-COVID, palliative care in COVID-19 protocol; PC, palliative care; CI, confidence interval.
Table 2 compares the characteristics of patients with CKD who were assisted by the PC team to those who were not. The patients assisted by the PC team had increased RR of death [2.35 (95% CI: 1.91–2.89)]. Dialysis treatment and CKD grades were not significantly associated with PC assistance. Of the 17 (7.8%) patients assisted by the PC team, only 5 were admitted to the PCU.
Table 2
| Characteristics | Assisted by the PC team | P value | |
|---|---|---|---|
| No (n=200) | Yes (n=17) | ||
| Gender | 0.89* | ||
| Female | 79 (39.5) | 7 (41.2) | |
| Male | 121 (60.5) | 10 (58.8) | |
| Median age (years) [IQR] | 61 [47–71] | 61 [47–71] | |
| Elderly (≥60 years) (yes) | 92 (46.0) | 13 (76.5) | 0.001* |
| Admission | 0.96* | ||
| Wards | 47 (23.5) | 4 (23.5) | |
| Emergency | 65 (32.5) | 5 (29.4) | |
| ICU | 88 (44.0) | 8 (47.1) | |
| Comorbidities (yes) | |||
| Hypertension | 119 (59.5) | 9 (52.9) | 0.59* |
| Diabetes mellitus | 73 (36.5) | 8 (47.1) | 0.39* |
| Dyslipidemia | 31 (15.5) | 3 (17.6) | 0.82* |
| CKD stages | 0.41* | ||
| 1–3b | 40 (20.0) | 2 (11.8) | |
| 4–5 | 160 (80.0) | 15 (88.2) | |
| SPICT criteria (yes) | 74 (37.0) | 14 (82.4) | <0.001* |
| Risk of death (yes) | 22 (11.0) | 10 (58.8) | <0.001* |
| PALI-COVID group | <0.001* | ||
| Red | 127 (63.5) | 1 (5.9) | |
| Yellow | 60 (30.0) | 5 (29.4) | |
| Green | 13 (6.5) | 11 (64.7) | |
| Dialysis (yes) | 138 (69.0) | 8 (47.1) | 0.062* |
| Death (yes) | 80 (40.0) | 16 (94.1) | |
| Relative risk of death (95% CI) | 1 | 2.35 (1.91–2.89) | <0.001** |
Data are presented as n (%) unless otherwise specified. *, Chi-square test; **, Log-binomial regression. CKD, chronic kidney disease; HCFMUSP, Clinics Hospital, Faculty of Medicine, University of Sao Paulo; COVID-19, coronavirus disease 2019; PC, palliative care; ICU, intensive care unit; SPICT, Supportive and Palliative Care Indicators Tool; PALI-COVID, palliative care in COVID-19 protocol; CI, confidence interval.
Table 3 compares the clinical characteristics and outcomes of patients based on their CKD grades. Patients with CKD grades 4 and 5 met SPICT criteria and were admitted to the ICU significantly more than patients with lower CKD grades (P<0.001). Although patients with higher CKD grade had increased RR of death, they were not assisted by the PC team to a higher degree (P=0.41).
Table 3
| Characteristics | CKD stage | P value | |
|---|---|---|---|
| 1–3b (n=42) | 4–5 (n=175) | ||
| Gender | 0.82* | ||
| Female | 16 (38.1) | 70 (40.0) | |
| Male | 26 (61.9) | 105 (60.0) | |
| Elderly (≥60 years) (yes) | 21 (50.0) | 80 (45.7) | 0.62* |
| Admission | <0.001* | ||
| Wards | 15 (35.7) | 36 (20.6) | |
| Emergency | 17 (40.5) | 53 (30.3) | |
| ICU | 10 (23.8) | 86 (49.1) | |
| Comorbidities (yes) | |||
| Hypertension | 25 (59.5) | 103 (58.9) | 0.94* |
| Diabetes mellitus | 13 (31.0) | 68 (38.9) | 0.34* |
| Dyslipidemia | 5 (11.9) | 29 (16.6) | 0.45* |
| SPICT criteria (yes) | 10 (23.8) | 78 (44.6) | 0.001* |
| Risk of death (yes) | 4 (9.5) | 28 (16.0) | 0.29* |
| PALI-COVID group | 0.041* | ||
| Red | 32 (76.2) | 96 (54.9) | |
| Yellow | 7 (16.7) | 58 (33.1) | |
| Green | 3 (7.1) | 21 (12.0) | |
| PC assistance (yes) | 2 (4.8) | 15 (8.6) | 0.41* |
| PC consult (yes) | 1 (2.4) | 11 (6.3) | 0.32* |
| PC unit (yes) | 1 (2.4) | 4 (2.3) | 0.97* |
| Death (yes) | 9 (21.4) | 87 (49.7) | |
| Relative risk of death (95% CI) | 1 | 2.32 (1.28–4.22) | <0.001** |
*, Chi-squared test; **, Log-binomial regression. CKD, chronic kidney disease; HCFMUSP, Clinics Hospital, Faculty of Medicine, University of Sao Paulo; COVID-19, coronavirus disease 2019; ICU, intensive care unit; SPICT, Supportive and Palliative Care Indicators Tool; PALI-COVID, palliative care in COVID-19 protocol; PC, palliative care; CI, confidence interval.
Discussion
In our study, patients with CKD met the SPICT criteria significantly more and had increased RR of death than patients without CKD. Individuals with CKD grades 4 and 5 were also found to meet SPICT criteria and were notably more frequently admitted to the ICU compared to those in lower CKD grades. These findings align with existing literature that identifies heightened baseline serum creatinine as an independent risk factor for in-hospital death (3). The rationale behind this association may lie in the chronically compromised immune systems of individuals with CKD, wherein uremia can induce a persistent state of immune dysfunction characterized by ongoing low-grade inflammation and chronic immunosuppression (20). As shown in our results, the high prevalence of CKD is also concomitant with advanced age and other comorbidities such as hypertension and diabetes, which can play a role in the worse outcome among this population. Additionally, emerging evidence suggests the potential for COVID-19 renal tropism, leading to renal cell injury and subsequent fibrosis, thereby exacerbating the already impaired renal function in patients with CKD (4,20).
Although patients with CKD had higher RR of death, they were not assisted by the PC team in a higher degree. There are several challenges in providing adequate end-of-life care during the COVID-19 pandemic including the scarcity of resources, the shortage of professionals, and the mandatory physical isolation from family and friends (6,21). In addition, many healthcare providers associate PC with the interruption of life-prolonging treatments instead of end-of-life support in the course of a serious illness (22). This can make it even harder for physicians to address PC issues for patients with CKD, which are commonly already using many life-prolonging treatments, including dialysis or hemodialysis (23).
The patients assisted by the PC team met the SPICT criteria and were in the GG in higher proportions, which is in accordance with the PALI-COVID protocol created by our team (15). However, despite the creation of a PC protocol to support clinical practice, only 17 (7.8%) patients with CKD were assisted by the PC team, again confirming the low utilization of PC during the pandemic. Studies suggest that around 40% and 17% of general patients with COVID-19 received a PC consult in New York and Brazil, respectively (24,25). Although we did not find previous studies assessing the PC provided specifically to patients with CKD and COVID-19 to compare our results, it seems to be much lower than that of the general population. Indeed, despite an annual mortality rate exceeding 20%, dialysis patients are observed to be only half as likely to receive hospice services compared to other hospice diagnoses (26).
In addition, only 5 (2.3%) patients with CKD were admitted to the PCU, which can also be explained by the shortage of hospital beds and personnel (6). However, it is important to emphasize that PCUs are linked to higher patient satisfaction than consultative services for patients suffering from a complex illness (27). Also, the implementation of PCUs can be particularly interesting in the pandemic context, as patients cannot be easily transferred to hospice or home health due to quarantine precautions but still need end-of-life care.
Strengths and limitations
Our study exclusively focused on hospitalized patients, making it inappropriate to generalize findings to individuals who either recovered or passed away without being referred to a high-complexity center. Other limitations of our study include the use of creatinine at the time of admission for CKD staging. As discussed above, COVID-19 has extensive effects on the kidney, making it difficult to differentiate basal CKD grade from acute-on-CKD (4).
Nevertheless, it is noteworthy mentioning that our study introduces a novel description of the PC provided to patients with CKD and COVID-19 during the pandemic in Brazil. To our knowledge, this is the first study published on this specific topic. This study’s strengths encompass the highly specific sample and the minimal number of patients lost due to missing data. Therefore, it serves as a starting point for new studies assessing the PC offered to patients with CKD, including during emergencies.
The PALI-COVID protocol was used at our institution only during the pandemic outbreak. Although we have not tested its effectiveness outside the pandemic, it may be used by other centers to help identify patients who most need end-of-life support.
Conclusions
Patients with CKD met the SPICT criteria significantly more and had increased RR of death than patients without CKD. Among those patients, higher CKD grades were associated with poorer outcomes. However, patients with CKD were not assisted by the PC team to a higher degree and many died without receiving adequate end-of-life care. It is crucial to raise attention to this matter due to the importance of PC for patients with CKD, especially those with higher disease grades.
Acknowledgments
Funding: None.
Footnote
Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://apm.amegroups.com/article/view/10.21037/apm-24-99/rc
Data Sharing Statement: Available at https://apm.amegroups.com/article/view/10.21037/apm-24-99/dss
Peer Review File: Available at https://apm.amegroups.com/article/view/10.21037/apm-24-99/prf
Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://apm.amegroups.com/article/view/10.21037/apm-24-99/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The study was approved by the Research Ethics Committee of the Clinics Hospital, Faculty of Medicine, University of Sao Paulo (CEP/HCFMUSP) under number 31385420.6.0000.0068. This study is a retrospective study based on chart review, and it is exempt from informed consent.
Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.
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