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Introduction

Coronavirus disease 2019 (Covid-19), which caused a global pandemic of unprecedented proportions, is caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and characterised by severe acute respiratory syndrome. Since the onset of the pandemic in Wuhan, China, SARS-CoV-2 has infected more than 28 million individuals worldwide and killed more than 6 million individuals. It is mainly characterised by moderate-to-severe pneumonia associated with progressive endothelial damage and coagulopathy, but it can also involve other organs, including the kidneys. Evidence has suggested a higher incidence of severe SARS-CoV-2 among individuals with chronic conditions, including chronic kidney failure [1], and an association with acute kidney damage caused by direct effects on tubular cells and podocytes and the production of cytokines and hypoxemic tubular damage [2, 3].

Recent data have shown that patients with chronic kidney disease experience worse outcomes after SARS-CoV-2 infection that are related to multi-organ involvement, thrombotic events, and accentuation of the inflammatory response [4–6].

The average age of patients undergoing chronic dialysis treatment is 65 years, and they present with multiple comorbidities such as cardiovascular diseases, diabetes, obesity, and uraemia-induced immune alterations. All these factors significantly increase the risk of negative outcomes if patients are infected with SARS-CoV-2 [7–9]. Furthermore, they are at increased risk for hospitalisation in intensive care units and mortality rates more than 25% [10].

No studies have differentiated between the causes of mortality among patients on maintenance haemodialysis with positive SARS-CoV-2 nasopharyngeal swab test results; in particular, mortality can be distinguished as that attributable to either Covid-19 disease or other causes. Therefore, this study aimed to evaluate the causes of and risk factors for mortality among patients on chronic HD who are hospitalised with positive SARS-CoV-2 nasopharyngeal swab test results and investigate whether the cause of death was directly attributable to Covid-19 or other pathologies.

 

Materials and methods

The clinical data of patients on chronic haemodialysis treatment hospitalised because of SARS-CoV-2 infection at the Fondazione Policlinico Universitario Agostino Gemelli from 15 March 2020 to 28 February 2022 were analysed. Our data refer to the first wave of SARS-CoV-2 infection (wild-type virus) and the delta and omicron variants.

The study protocol was approved by the ethics committee of Fondazione Policlinico Universitario Agostino Gemelli on 21 April 2022 (prot. 001452/22). We analysed patient data from the electronic databases of medical records and hospital discharge records to determine the cause of mortality. Personal data, laboratory test results, types and modalities of renal replacement treatment, active comorbidities (type 2 diabetes mellitus, vascular disease, heart disease, tumours), and vaccination status of each patient were collected. Additionally, the Charlson comorbidity index (CCI) adjusted for age was calculated.

In Italy, in-hospital death attributable to Covid-19 has been identified with specific codes since the publication of Gazzetta Ufficiale on 28 October 2020 [11].

These codes are national hospital coding mandatorily reported upon patient discharge and used by national health system to identify causes of death for each patient. Furthermore, they are used for national statistics and reports.

The following mortality data codes were recorded in the hospital discharge forms of patients whose deaths were caused by Covid-19: Covid-19 pneumonia (480.41), Covid-19 acute respiratory distress syndrome, and Covid-19 respiratory failure (518.91).

All patients with Covid-19 were treated with bicarbonate haemodialysis and a Theranova 400 Baxter® filter. Bedside treatments were performed in the patient’s room using the Genius® Fresenius system. Each treatment lasted 180 to 210 min to reduce the exposure time to Covid-19 among healthcare personnel.

During our study, we considered all patients who received at least one dose of the SARS-CoV-2 vaccine to be vaccinated. Complementary mRNA (BNT162b2) was the first vaccine approved in Europe by the European Medicines Agency in December 2020. However, it has been available in Italy for long-term haemodialysis patients since February 2021.

Because all our patients were infected with SARS-CoV-2 during the first wave of the Covid-19 pandemic, we included patients in the vaccinated group if they were administered one dose of the vaccine.

 

Statistical analysis

Univariate and multivariate regression analyses of mortality risk factors, such as mean age, sex, number of haemodialysis sessions, hospitalisation (days), CCI, comorbidities (type 2 diabetes mellitus, vascular disease, heart disease, tumours), and diagnosis at the time of hospitalisation (Covid-19 pneumonia, asymptomatic SARS-CoV-2 infection, paucisymptomatic SARS-CoV-2 infection, Covid-19 respiratory failure, and radiological diagnosis of Covid-19 pneumonia) were performed.

The primary outcome was the in-hospital mortality rate. Numerical data were expressed as the mean and standard deviation (SD) for normally distributed variables; they were expressed as the median and interquartile range (IQR) for non-normally distributed data. The normality of the numerical variables was assessed using the Kolmogorov-Smirnov and Shapiro-Wilk tests. Categorical data are presented as numbers and percentages.

The differences between the numerical variables were assessed using Student’s t test (for normally distributed data) or the Mann-Whitney U test (for non-normally distributed data), as appropriate. Differences between qualitative variables were determined using the chi-squared test or Fisher’s exact test, as appropriate.

Logistic and multivariate regression analyses were performed to analyse the predictors of in-hospital mortality. The multivariate analysis was adjusted for factors significantly associated with the univariate analysis (p < 0.05) or trend (p < 0.1). Statistical significance was set at p < 0.05. All analyses were performed using IBM SPSS Statistics 25 software (IBM Corporation, Armonk, NY, USA).

 

Results

152 patients undergoing maintenance haemodialysis with positive SARS-CoV-2 test results were hospitalised during the study period. The demographic characteristics of the study population are shown in Table 1.

There were 100 male (65.8%) and 52 female (34.2%) patients with a mean age of 69 years (SD, 14.14). The mean CCI was 6.44 (SD, 2.64). The average hospitalisation length was 23.57 days (SD, 24.55 days). 52 (34.2%) patients had diabetes, 54 (35.5%) had vasculopathy, 64 (42.1%) had cardiopathy, 30 (19.7%) had neoplasms, 16 (10.5%) required admission to the intensive care unit (ICU). 42 (27.6%) patients died. Among these patients, based on the administrative coding, the main causes of death were SARS-CoV-2 infection for 22 (59%) patients and other pathologies for 20 (41%) patients (Table 2).

For all patients, ICU admission, dyspnoea, ICU admission, vasculopathy, cardiopathy, neoplasm, CCI, vaccination status, and radiological diagnosis of pneumonia were significant according to the chi-square test (p < 0.01).

According to Student’s t test, older patients and those with lower albumin levels were at higher risk for death. For those in the deceased patient group, the median age was 64.43 years (SD, 14.62 years) and the median albumin level was 25.19 (SD, 5.02) g/L.

According to the Mann–Whitney U test, the following variables had statistical significance: HD frequency (median, 5.50; IQR, 2.00-10.00; p < 0.001); CCI (median, 6.00; IQR, 5.00-8.00; p < 0.001); ICU length of stay (median, 0.00; IQR, 0.00-0.00; p < 0.001); white blood cell count (median, 7.02; IQR, 4.90-9.51; p < 0.001); C-reactive protein (median, 50.30; IQR, 15.05-141.45; p < 0.001); NT-proBNP (median, 16480.00; IQR, 3917.50-45738.25; p < 0.05); D-dimer (median, 1801.00; IQR, 952.75-3514.00; p < 0.05); activated partial thromboplastin time (median, 37.80; IQR, 34.38-43.40; p < 0.05); and IL-6 (median, 24.06; IQR, 10.73-55.33; p < 0.05).

For patients with SARS-CoV-2 who died, 74 (48.7%) had fever and 65 (42.8%) had dyspnoea; furthermore, 74 (48.7%) had a radiological diagnosis of pneumonia (Table 3).

We analysed the causes of death unrelated to SARS-CoV-2. Most of deaths were caused by severe sepsis (31.6%), followed by respiratory failure (23.5%) and pneumonia attributable to other pathogens (15.7%).

We divided the hospitalisations into two periods. The first period was approximately 11 months (March 2020 to February 2021) and characterised by infections attributable to the wild-type virus and the absence of vaccines. The second period was approximately 19 months (March 2021 to October 2022) and characterised by infections related to the delta and omicron variants and the availability of vaccines. Vaccination, even a single dose, conferred protection against mortality (Figure 1).

	Patients (152)
Middle age (mean ± SD)	69 ± 14.14
M/F	100/52
N° HD	1007
N° HD average/patients (mean ± SD)	7.66 ± 6.54
N° Hospitalized ward	152
N° Hospitalized Intensive Care Unite	18
Average days of hospitalization (mean ± SD)	23.57 ± 24.55
Charlson Comorbidity Index (mean ± SD)	6.44 ± 2.64
COMORBIDITY	N (%)
Diabetes Mellitus	52 (34.2%)
Vasculophaty	53 (34.9%)
Cardiophaty	64 (42.1%)
Cancer	30 (19.7%)
ADMISSION DIAGNOSIS	N (%)
COVID-19 pneumonia	59 (38.8%)
Symptomatic SARS-CoV2 infection	53 (34.9%)
Asymptomatic SARS-CoV2 infection	8 (5.3%)
SARS-CoV2 respiratory failure	3 (2%)
Radiological diagnosis of pneumonia	74 (48.7%)

Table 1. Characteristics of the study population.

Causes of death	N (%)
Respiratory failure by other causes	4 (23.5%)
Pneumonia by other pathogens	3 (15.7%)
GI perforation	1 (5.3%)
Severe sepsis	6 (31.6%)
Heart attack	1 (5.3%)
Thromboembolism	1 (5.3%)
Acute vascular failure	1 (5.3%)
Total deaths	17 (100%)

Table 2. Causes of death other than COVID-19.  Most deaths that were not related to COVID-19 were related to sepsis by other pathogens. GI, gastrointestinal.

Variable	Median [IQR8]	p value
HD1 frequency	5.50 [2.00-10.00]	<0.001*
CCI2	6.00 [5.00-8-00]	<0.001*
Length of stay (ICU3)	0.00 [0.00-0.00]	<0.001*
WBC4	7.02 [4.90-9.51]	<0.001*
CRP5	50.30 [15.05-141.45]	<0.001*
NT-proBNP	16480.00 [3917.50-45738.25]	0.037*
LDH6	227.00 [183.00-319.00]	<0.001*
D-dimer	1801.00 [952.75-3514.00]	<0.001*
aPTT7	37.80 [34.38-43.40]	0.049*
IL-6	24.06 [10.73-55.33]	0.022*

Table 3. Multivariate regression analysis of the mortality risk and variables with statistical significance according to the Mann-Whitney U test.
¹HD, haemodialysis; ²CCI, Charlson comorbidity index; ³ICU, intensive care unit; ⁴WBC, white blood cell; ⁵CRP, C-reactive protein; ⁶LDH, lactate dehydrogenase; ⁷aPTT, activated partial thromboplastin time; ⁸IQR, interquartile range.

 

Discussion

To our knowledge, no studies have investigated whether the cause of death is directly attributable to the virus or other causes among patients on maintenance haemodialysis with positive SARS-CoV-2 test results.

Our study tried to distinguish between deaths caused by Covid-19 and deaths that occurred with Covid-19. Our data showed that of the total number of deaths of patients with positive SARS-CoV-2 test results, 59% were directly caused by infection and 41% were attributable to other causes. Age, ICU admission, dyspnoea, ICU stay, vasculopathy, cardiopathy, neoplasm, vaccination status, and radiological diagnosis of pneumonia were risk factors for mortality. According to the European Renal Association registry, our study showed that the intrahospital all-cause mortality rate for patients with positive nasopharyngeal swab results was 21.9%; however, only 11.9% of these deaths were directly caused by Covid-19.

The mortality risk factors in our study were the same as those for the general population on dialysis, such as the coexistence of cardiovascular disease, advanced age, ICU admission, and CCI [12, 13].

Several studies have demonstrated that multiple markers and factors influence the risk of cardiac mortality and mortality for patients undergoing haemodialysis. Age, sex, diabetes mellitus, previous cardiovascular disease, and HD duration markedly increased the risk of mortality for these patients.

According to a study by Jager et al. [14], risk factors associated with Covid-19 mortality among patients on dialysis are age 75 years or older, male sex, and black race; furthermore, hypertension and cardiovascular disease were the most common comorbidities, followed by diabetes mellitus, previous kidney transplantation, and glomerular disease.

During the present study, vaccination was confirmed to be a protective factor. Only one dose effectively reduced the hospitalisation and mortality rates. The number of hospitalisations during different periods (wild-type virus and delta and omicron variants) remained constant despite the higher overall number of infected patients in the population with variants of the virus. This was attributable to the mass vaccination of the Italian population, with those at the highest risk being vaccinated first.

In Italy, of the 2,974,536 individuals infected during the first studied period, 101,346 died; furthermore, of the 20,850,660 individuals infected during the second studied period, 78,611 died [15].

The reported incidence of Covid-19 among individuals with chronic kidney disease is 66 per 10,000 affected individuals per week (estimated from 88 studies of 14,972 patients with chronic kidney disease and Covid-19 infection and 740,452 participants with Covid-19 and kidney disease), which is higher than the global incidence of 5 per 10,000 affected individuals per week.

Chronic kidney disease is a risk factor for developing a severe form of Covid-19, increased risk of mortality, and increased need for hospitalization [16, 17]. Furthermore, these risks increase as kidney disease worsens, reaching their maximum in patients on haemodialysis [18].

Patients undergoing haemodialysis are generally frail, immunodeficient, and at greater risk for infectious diseases. Additionally, the incidence of infection was higher among patients with chronic kidney disease undergoing renal replacement treatment, and it was related to worsening renal function [19].

During the pandemic, the prevalence of Covid-19 among dialysis patients was 0% to 37.6%. Furthermore, during the first outbreak of Covid-19, the mortality rate associated with SARS-CoV-2 was higher than that of most other viral infections. However, a death rate of 2.3% was reported in China, and the average death rate in Europe was 11.7% (range, 0.6%–18.9%). Among patients hospitalised for severe forms of Covid-19 in the United Kingdom, the mortality rate reached 26% [20, 21]. Mortality rates of patients with chronic kidney disease and Covid-19 were also higher than those of patients with chronic kidney disease without SARS-CoV-2 and those of the general population, as demonstrated by different studies conducted in China, Italy, the United States (New York and southern California), and the United Kingdom [22–28].

Our study results suggest that vaccination against SARS-CoV-2 for patients undergoing chronic haemodialysis is effective for preventing complications associated with SARS-CoV-2. As reported by Miao et al. [29], the incidences of death (11.1% vs. 3.8%) and hospitalisation (55.6% vs. 23.5%) were higher for unvaccinated patients than for vaccinated patients. These results were strengthened by the significantly greater incidence of hospitalisation among partially vaccinated patients (63.6% vs. 20.9%; p = 0.004) and patients who did not receive booster vaccines (32% vs. 16.4%; p = 0.04) compared to that among patients who were fully vaccinated and received booster vaccines. Moreover, the composite risk of death or hospitalisation was lower among vaccinated patients after adjusting for age, sex, and CCI (odds ratio, 0.24; 95% confidence interval, 0.15-0.40). However, according to other studies, patients who received a single dose of the vaccine experienced good results. Bernal et al. [30] reported that patients who received one dose of ChAdOx1-S had a 37% (3%-59%) reduced risk of emergency hospital admission. A single dose of either vaccine was 80% effective for preventing hospitalisation attributable to Covid-19, and a single dose of BNT162b2 was 85% effective for preventing death caused by Covid-19.

During the pandemic, the most complex challenges included the management and organisation of dialysis centres. Patients undergoing renal replacement treatment are more vulnerable to SARS-CoV-2; often, it is not possible to maintain physical distance because of the need to perform treatment in an overcrowded environment. Additionally, these patients frequently rely on social support and caregivers for assistance, daily activities, and medication management, resulting in possible opportunities for infection. Therefore, it is essential to ensure the constant support and monitoring of these patients through continuous screening, vaccination, and rapid hospitalisation when their nasopharyngeal molecular swab test results are positive.

However, despite attempts at good resource management in dialysis centres, the incidence rate of SARS-CoV-2 among patients with end-stage renal disease undergoing renal replacement treatment is significantly higher than that among patients with chronic disease receiving conservative treatment. This hypothesis is supported by the results of a study conducted in Italy and the United States [19] that found that the incidence rate of SARS-CoV-2 was similar for patients undergoing home haemodialysis and the general population (6 affected individuals per week vs. 2-6 affected individuals per week). We based our analysis on hospital discharge forms and the presence or absence of patients who died of causes other than SARS-CoV-2.

However, the long-term consequences of Covid-19 for patients undergoing dialysis remain poorly understood. Long Covid, which comprises the persistence of symptoms or the appearance of a new infection after 4 weeks, has been observed in both mildly and severely infected patients. The plethora of associated symptoms include fatigue, dyspnoea, heart involvement, muscle aches, headaches, joint pain, and neuropsychological disorders; however, because the majority of patients administered haemodialysis replacement treatment commonly present with these symptoms, it is difficult to assess the true correlation with long Covid [31].

Overall, the SARS-CoV-2 pandemic has brought the scientific community’s focus back to the importance of chronic renal failure as a systemic and non-district disease, associated with an increased risk of death from all causes.

 

Limitations

Our study is one of the few to investigate the primary cause of death of patients with positive nasopharyngeal swab test results during the haemodialysis regimen. However, this study had some limitations. First, it was a monocentric retrospective study. Consequently, it had a small sample size, but errors could be reduced because of methodological approaches. Furthermore, the population analysed was highly heterogeneous and difficult to standardise because of the heterogeneity of clinical presentations. Because of the small size of the study population, we were unable to statistically identify any differences in mortality risk factors of the group who died as a result of Covid-19 and those who died as a result of other causes with positive Covid-19 nasopharyngeal swab test results.

Another limitation could be the dialysis methodology. We analysed only bicarbonate haemodialysis, and there is some evidence that other methodologies associated with a convective flux such as hemodiafiltration or the adsorption properties of many dialysers can improve cytokine depuration implicated in the pathogenesis of Covid-19. However, there is no evidence that this technique improves disease outcomes. Furthermore, we utilised a particular type of dialyser, Theranova (manufactured by Baxter), which is a medium cutoff filter that is used in the HD mode and can generate an internal convective flux because of a very high amount of back-filtration that generates a high-pressure gradient. The combination of a moderately high internal convection volume and a higher sieving coefficient yielded better performance clearing middle molecules compared with standard HD.

 

Conclusions

Our study highlighted a mortality rate of 21.9% for patients with positive SARS-CoV-2 nasopharyngeal molecular swab test results, which was in line with the current data available in the literature. Of the total number of deaths of patients with positive SARS-CoV-2 test results, 59% were caused by the infection and 41% were attributable to other causes. The mortality risk factors were almost the same as those of the general dialysis population, such as the coexistence of cardiovascular disease, advanced age, and the need for ICU admission. Age, CCI, presence of peripheral vascular disease, and the need for ICU admission were independent risk factors for mortality. Vaccination has been confirmed to be a protective factor. Special care is necessary to prevent Covid-19 in patients on dialysis, hospitalisation, severe disease courses, and poor outcomes.

 

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