Clinical features of patients undergoing hemodialysis with COVID‐19

Abstract Hemodialysis patients are susceptible to coronavirus disease 2019 (COVID‐19). The aim of this study was to describe the epidemiological, clinical characteristics, and mortality‐related risk factors for those who undergoing hemodialysis with COVID‐19. We conducted a retrospective study. A total of 49 hemodialysis patients with COVID‐19 (Group 1) and 74 uninfected patients (Group 2) were included. For patients in Group 1, we found the median age was 62 years (36‐89 years), 59.3% were male, and the median dialysis vintage was 26 months. Twenty‐eight patients (57%) had three or more comorbidities and two patients (4%) died. The most common symptoms were fever (32.7%) and dry cough (46.9%), while nine patients (18.4%) were asymptomatic. Blood routine tests indicated lymphocytopenia, the proportion of lymphocyte subsets was generally reduced, and chest CT scans showed ground‐glass opacity (45.8%) and patchy shadowing (35.4%). However, these findings were not specific to hemodialysis patients with COVID‐19, and similar manifestations could be found in patients without SARS‐CoV‐2 infection. In conclusion, for hemodialysis patients with COVID‐19, lymphocytopenia and ground‐glass opacities or patchy opacities were common but not specific to them, early active treatment and interventions against nosocomial infection can significantly reduce the mortality and the risk of SARS‐CoV‐2 infection.

that herd infection may occur in the absence of appropriate prevention and control measures. Apart from strict travel restrictions and home quarantine, effective control measures are lacking. 7 Essentially, the treatment procedure and setting in the hemodialysis room is completely in contrast to the current isolation policy because the patients are supposed to be relatively crowded and highly mobile. That the end-stage kidney disease (ESKD) patients need long-term aggregate hemodialysis appreciably increases the risk of herd infection and disease transmission, making the prevention and control of infectious diseases more challenging than that in the general population. 8 Still, there are limited epidemiological data on hemodialysis patients with COVID-19 during the outbreak of COVID-19 caused by SARS-CoV-2. An early study showed that 37 of the 230 patients enrolled were infected with SARS-CoV-2, among whom six died (crude mortality rate: 16.2%). 9 This suggests that it is imperative to take effective protective interventions to contain the spread of SARS-CoV-2 in dialysis units. In the present study, we conducted a retrospective study on the epidemiological characteristics of such special population to foster clinicians' better understanding.

| Participants
We retrospectively reviewed patients undergoing hemodialysis with suspected or confirmed COVID-19 who were admitted or

| Methods
We collected baseline data of patients, including demographics, primary kidney disease, dialysis vintage, vascular access, and comorbidities including diabetes, hypertension, kidney transplantation, cerebrovascular disease, cardiovascular disease, systemic lupus erythematosus. We also collected the laboratory and radiological findings of patients during the outbreak or during the disease, including blood routine, myocardial enzymes, hepatic, and renal function, electrolytes, ferritin, parathyroid hormone, prothrombin time (PT), activated partial thromboplastin time (APTT), D-dimer, highsensitive C-reactive protein (hs-CRP), lymphocyte subsets, chest CT scan, SARS-CoV-2 nucleic acid results of nasopharyngeal swabs, and SARS-CoV-2 specific antibodies (colloidal gold method, reagent No. 20203400177, from Innovita (Tangshan) Biotech Co., Ltd.). 10 Blood specimens for biochemical tests were collected from the vascular access before midweek hemodialysis sessions. They were collected 7:00-8:00 h before morning sessions and 11:00-12:00 h before midday sessions. The patients were grouped into Group 1 (patients undergoing hemodialysis with COVID-19) and Group 2 (uninfected with COVID-19).

| Criteria for diagnosis and clinical prognosis
All patients are in compliance with the Health Committee of the people's Republic of China about the criteria for COVID-19 diagnosis and treatment plan (trial version 7) at http://www.nhc.gov.cn/yzygj/ s7652 m/20200 3/a3119 1442e 29474 b98bf ed557 9d5af 95.shtml.

| Endpoint of the study
All patients were followed up (Tracking by phone and electronic medical records) until the end event (all-cause mortality), loss to follow-up, or study deadline on April 11, 2020.

| Statistical analysis
Continuous variables were described by median, minimum, and maximum values, whereas categorical variables were described by counts and percentages. The differences between the two Groups were compared using Mann-Whitney U rank-sum test. A value of p < 0.05 was considered statistically significant. All statistical results were calculated using R software version 3.6.3. Graphics were made using Origin version 9.1 and Photoshop version 6.0.

| Epidemiological characteristics
At that time, Wuhan was at the epicenter of the epidemic in China.

The hemodialysis centers of Wuhan Fourth Hospital in Gutian
District were one of the first designated hospitals to care for hemodialysis patients with confirmed or suspected COVID-19. There were two hemodialysis units, one was in Building 1 with negative-pressure isolation ward, and 56 hemodialysis machines for patients with  Table 1.
There was no significant difference in epidemiological data be- between 61 and 70 years (34.7%), and 10 cases were above 70 years (20.4%). Most of the patients were male (61.2%). The longest dialysis vintage was 218 months, and the median dialysis vintage was 26 months. Overall, 69.4% of patients had arteriovenous fistula as vascular access. The frequency of dialysis was three times a week in most patients and five times in 2 weeks in very few patients. The primary diseases that caused ESKD were diverse, among which primary glomerulonephritis and diabetes predominated, accounting for 36.7% and 30.6%, respectively. Moreover, we found that more than 50% of the patients had three or more chronic underlying diseases, and the proportion increased with age ( Figure 2).

| Clinical symptoms and signs
To better understand the clinical symptoms of hemodialysis patients with COVID-19, we considered Group 2 patients who were

| Laboratory results, radiographic findings, and clinical outcomes
For laboratory tests, we perceived no appreciable differences in white blood cell count, neutrophil count, lymphocyte count, myocardial enzymes, renal function, or coagulation function between the two Groups. Lymphocytopenia occurred regardless of whether F I G U R E 1 The flow chart of patient recruitment. After excluding 430 patients, the final sample size of 123 participants was enrolled.
the patient was infected with COVID-19. To better understand whether there was a difference in the distribution of lymphocyte count between the two Groups, we conducted quartile grouping in Figure 4. Furthermore, the results showed that the median hs-CRP and ferritin in Group 1 were appreciably higher than that in Group 2.
Although D-dimer levels in Group 1 were higher than that in Group 2, because the vast majority of patients use heparin for dialysis, the difference in coagulation function between the two Groups was not easy to identify. To determine whether there were changes in lymphocyte subsets between the two Groups, we examined the two TA B L E 1 Demographic and Clinical Characteristics of the Patients at Baseline. Groups of patients and found that there were no significant changes in the proportions of CD8 + T cells, CD4 + T cells, Natural killer cells, and B cells. Moreover, there was no significant difference in CD4to-CD8 ratio between the two Groups in Figure 5 and Table 2.
Collecting 48 chest CT scan results from Group 1, we found that   19 and that both Groups of patients had lymphocytopenia. There was no significant difference in lymphocyte count and lymphocyte subsets between the two Groups that may be related to extensive damage to lymphocyte and granulocyte functions caused by ESKD status, whose responses to SARS-CoV-2 infection may be changed by an abnormal immune system. 20 Early studies have shown that COVID-19 patients with comorbidities tend to have a poor prognosis. [21][22][23] In our study, more than 50% were above 60 years and had multiple diseases in Group 1, but they did not contribute to a significant increase in mortality. The mortality in the present study was higher than the crude mortality rate of COVID-19 patients in China but lower than the recently reported crude mortality rate of Italian patients (4% vs 2.3% vs, 7.2%). 14,24 The reason for the low mortality rate of dialysis patients may be that compared with non-dialysis patients, dialysis patients can make better use of nearby medical resources due to frequent encounters with medical care and be treated at the early stage of the disease, so that medical runs are less likely to cause treatment delays.
Effective infection control intervention is the sole way to prevent the spread of SARS-CoV-2 so far, 25 at the core of which during the outbreak is early identification and isolation and providing supportive care. Unlike ordinary patients, those who undergoing hemodialysis visit hospitals frequently and need to go to designated hospitals for hemodialysis two to three times a week. Due to a dense population and high mobility in the dialysis room, patients repeatedly going back and forth between the family and the hospital caused

CO N FLI C T O F I NTE R E S T
All authors have declared no conflict of interest.