Nephrol Dial Transplant (2020) 35: 737–741

doi: 10.1093/ndt/gfaa069
Advance Access publication 20 March 2020

Recommendations for the prevention, mitigation and

containment of the emerging SARS-CoV-2 (COVID-19)
pandemic in haemodialysis centres

REVIEW
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Carlo Basile 1,2, Christian Combe 3, Francesco Pizzarelli 4, Adrian Covic5,6, Andrew Davenport7,
Mehmet Kanbay8, Dimitrios Kirmizis9, Daniel Schneditz 10, Frank van der Sande11 and Sandip Mitra12
on behalf of the EUDIAL Working Group of ERA-EDTA
1
Division of Nephrology, Miulli General Hospital, Acquaviva delle Fonti, Italy, 2Associazione Nefrologica Gabriella Sebastio, Martina Franca,
Italy, 3Service de Néphrologie Transplantation Dialyse Aphérèse, Centre Hospitalier Universitaire de Bordeaux, Bordeaux, France, 4Nephrology
Unit, SM Annunziata Hospital, Florence, Italy, 5Nephrology Clinic, Dialysis and Renal Transplant Center - ‘C.I. Parhon’ University Hospital,
Iasi, Romania, 6‘Grigore T. Popa’ University of Medicine, Iasi, Romania, 7UCL Centre for Nephrology, Royal Free Hospital, Division of
Medicine, University College, London, UK, 8Division of Nephrology, Department of Medicine, Koc University School of Medicine, Istanbul,
Turkey, 9Department of Nephrology, Colchester General Hospital, Colchester, UK, 10Otto Loewi Research Center, Medical University of Graz,
Graz, Austria, 11Division of Nephrology, Department of Internal Medicine, University Hospital Maastricht, Maastricht, The Netherlands and
12
Manchester Academy of Health Sciences Centre, Manchester University Hospitals Foundation Trust and University of Manchester,
Manchester, UK

Correspondence to: Carlo Basile; E-mail: basile.miulli@libero.it

GRAPHICAL ABSTRACT

How can we reduce transmission of COVID-19 in haemodialysis centres?

This review from the Eudial Working Group of ERA–EDTA provides recommendations for the prevention,
mitigation and containment of the emerging SARS-CoV-2 (COVID-19) pandemic in haemodialysis centres

Recommendations for the Recommendations for dialysis patients

healthcare team
Be trained in use of
personal protective
equipment
Be provided with Should perform hand Body temperature
Inform your team leader clear instructions on hygiene on arrival and should be checked
if symptomatic or in appropriate hand and departure from the before the start and end
contact with a case respiratory hygiene dialysis unit of dialysis sessions

Stay home if unwell

Use full personal protective Should inform staff of Should be instructed Symptomatic patients
equipment when caring for symptoms in advance of to self-isolate should be dialyzed in a
confirmed cases arrival at the dialysis unit separate isolation room

Basile, C. et al. NDT (2020)

@NDTSocial

C The Author(s) 2020. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved.
V 737
ABSTRACT Uraemic patients on dialysis combine an intrinsic fragility
COVID-19, a disease caused by a novel coronavirus, is a major and a very frequent burden of comorbidities with a specific set-
global human threat that has turned into a pandemic. This ting in which many patients are repeatedly treated in the same
novel coronavirus has specifically high morbidity in the elderly area (haemodialysis centres). Dialysis patients constitute a sus-
and in comorbid populations. Uraemic patients on dialysis ceptible population because of their older age and their less effi-
combine an intrinsic fragility and a very frequent burden of cient immune system, and they are therefore more prone to
comorbidities with a specific setting in which many patients are develop severe infectious diseases than the general population
repeatedly treated in the same area (haemodialysis centres). [5, 6]. Dialysis patients are exposed and re-exposed to a higher
Moreover, if infected, the intensity of dialysis requiring special- contamination risk than the general population because their
ized resources and staff is further complicated by requirements routine treatment usually requires three dialysis sessions per
for isolation, control and prevention, putting healthcare systems week. Moreover, if infected, the intensity of dialysis requiring
under exceptional additional strain. Therefore, all measures to specialized resources and staff is further complicated by
slow if not to eradicate the pandemic and to control unmanage- requirements for isolation, control and prevention, putting
ably high incidence rates must be taken very seriously. The aim healthcare systems under exceptional additional strain.

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of the present review of the European Dialysis (EUDIAL) Therefore, all measures to slow if not to eradicate the pandemic
Working Group of ERA-EDTA is to provide recommendations and to control unmanageably high incidence rates must be
for the prevention, mitigation and containment in haemodialy- taken very seriously.
sis centres of the emerging COVID-19 pandemic. The manage- To the best of our knowledge, at the time of writing of this
ment of patients on dialysis affected by COVID-19 must be car- article (14 March 2020), only one series of cases from one hae-
ried out according to strict protocols to minimize the risk for modialysis centre in Wuhan has been published [7]. The
other patients and personnel taking care of these patients. authors reviewed the whole course of the outbreak emerging in
Measures of prevention, protection, screening, isolation and the haemodialysis centre of Renmin Hospital, Wuhan
distribution have been shown to be efficient in similar settings. University, from 14 January 2020, the day the first case was con-
They are essential in the management of the pandemic and firmed, to 17 February 2020, the day of the epidemic extinction.
should be taken in the early stages of the disease. The authors reported that 37 cases in 230 haemodialysis
patients (16.1%) and 4 cases out of 33 staff members (12.1%)
Keywords: coronavirus, COVID-19, end-stage kidney disease, were diagnosed with COVID-19. Dialysis patients with
haemodialysis, pandemic COVID-19 had less lymphopenia, lower serum levels of inflam-
matory cytokines and milder clinical disease than other patients
INTRODUCTION affected by COVID-19 infection. During that epidemic, seven
An epidemic of Severe Acute Respiratory Syndrome-Corona dialysis patients died, including six with COVID-19 and one
Virus-2 (SARS-CoV-2) (COVID-19), a new strand of the coro- without COVID-19. The presumed causes of death were not di-
navirus family, originated from Wuhan (China) in December rectly related to pneumonia, but due to cardiovascular and cere-
2019, and was declared a pandemic by the World Health brovascular diseases, and hyperkalaemia. The outcome of the
Organization as of 11 March 2020 (https://www.who.int/emer four staff members was favourable [7].
gencies/diseases/novel-coronavirus-2019). The global pan- Isolation practices can be effective for preventing secondary
demic of SARS-CoV-2 (COVID-19) is quickly affecting the de- transmission of viruses closely related to COVID-19. For in-
livery of health care worldwide [1–4]. This novel coronavirus stance, during the 2015 MERS-CoV outbreak in Korea, al-
has specifically high morbidity in the elderly and in comorbid though 116 participants in three haemodialysis units were
populations [1–4]. Chronic kidney disease constitutes a relevant incidentally exposed to the virus, strict patient surveillance and
co-morbidity, and dialysis centres pose a risk as potential vector proper isolation practice prevented secondary transmissions
in the spreading of this pandemic [1–4]. In previous epidemics [8].
or catastrophic situations, the case fatality rate has always been COVID-19 infection in patients treated in dialysis centres
much higher in dialysis patients than in the general population. presents a particular challenge as the risk of transmission to the
In the first two decades of this century, three members of the medical staff, facility workers, other patients and to family
coronavirus family, Severe Acute Respiratory Syndrome- members is significantly increased.
Corona Virus (SARS-CoV), Middle East Respiratory The Chinese Society of Nephrology [9], the Taiwan Society
Syndrome-Corona Virus (MERS-CoV) and SARS-CoV-2, have of Nephrology [10] and the Centers for Disease Control and
caused three major pandemic outbreaks of infectious respira- Prevention (https://www.cdc.gov/coronavirus/2019-ncov/
tory diseases. At the present time, it is believed that SARS-CoV- healthcare-facilities/dialysis.html) have recently developed
2 is more contagious, but with a lower case fatality rate than the guidelines for dialysis units during the COVID-19 outbreak.
other two viruses. Compared with the previous two outbreaks, The aim of the present review of the EUDIAL Working Group
the epidemic area of COVID-19 caused by SARS-CoV-2 is of ERA-EDTA is to provide recommendations for the preven-
larger, the number of infected people and, consequently, the tion, mitigation and containment in haemodialysis centres of
number of deaths higher, and the strain on the healthcare sys- the emerging SARS-CoV-2 (COVID-19) pandemic. In doing
tem, as well as the global economic loss, greater [1–4]. so, we have held in high consideration the suggestions of our

738 C. Basile et al.

Asian colleagues, given their significant experience in dealing the nose and mouth when coughing or sneezing, how to
with COVID-19 [9, 10], the interim additional guidance re- dispose of, preferably disposable paper, tissues and con-
leased by the Centers for Disease Control and Prevention on 10 taminated items in waste receptacles, and how and when
March 2020 [11] and the World Health Organization recom- to perform hand hygiene. Dispensers of hydroalcoholic
mendation for the rational use of personal protective equip- solutions should be installed in waiting rooms. Patients
ment for COVID-19 [12]. The EUDIAL Working Group will must be educated and encouraged to perform hand hy-
update its recommendations any time new data and evidences giene at least on arrival and at the time of departure from
become available. The ERA-EDTA has also launched a dedi- the unit and if in contact with respiratory secretions.
cated webpage that is regularly updated at https://www.era- Dialysis facilities should have space in waiting areas for ill
edta.org/en/covid-19-news-and-information/. patients to sit separated from other patients by at least 2
m. Medically stable patients might opt to wait in a per-
RECOMMENDATIONS sonal vehicle or outside the healthcare facility. Two
metres separation between dialysis stations is advisable.
Healthcare team • Treatment and waiting areas should have good air condi-

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• A working team consisting of dialysis physicians, nursing tioning and ventilation to remove particles and aerosol
staff and technicians should receive training in updated droplets from the air.
clinical knowledge of the COVID-19 epidemic, epidemic
• Body temperature should be systematically measured be-
prevention tools and guidelines from the government, sci- fore the start and at the end of the dialysis session in all
entific societies and hospital authorities. Instructions patients.
should include how to use the different types of face-
• Early recognition and isolation of individuals with respi-
masks, how to use tissues to cover the nose and mouth ratory infection are mandatory: (i) dialysis facilities
when coughing or sneezing, how to dispose of tissues and should identify patients with signs and symptoms of fever,
contaminated items in waste receptacles, and how and cough, upper airway involvement or conjunctivitis before
when to perform hand hygiene. Training can be done they enter the waiting room and treatment area; (ii)
peer to peer or online. patients must inform staff of fever or respiratory symp-
• Latest care recommendations and epidemic information toms before arrival at the facility by phone or appropriate
should be updated and delivered to all medical care per- electronic means; thus, the facility can be prepared for
sonnel as needed. their arrival (preferably they should be seen in a first aid
• Staff members should self-monitor their symptoms (if department and not in a dialysis department) or triage
any) and should inform the team leader in case they or them to a more appropriate setting such as an acute care
their family members develop symptom(s) suggestive of hospital; (iii) patients with respiratory symptoms should
COVID-19 infection. Sick members of the team should be brought to an appropriate treatment area as soon as
stay at home, and in any case should not be in contact possible to minimize the time in waiting areas; (iv) all
with patients or other team members. patients who have fever, cough, upper airway involvement
• Nurses should be trained to take nasopharynx swabs for or conjunctivitis should be screened for novel COVID-19
COVID-19 polymerase chain reaction, with appropriate infection. For sampling, patients should be either in a
dressing using a filtering face piece 2 (FFP2) mask (filter- single-patient room or in a room dedicated to sampling.
ing 95% of particulate matter and aerosols in inhaled air), Disinfection of the room after sampling is mandatory.
goggles, mobcap, disposable surgical blouse and gloves.
• Ideally, symptomatic patients should be dialysed in a sep-
arate isolation room (if available), in which a negative
pressure atmosphere can be established, with the door
Dialysis patients and dialysis facilities
closed. Otherwise, they should wait in a separate isolation
• Dialysis patients should be instructed to stay at home room and receive dialysis in the last shift of the day until
while off dialysis and on their non-dialysis days, to use in- infection is excluded. He/she should wear a proper (surgi-
dividual transport to and from dialysis facilities, to avoid cal or N95) mask filtering 95% of the particulate matter
public transportation, to abstain from travelling around <2.5 mm in the aerosol of exhaled air.
the country, to avoid personal contact, and to abstain • Patients with confirmed COVID-19 infection should be
from public, private or religious events (family reunions, admitted to an airborne infection isolation room and
marriages, funerals, etc.). Parents and grandparents on di- should not receive dialysis in an outpatient dialysis facil-
alysis may want to abstain from personal contact espe- ity, unless an airborne infection isolation room is avail-
cially with their children and grandchildren, because the able. All personnel involved in the direct care of patients
younger population serves as a vector of the disease often affected by COVID-19 must undertake full protection, in-
without showing symptoms. cluding long-sleeved waterproof isolation clothing, hair
• Dialysis facilities should provide patients with instructions caps, goggles, gloves and medical masks (FFP2 or FFP3
(in appropriate languages) about hand hygiene, respira- mask if available) filtering 95–99% of particulate matter
tory hygiene and cough etiquette. Instructions should in- and aerosols in inhaled air. Hand hygiene must be strictly
clude how to use facemasks, how to use tissues to cover implemented, carefully washing hands with soap and

Recommendations against SARS-CoV-2 (COVID-19) pandemic 739

 water and systematically using alcoholic solutions and coronavirus but not showing any signs of infection) [13],
disposable gloves. can have dialysis as usual during the 14-day period of
• Consideration should be given to cohorting more than quarantine of the family members or caregivers.
one patient with suspected or confirmed COVID-19 and • Once family members or caregivers of dialysis patients
the healthcare team caring for them in the same section of have been converted to a confirmed case, the patient’s
the unit and/or on the same shift (e.g. consider the last identity must be upgraded and treated in accordance with
shift of the day). Avoid, however, mixing of suspected and the above-mentioned conditions.
confirmed cases.
• Manpower should be cohorted in separate teams for the Home haemodialysis and peritoneal dialysis
management of high-risk and low-risk patients. Only the
assigned healthcare team should enter the isolation room/
• These patients should be assisted at home as far as is pos-
cohort area, all non-scheduled team-mates should be ex- sible, using telereporting assistance or other electronic
cluded at all times. systems for clinical management and to supplement
• If a newly confirmed or highly suspected case of novel co- home visits by healthcare staff, as deemed necessary.

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ronavirus infection in dialysis centres is identified, disin-
fection must be carried out immediately. Areas in close CONCLUSIONS
contact with these patients must not be used for other
patients until cleared. COVID-19, a disease caused by a novel coronavirus, is a major
• The medical waste from confirmed or suspected patients global human threat that has turned into a pandemic. The only
with novel coronavirus infection must be considered as study so far reporting an outbreak of COVID-19 in a dialysis
infectious medical waste and disposed of accordingly. centre indicates that dialysis patients are a highly susceptible
population and haemodialysis centres are a high-risk area in the
outbreak of a COVID-19 epidemic [7]. The management of
Duration of isolation precautions for patients under patients on dialysis affected by COVID-19 must be carried out
investigation for or with confirmed COVID-19 according to strict protocols to minimize the risk for other
• Discontinuation of isolation precautions should be deter- patients and personnel taking care of these patients. Measures
mined on a case-by-case basis, in conjunction with local, of prevention, protection, screening, isolation and distribution
state and federal health authorities, until the information have been shown to be efficient in similar settings [8].
is available regarding viral shedding after clinical Prevention plays a key role; the other measures are essential in
improvement. the mitigation and containment of the COVID-19 pandemic in
• Factors to be considered include presence of symptoms haemodialysis centres.
related to COVID-19 infection, date when symptoms re-
solved, other conditions that require specific precautions CONFLICT OF INTEREST STATEMENT
(e.g., tuberculosis, Clostridium difficile), other laboratory
information reflecting clinical status and alternatives to None declared.
inpatient isolation, such as the possibility of safe recovery
at home. REFERENCES
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pneumonia in China, 2019. N Engl J Med 2020; 382: 727–733
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MERS combined, despite lower case fatality rate. BMJ 2020; 368: m641
• Patients who need vascular access surgery should be 3. Huang C, Wang Y, Li X et al. Clinical features of patients infected with 2019
screened for COVID-19. Operations on patients with con- novel coronavirus in Wuhan, China. Lancet 2020; 395: 497–506
firmed or suspected COVID-19 infection must be carried 4. Naicker S, Yang CW, Hwang SJ et al. The novel coronavirus 2019 epidemic
out in a designated room with necessary protection for and kidneys. Kidney Int 2020; doi:10.1016/j.kint.2020.03.001
5. Syed-Ahmed M, Narayanan M. Immune dysfunction and risk of infection
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Operational strategies for family members and disease. Nat Rev Nephrol 2013; 9: 255–265
7. Ma Y, Diao B, Lv X et al. 2019 Novel Coronavirus Disease in Hemodialysis
caregivers (HD) Patients: Report from One HD Center in Wuhan, China. https://www.
• All family members living with dialysis patients must fol- medrxiv.org/content/10.1101/2020.02.24.20027201v2 (14 March 2020, date
last accessed)
low all precautions and regulations given to patients to 8. Park HC, Lee SH, Kim J et al. Effect of isolation practice on the transmission
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11. Centers for Disease Control and Prevention. Interim Additional Guidance 13. Lauer SA, Grantz KH, Jones FK et al. The incubation period of coronavirus
for Infection Prevention and Control Recommendations for Patients with disease 2019 (COVID-19) from publicly reported confirmed cases: estima-
Suspected or Confirmed COVID-19 in Outpatient Hemodialysis Facilities, tion and application. Ann Intern Med 2020; doi:10.7326/M20-0504
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Nephrol Dial Transplant (2020) 35: 741–751

doi: 10.1093/ndt/gfaa072

REVIEW
Muscle protein turnover and low-protein diets in patients with

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chronic kidney disease

Giacomo Garibotto, Daniela Picciotto, Michela Saio, Pasquale Esposito and Daniela Verzola
Division of Nephrology, Dialysis and Transplantation, Department of Internal Medicine and IRCCS Ospedale Policlinico San Martino,
University of Genova, Genova, Italy

Correspondence to: Giacomo Garibotto; E-mail: gari@unige.it

This Review has been written in collaboration with NDT-Educational.

ABSTRACT short-term studies on muscle protein turnover can be extrapo-

Adaptation to a low-protein diet (LPD) involves a reduction in lated to the long-term period.
the rate of amino acid (AA) flux and oxidation, leading to more Keywords: CKD, low-protein diets, nutrition, protein
efficient use of dietary AA and reduced ureagenesis. Of note,
the concept of ‘adaptation’ to low-protein intakes has been sep-
arated from the concept of ‘accommodation’, the latter term im- BACKGROUND
plying a decrease in protein synthesis, with development of
Despite the fact that protein restriction has been used for many
wasting, when dietary protein intake becomes inadequate, i.e.
decades in the treatment of patients with chronic kidney disease
beyond the limits of the adaptive mechanisms. Acidosis, insulin
(CKD), there are still several unresolved issues regarding the
resistance and inflammation are recognized mechanisms that metabolic effects of low-protein diets (LPDs). One major issue
can increase protein degradation and can impair the ability to is our still incomplete understanding of the response of muscle
activate an adaptive response when an LPD is prescribed in a metabolism to protein restriction in humans. Skeletal muscle is
chronic kidney disease (CKD) patient. Current evidence shows a highly adaptive tissue that responds to hormones, substrate
that, in the short term, clinically stable patients with CKD supply and exercise with changes in protein metabolism and ul-
Stages 3–5 can efficiently adapt their muscle protein turnover to timately in muscle composition and size [1]. However, how and
an LPD containing 0.55–0.6 g protein/kg or a supplemented to what extent muscle protein metabolism adapts to decreased
very-low-protein diet (VLPD) by decreasing muscle protein protein intake in humans is still largely unexplored. Studies per-
degradation and increasing the efficiency of muscle protein formed using the nitrogen (N) balance have shown that healthy
turnover. Recent long-term randomized clinical trials on sup- young subjects can stay on neutral or even slightly positive bal-
plemented VLPDs in patients with CKD have shown a very ance with protein intakes as low as 0.55–0.6 g/kg [2–5]. Studies
good safety profile, suggesting that observations shown by performed using stable isotope amino acid (AA) kinetics have

C The Author(s) 2020. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved.
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