Received: 24 March 2020 | Revised: 12 April 2020 | Accepted: 20 April 2020 DOI: 10.1111/ajt.15948 B R I E F C O M M U N I C AT I O N The impact of the COVID-19 outbreak on liver transplantation programs in Northern Italy Umberto Maggi1 | Luciano De Carlis2 | Daniel Yiu3 | Michele Colledan4 Enrico Regalia5 | Giorgio Rossi6 | Marco Angrisani2 | Dario Consonni7 Gianluca Fornoni1 | Giuseppe Piccolo8 | T. Maria DeFeo9 1 General Surgery and Liver Transplantation Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico di Milano, Milan, Italy | | In January 2020, Novel Coronavirus Disease 2019 (COVID-19) resulted in a global pandemic, creating uncertainty toward the management of liver transplantation (LT) Division of General Surgery & Abdominal Transplantation, ASST Grande Ospedale Metropolitano Niguarda, Milan, Italy programs. Lombardy has been the most affected region in Italy: the current mortal- Emergency Department, Oxford University Hospitals NHS Trust, Oxford, UK in Lombardy having to expand the total number of ICU beds from 724 to 1381 to 2 3 Division of Liver and Small Bowel Transplantation, Azienda Ospedaliera Papa Giovanni XXIII, Bergamo, Italy 4 Hepato-Pancreato-Biliary Surgery and Liver Transplant Unit, Istituto Nazionale Tumori, Istituto di Ricovero e Cura a Carattere Scientifico, Milan, Italy 5 Department of Pathophysiology and Transplantation, University of Milan, Milan, Italy 6 Occupational Health Unit, Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico, Milano, Italy 7 Regional Transplant Coordination, Lombardy Region, Milan, Italy ity rate of COVID-19 patients is 18.3% (10 022 deaths; April 10th) with hospitals accommodate infected patients. There has been a drastic decrease in liver donors. From February 23rd until April 10th, 17 LTs were performed in Lombardy. Mean donor age was 49 years (range 18-74) whereas mean recipient age was 55 (13-69); mean MELD score was 12 (6-24). All donors underwent screening for SARS-CoV-2 prior to LT. Two patients tested positive after LT, and one patient died for COVID on POD 30. Sixteen patients are alive after an average of 30 days post-LT (range 3-46). 10 patients have been discharged. This study has found no specific reason concerning the safety of recipients, to stop LT programs. Several key lessons from our experience are reported. However, due to the complex circumstances which surround the viral outbreak, the cessation or a reduction in LT activity is a pragmatic requirement. 8 Transplant Coordination Reference Center – North Italy Transplant program (CRR/NITp), Fondazione IRCCS Ca' Granda Ospedale Maggiore Policlinico di Milano, Milan, Italy 9 KEYWORDS bronchoalveolar lavage (BAL), clinical research/practice, critical care/intensive care management, epidemiology, infection and infectious agents – viral, liver transplantation/ hepatology, organ allocation Correspondence Umberto Maggi Email: maggi.umberto@gmail.com 1 | I NTRO D U C TI O N throughout China and was later identified as the Novel Coronavirus Disease 2019 (COVID-19), resulting in a global pandemic. The first cases of COVID 19 in Italy were confirmed in 2 Chinese In December 2019, the world saw the initial reports of a new respira- tourists on January 30, 2020. On February 18, the first documented tory illness in patients from Wuhan, China. The disease rapidly spread secondary transmission was identified in an Italian citizen and shortly Abbreviations: BAL, brochoalveolar lavage; CNT, Centro Nazionale Trapianti; CoV, coronavirus; COVID, coronavirus disease; CPAP, continuous positive airway pressure; ICU, intensive care unit; INMI, Istituto Nazionale Malattie Infettive; LT, liver transplantation; MERS, Middle East respiratory syndrome; NITp, North Italy Transplant program; POD, postoperative day; SARS, severe acute respiratory syndrome; WHO, World Health Organization. © 2020 The American Society of Transplantation and the American Society of Transplant Surgeons 1840 | amjtransplant.com Am J Transplant. 2020;20:1840–1848. | MAGGI et Al. afterwards, Northern Italy experienced an alarming acceleration in 1841 2.1 | Timeline of events the number of confirmed cases. Liver transplantation (LT) is a well-established procedure in Italy The first two confirmed cases of COVID-19 in Italy were identified for end-stage liver diseases, with 1031 patients on the waiting list in on January 30, 2020 at the Istituto Nazionale Malattie Infettive December 2019.1 Lazzaro Spallanzani (INMI) in Rome, one of the leading tertiary cent- Lombardy, the most highly affected region in Italy, is a region ers for infectious diseases in Italy. The patients were reported to be where there are currently four active liver transplant programs 2 Chinese tourists who were isolated on January 29 and discharged (Ospedale Niguarda in Milan, Fondazione IRCCS Policlinico in Milan, on February 26. In response, Italy declared a state of emergency, Istituto dei Tumori in Milan, and Ospedali Riuniti in Bergamo). suspending all incoming and outgoing flights to China. There is currently a large degree of uncertainty toward the man- The first documented case of secondary transmission was identi- agement of LT programs during the coronavirus outbreak. Our aim fied on February 18 in Codogno, a town of 15 000 inhabitants south- is therefore to share our observations on the coronavirus outbreak east of Milan within the Lombardy region of Northern Italy. in order to demonstrate the impact that such a disease may have on liver transplant programs. Specifically, we aim to identify: Afterward, the number of confirmed cases of COVID-19 slowly grew, until February 23, when suddenly 121 new cases were confirmed. On February 24 the National Department of Transplantation 1. If the outbreak of coronavirus has led to a decrease in the number of LTs, and the reasons for this. (Centro Nazionale Trapianti: CNT) issued a directive2 stating that all deceased donors from 5 Northern Regions of Italy (Lombardy, 2. The effect of the coronavirus outbreak, whether direct or indirect Veneto, Piemonte, Emilia Romagna, and Trento) were to be tested on the survival of liver transplant patients, including their risk of for SARS-CoV-2 prior to transplantation. Broncho Alveolar Lavage infection with resulting morbidity and measures to be kept to pre- (BAL), if positive, would result in the transplantation process to be vent SARS-CoV-2 infections in LT patients. aborted. On March 6, the recommendation was extended to donors in all Italian regions. On March 16, the CNT released a new directive, 2 | PATI E NT S A N D M E TH O DS stating that additionally, all recipients were to be screened prior to a transplantation via nasal pharyngeal swabbing. From February 24, infections and deaths from SARS-CoV-2 in Regional (Lombardy) data on patients with confirmed COVID-19 were gathered prospectively from January 30, 2020 onward. Lombardy rose sharply (see Figure 1). The Councils of Ministers enacted new 9 decree-law3 (from We compared data regarding liver donations in NITp area February 23 to March 22) in order to contain the outbreak. It was (Lombardy, Veneto, Liguria, Friuli Venezia Giulia, Trento, and Marche), initially decided that more than 50 000 people from 11 different to the number of COVID positive patients in Lombardy, through the municipalities in Northern Italy were to be quarantined; however, North Italy Transplant program (NITp) Database. shortly afterward, this was expanded, leading to the cessation of all We analyzed the number of liver donations performed in Lombardy from January to March 2020. We calculated percent commercial activity across Italy (March 21), with the exception of supermarkets and pharmacies. reduction and 95% confidence intervals (95% CI) of mean weekly counts of donors (referred and recovered) in the 4 weeks period from February 23 (period 1) with those in the previous 8 weeks (pe- 3 | R E S U LT S riod 0), using univariate Poisson regression. Statistical analysis was performed with Stata 16 (StataCorp. 2019). We prospectively collected data on LTs performed in Lombardy before and after the onset of the outbreak. From February 23, 2020 until March 22, liver donation in the NITp area decreased. The comparison of data from the January to end of March indicates a drastic reduction in the donor rate. Donors re- Data regarding donors (age, laboratory data, ICU days, BMI, city ferred and recovered before and after the onset of the outbreak in of residence, graft), recipients (age, gender, basic laboratory data, Lombardy are reported in Figure 2. Referred donors dropped from MELD score, BMI, disease, city of residence, immunosuppression, 9.6 (period 0) to 4.0 (period 1) per week (−58%, 95% CI: −44% to hospitalization days, outcome, surgical and medical complications, −73%). Recovered donors dropped from 5.4 (period 0) to 3.0 (period tests for coronavirus), LT (date, ischemia time), and retransplantation 1) per week (−46%, 95% CI: −71% to +6%). procedures performed in the Lombardy Region were collected prospectively from February 23, 2020 onward. The survival of liver-transplanted patients from February 23, 2020 to April 10, 2020 was documented. The study was approved by the Ethical Committee of the promoting center. LTs in Lombardy also decreased (Figure 3) from the 4th week of February onward. In Italy there are approximately 5090 ICU beds.4 The number of curative care beds5 in Italy in 2017 were estimated at 2.62 per 100 000 inhabitants, and 3.72 in the European Union. Existing data on curative care beds for comparison have reported that Germany 1842 | FIGURE 1 MAGGI et Al. The number of confirmed SARS-CoV-2 cases in Lombardy F I G U R E 2 Donors referred and recovered in Lombardy before and after the onset of outbreak (the arrow shows the beginning of the outbreak) [Color figure can be viewed at wileyonlinelibrary. com] has 6.01/100 000 inhabitants. Current European data on ICU beds do not allow for the direct comparison of different countries. In mid-February there were 724 ICU beds in the Lombardy re- (6-24). All donors underwent screening for SARS-CoV-2 prior to LT with BAL and 13 recipients were tested with nasal pharyngeal swabbing prior to LT. All patients except 4 were treated with Basiliximab, gion. In response to the outbreak, by March 19 this was increased to Prednisolone, and Tacrolimus after LT. Medical complications oc- 1250. Then, a reported 1381 patients were being treated in ICU by curred in 6 patients and in 5 patients repeated screening for coro- April 4 indicative of an acute influx of COVID-19 patients requiring navirus was performed. Of these 5 patients, 2 patients, males, aged treatment in secondary care (Figures 4 and 5). 61 and 69, resulted positive. The first patient manifested with fever The current mortality rate in COVID patients in Italy is 12.7% (18 279 deaths; April 10) and 18.3% (10 022 deaths) in Lombardy. on postoperative day (POD) 9 but had a normal chest x-ray findings. The second patient, HIV pos, had positivity for SARS-CoV-2 on POD From February 23 to April 10, 16 LTs and 1 retransplantation 22 and died with COVID-19 on POD 30; 16 patients are currently were performed in Lombardy in 16 adults and 1 pediatric patient. alive after a mean time of 30 days post-LT (range 3-46). A total of 10 All donors except 1 and all recipients except 3 were from Northern patients have been discharged after a mean time of 16 days (range Italy. Mean donor age was 49 years (range 18-74) whereas recipient 11-31) and are being follow-up as outpatients. mean age was 55 (13-69); 6 patients were affected by hepatocellular carcinoma. One was HIV pos; the mean MELD score was 12 Data regarding donors, recipients, and transplantation procedures are reported in Figure 6. | MAGGI et Al. 1843 F I G U R E 3 Liver transplantations in Lombardy before and after the onset of outbreak (the arrow shows the beginning of the outbreak) FIGURE 4 The treatment location of SARS-CoV-2-infected patients in Lombardy 4 | D I S CU S S I O N A total of 81 907 cases have been reported in China since the outbreak (April 10, 2020)7; however, the rapid doubling time of cases The World Health Organization (WHO) declared COVID-19 a Public Health Emergency of International Concern as of February 1, 2020 and declared as a pandemic on March 11, 2020. Over recent decades6 coronavirus has been responsible for sev- and spread in other countries has been alarming. For example in Italy, only a handful of cases were reported on January 30, but by February 23, Italy had reported 121 cases8 and by April 10, 147 577 cases. eral outbreaks, including the 2002 SARS (Severe acute respiratory syndrome) outbreak in Guandong Province, China, and the 2012 MERS (Middle East respiratory syndrome) outbreak in Saudi Arabia. The current SARS-CoV-2 is highly contagious and as to date 4.1 | Liver transplantation and the COVID-19 outbreak (April 10, 2020) 1 687 857 cases have been identified worldwide with 102 198 deaths. The mortality rate in closed cases (recovered The first LT in Italy dates back to 1983, and to date (December 2019) and deceased) is 21%.7 24 518 LT have been performed.1 1844 | MAGGI et Al. FIGURE 5 Intensive care beds with COVID patients in Lombardy during SARS-CoV-2 outbreak D Dresidence Age R R sex age (M/F) HCC MELD Score POD 1 opera (MI) 63 61 M 0 24 39 Y Y 2 3 4 Milano Milano Milano 74 57 18 47 66 64 F F M 0 0 1 13 22 8 46 43 42 Y Y Y 5 Agrigento 25 59 M 0 6 38 6 7 8 9 10 Como Cormano Novara Sondrio Verbania 64 54 68 57 45 68 61 47 49 54 M M M F M 0 1 0 1 1 11 11 14 6 15 36 32 25 24 45 11 Bergamo 29 69 M 1 8 12 13 14 15 Bari Genova Milano Cuneo 30 47 49 61 13 63 60 31 F F M M 0 0 0 0 11 9 13 13 16 Desio (MI) 42 62 M 1 17 Chieti 50 63 M 1 n LT D pre-LT R pre- R posttest LT test LT test Medical complications outcome discha POD rged Discharge N 0 alive Y 13 N N N N N N alive alive alive Y Y Y 15 17 11 Y Y Y (neg) alive Y 17 Y Y Y Y Y Y Y Y Y N Y (neg) Y (pos) Y (neg) N N 0 fever in pod 5 0 lung bacterial infection pleural effusion COVID+ 0 0 ascitis Y Y Y Y Y 13 31 20 10 12 Y Y Y (pos) dyspnea 36 31 18 13 Y Y Y Y Y Y Y Y Y (neg) N Y (neg) 0 0 0 0 alive alive alive alive alive dead (POD 30) alive alive alive alive 6 10 Y Y N 0 alive 14 3 Y Y N 0 alive F I G U R E 6 Main donor and recipient data of LTs performed during SARS-CoV-2 outbreak in Lombardy. All “D residences” are towns from Northern Italy except for Agrigento. D, donor; R, recipient; Y, yes; N, no; F, female; M, male; POD, postoperative day There are currently 21 active liver transplant units, and accord- performed in all cases and negative in all donors. Based on data from ing to European Liver Transplant Registry 9 these units are operating Lombardy, the most at risk age group for mortality are those over the at the rate of more than 1000 liver transplants per year. In 2019, age of 5011 with worse prognosis over the age 70. CT chest scans of 1302 liver transplants were performed, including 1278 liver trans- donors are not always readily available during the current pandemic. plants from brain-dead donors. 10 However, when available, may represent a further diagnostic advan- As the impact of COVID-19 during the start of the outbreak was tage. Screening for COVID-19 in recipients has only recently been not well established, the National Department of Transplantation (March 16) suggested in Italian national protocols; however, prior to (Centro Nazionale Trapianti: CNT) opted to continue with LTs, as these regulations most transplant units were already performing re- they are regarded as a life-saving procedure. These procedures were cipient testing for SARS-CoV-2. We believe that additionally testing to continue, despite concerns regarding the safety from these do- the recipient is the best practice as the immunosuppression post- nors. Initially the national guidelines stated that only donors had transplant may allow for uncontrolled viral proliferation in previously to be screened with BAL for SARS-CoV-2. Donor screening was undiagnosed patients. | MAGGI et Al. Testing performed through BAL samples in donors is likely more sensitive, 12 and allows the exclusion of disease in at risk donors. The 1845 and prolonged shedding of virus thus potentially increasing the risk of transmission to contacts including health-care workers.” same cannot be said for recipients who undergo testing via nasal The two cases of MERS CoV infections in 2014 reported by pharyngeal swabbing. A single negative test is likely to be unreliable AlGhamdi were two renal transplant recipients with variable clinical and the results from BAL cannot be logistically obtained prior to LT presentations and outcomes. The first patient presented with progres- due to such strict time constraints. It is therefore a possibility that sive respiratory symptoms, acute renal failure and died. The second unrecognized positive patients may undergo LT. If this occurs, the survived. The authors state that although a few changes to the trans- patient may represent an unrecognized super-spreader13 after LT. plant program were made in response to the MERS-CoV endemic, We believe that BAL in recipients, even if nasal pharyngeal swab- transplant procedures were ultimately stopped during the epidemic.16 bing is negative, may still represent an important diagnostic test, In Canada 2003, Kumar17 reported the case of a 74-year-old when the recipient is intubated, either performed at the end of LT, male who died of SARS 18 days after the onset of symptoms. The or immediately before. In our first patient who tested positive 9 days patient had undergone LT 9 years prior and as such, due to an out- after LT, only nasal pharyngeal swabbing was performed; therefore, break of SARS in the greater Toronto area, all programs in the city it is impossible to know if infection was present prior LT or if it was were temporarily closed. Prior to restarting the transplant program, contracted afterwards during recovery in hospital. We therefore rec- a donor SARS screening tool was performed due to risk of coronavi- ommend BAL in all LT recipients, even if the result may only be avail- rus transmission from undiagnosed organ donors. able during or soon after LT. This allows for reliable information to Chui18 reported that during the 2003 SARS outbreak in Hong be retrieved, aiding both in the prevention of disease in health-care Kong, no LTs were performed, as the intensive care unit was ded- workers and in the management of the patient. In case of BAL positiv- icated to the care of SARS patients. The author reminds that “the ity during LT, the patient should be transferred in a COVID ICU after SARS outbreak demonstrated the vulnerability of an organ trans- LT. The second patient was found to be positive on postoperative 22, plantation service. The human and financial costs are significant.” therefore it is likely that this represents infection posttransplant. In recipients a further diagnostic tool for COVID-19 should be While closely related to SARS-CoV and MERS-CoV, the mortality associated with COVID-19 may be lower than what is reported. a chest CT scan at arrival in the hospital for LT. In case of suspect However, caution is still required as we do not yet know the full im- COVID-19 at pre-LT CT scan, LT should not be performed. pact of the infection as it spreads to more diverse populations. The debate regarding the impact of immunosuppression is currently wide open14 as some authors believe that immunosuppression may be beneficial in COVID-19. 4.3 | Limiting factors for liver transplantation The full natural history of COVID-19 is currently unknown; however, the use biologics such as Basiliximab, a monoclonal antibody to Although authorities in Italy have not formally halted the transplant the α chain (CD25) of the IL-2 receptor of T cells, may act toward the programs across Lombardy, several factors have contributed to a attenuation of cytokine storm syndrome.14 The impact of biologics temporary decrease in LTs: and their associated benefits effects in COVID-19 has yet to be reported. The patient who died among our cases was not treated with basiliximab. 1. There has been an overwhelming influx of COVID-19 patients to ICU beds. This has affected both the identification process for potential donors, as well as the availability of beds for recipients. 4.2 | Current literature on organ transplant and coronavirus 2. ICU doctors have been redeployed in the care of COVID-19 pa- In the literature there have been few papers published regarding LT 3. There are concerns toward the risk of nosocomial COVID-19 in- during outbreaks of coronavirus disease. In the first publication15 fection in recipients, especially considering the potential contact during the recent outbreak of SARS-CoV-2, several measures includ- with asymptomatic carriers within the hospital. Separation of ing screening of medical staff, the creation of a donation protocol, Units into COVID-19-positive and COVID-19-negative patients and the documentation of pre/postoperative management measures is mandatory, so that in case of difficulty to obtain that, a LT were reported by the Organ Transplant Center, Sichuan Academy should not be performed as the risk of infection is too high. For of Medical Sciences and Sichuan Provincial People's Hospital, the same reason, from the beginning of the outbreak our hospital University of Electronic Science and Technology in Western China. has prohibited family/visitors at the bedside. Patients in medical However, to date no results regarding LTs have been reported. units should wear face coverings such as doctors, nurses, and tients, and thus there has been a paucity of ICU specialists for the liver transplant programs. on the basis of two cases of kidney transplanted health-care workers. Moreover, the transfer of patients to radi- people during the MERS outbreak in 2014 reported by AlGhamdi16 Michaels, ology units for a chest X-ray represents an additional infection suggests that “due to the need for immunosuppression in solid organ risk. Thus a bedside chest ultrasound may be a useful alterna- transplant recipients, they may be anticipated to have more intense tive in these situations. All at risk staff including doctors, nurses, 13 1846 1 | MAGGI et Al. Check the availability of beds in COVID negative ICU and COVID negative units in the hospital 2 F I G U R E 7 Suggested measures for liver transplantation during SARS-CoV-2 outbreak Not to send the procurement team to the donor hospital but to ask if a local team in the donor hospital are capable of organ retrieval and send the liver to the recipient hospital 3 Perform BAL for SARS-CoV-2 testing in all donors and a chest CT scan if available. 4 Perform a chest CT-scan at the arrival of the recipient. If positive the patient is not to be transplanted. 5 Perform a nasal pharyngeal swabbing at the arrival of the recipient, waiting for its result before LT. 6 Perform a BAL for SARS-CoV-2 when the recipient is intubated just before or at the end of the LT procedure 7 If SARS-CoV-2 positivity in the recipients during or after LT, the patient should be transferred in a COVID positive ICU/Unit. 8 During the in-patient post-op follow-up, limit transport of the patients to other units such as Radiology or Endoscopy. No family/visitors allowed at bedside. In medical units patients should wear face coverings such as doctors, nurses and healthcare workers 9 Chest Ultrasound may be a viable alternative to chest X-ray in the recipient for the study of lungs in ICU or medical units. 10 All at risk staff including doctors, nurses, healthcare workers, ambulances, Endoscopy Units and Radiology Units should be routinely screened for Coronavirus. 11 We suggest the addition of Basiliximab to the immunosuppressive protocol. 12 No serial test for Sars-CoV-2 should be performed in the post-op time in asymptomatic recipients; a swabbing test should be performed in case of fever or elevated CRP of unknown origin. If persisting doubts perform a chest CT scan. 13 After discharge, minimize patients coming to hospitals for outpatient follow up, unless strictly necessary. 14 Evaluate and reserve LT to only recipients with incredibly poor prognosis and those with advanced HCC. health-care workers, ambulances, endoscopy units, and radiology the procurement team should not be sent to the donor hospital units should be routinely screened for coronavirus. advising the local team at the donor hospital for organ retrieval 4. Close clinical monitoring is mandatory if an LT program is in- and sending to the recipient hospital. tended to continue; no serial testing for SARS-CoV-2 in asymptomatic recipients should be performed in the postoperative period If organization and the situation at a local level permits, there unless there are clinical manifestations such as fever or elevated must be a careful risk/benefit analysis for performing transplanta- CRP of undetermined origin. In that case a nasal pharyngeal swab- tion, taking into consideration the recipient's risk of dying of end- bing test should be performed. If clinical doubts persist it is better stage liver disease or cancer vs the risk of COVID-19. Therefore, to perform a chest CT scan and if positive LT patients should be during an outbreak, we advise the avoidance of performing LTs in transferred in a COVID Unit. nonurgent cases, with LT reserved to those patients with true end- 5. As already reported by others there are concerns regarding the safety of the procurement teams,13 who may be exposed to potentially infected patients during the procurement process. Ideally stage liver disease and extremely poor prognosis. A table summarizing key lessons that we learnt from our experience is reported in Figure 7. | MAGGI et Al. 1847 4.4 | Limits of this study Michele Colledan https://orcid.org/0000-0002-3880-4763 The primary limit of our study is the short follow-up time for our Enrico Regalia patients. If serious complications are reported in the future, though Giorgio Rossi the adoption of all measures to obviate them, then the evidence sur- Marco Angrisani https://orcid.org/0000-0001-6414-7835 rounding the management of liver transplant programs during out- Dario Consonni https://orcid.org/0000-0002-8935-3843 breaks should be reconsidered. Gianluca Fornoni https://orcid.org/0000-0001-8287-5836 Giuseppe Piccolo https://orcid.org/0000-0001-8721-0067 Furthermore, it should be noted that data concerning the number of infected patients in Italy from March 1 onward is not likely to T. Maria DeFeo https://orcid.org/0000-0002-9528-5859 https://orcid.org/0000-0002-5588-1306 https://orcid.org/0000-0001-6600-2998 be representative of the true number of cases, as testing was limited to only patients who were exhibiting symptoms. 5 | CO N C LU S I O N During the current ongoing outbreak of SARS-CoV-2 in Lombardy, Italy, there is a drastic decrease in the number of LTs performed. The main reasons behind this are the lack of ICU beds, organizational difficulties for ICU workers and concerns for infection in both patients and staff. On the basis of our results, this study has found no specific reason concerning the safety of liver recipients to stop LT programs. However, due to the complex circumstances which surround the viral outbreak, a rapid cessation or limitation of activity is often required pragmatically. Over the short follow-up period, the current survival of liver-transplanted patients during the coronavirus outbreak is quite good. However, the positivity of two patients after LT and the death of one of them, raises important questions regarding the facilitation of liver transplants during an outbreak. We suggest that only patients with true end-stage liver disease and extremely poor prognosis should undergo LT. We believe that COVID-19 protocols should include screening for both donors and recipients prior to LT. Testing both patient populations advocates not only for the safety of the recipients but also of the health workers too. BAL is the preferred method for recipient screening, either performed prior or immediately after the transplant procedure as this allows for rapid availability of reliable results. Different measures and precautions are to be taken in order to promote the safety of LT during the coronavirus outbreak. D I S C LO S U R E The authors of this manuscript have no conflicts of interest to disclose as described by the American Journal of Transplantation. DATA AVA I L A B I L I T Y S TAT E M E N T Data are available from the authors on request. ORCID Umberto Maggi Luciano De Carlis Daniel Yiu https://orcid.org/0000-0002-5337-2866 https://orcid.org/0000-0002-9133-8220 https://orcid.org/0000-0002-3677-7423 REFERENCES 1. CNT. Attività di donazione e trapianto di organi. http://www.trapi anti.salute.gov.it/imgs/C_17_cntPu bblic azioni_351_alleg ato.pdf. Published 2020. Accessed April 10, 2020. 2. CNT. Aggiornamento delle misure di prevenzione. http://www.trapi anti.salute.gov.it/imgs/C_17_cntAv visi_225_0_file.pdf. Published 2020. Accessed April 10, 2020. 3. Il_Sole_24_ore. Coronavirus, tutti i provvedimenti economici e sanitari varati dal Governo. https://www.ilsole24ore.com/art/elenco-provv edimenti-ADyvx9C. Published 2020. Accessed April 10, 2020. 4. AGI. Annuario Statistico del Servizio SanitarioNazionale. https:// www.agi.it/fact-check ing/news/2020-03-06/coron aviru s-posti -letto-ospedali-7343251/. Published 2020. 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