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Effect of COVID-19 Pandemic on Hematopoietic Stem Cell Transplant Activity: Experience of a JACIE-Accredited Center

Objectives: The adoption of international quality and accreditation standards is important for the success of transplant centers. Guidelines from the Joint Accreditation Committee ISCT-Europe and EBMT (JACIE) have enabled quality management of the operations of clinical units of cellular therapy centers, including cell collection and processing, thus minimizing errors and adverse events. COVID-19 has had significant implications for immunocompromised patients, particularly hematopoietic stem cell transplant recipients, as well as their donors and caregivers. Here, we retrospectively examined measures, taken in our transplant center in Turkey during the pandemic period between March 2020 and October 2021, to investigate how JACIE accreditation has affected patient, donor, product, and employee safety.
Materials and Methods: We analyzed data on transplant activity, as well as donor, patient, product, and employee safety, during the pandemic in 3 separate 6-month periods. The measures were analyzed starting from March 2020, when the first COVID-19 case was seen in Turkey.
Results: Since the beginning of the pandemic, 140 patients have undergone stem cell transplant in our center. Stem cell transplant was delayed in 22 patients because of the pandemic. Transplant was also postponed due to COVID-19 positivity in 6 patients, and 2 patients died due to COVID-19 infection during the transplant process. Unrelated donor activity continued to be performed safely throughout this period. COVID-19 infection developed in 12 of the 52 personnel working in the bone marrow transplant unit, one of whom needed intensive care due to severe pneumonia. In terms of quality management activities, the impact of the pandemic was greatest during the first month.
Conclusions: Results from our retrospective study examining the impact of JACIE accreditation in a stem cell transplant center during the COVID-19 pandemic showed that, when national and international guidelines are followed, JACIE accreditation can facilitate adaptation to changing conditions in transplant centers.

Key words : Cellular therapy, Infection, Safety


COVID-19 is a respiratory illness caused by a new coronavirus that was first detected in Wuhan, China during December 2019. COVID-19 quickly spread throughout China, and then worldwide, and was declared a pandemic by the World Health Organization in March 2020.1

There are no specific clinical features to reliably distinguish COVID-19 from other viral respiratory infections. In the initial cases, the most common symptoms were fever (98%), cough (76%), myalgia or fatigue (44%), and shortness of breath (in about half of the patients).2 In most people, COVID-19 is asymptomatic or mild, although some people experience a severe course ranging from pneumonia to acute respiratory failure and death. The severity and mortality of COVID-19 have been shown to be associated with cardiovascular diseases, diabetes, hypertension, chronic lung and kidney diseases, and cancers. The fatality rate is higher in people with comorbid conditions.2,3

Stem cell transplantation is a curative treatment option in many diseases. In recent years, the discovery of new drugs, developments in apheresis technology, and tailoring of treatment regimens according to the disease, patient, and transplant type have increased the success of transplant procedures. Factors important for the success of transplant centers include the adoption of international quality and accreditation standards.4 International standards in this field have been established under European Union directives.4-8 The institution that ensures the application of these standards is the Joint Accreditation Committee of the International Society of Cell and Gene Therapy (ISCT)-Europe and the European Society for Blood and Marrow Transplantation (EBMT) (JACIE). The primary aim of JACIE is to ensure high-quality, continuously improving patient care in transplant centers and to improve the performance of laboratories in terms of hematopoietic stem cell collection and processing, through an internationally accepted system.4-8 In 2012, our center became the first accredited stem cell transplant center in Turkey, and our second accreditation was obtained in 2016. An application was made for a third accreditation in May 2020, but this was delayed by the COVID-19 pandemic.

In this study, we examined the measures taken in our transplant center during the pandemic period between March 2020 and October 2021 to investigate how JACIE accreditation has affected patient, donor, product, and employee safety.

Materials and Methods

Study plan and analysis of the impact of the COVID-19 outbreak
This was a single-center multidisciplinary, retros-pective, cross-sectional clinical study approved by the COVID-19 Scientific Research Committee of the Ministry of Health (SB 2021-03-10T11_05_07) and by the Non-Interventional Research Ethics Committee of Baskent University (KA 21/215).

The measures taken in our stem cell transplant center to ensure patient, donor, stem cell product, and employee safety were analyzed in 6-month periods, starting from March 2020 when the first COVID-19 case was seen in Turkey. The first 6 months between April and September 2020 were defined as the first period, the second 6 months between October 2020 and March 2021 were defined as the second period, and the third 6 months between April and October 2021 were defined as the third and last period.

Transplant frequency and outcomes were evaluated in each period, along with disease types and COVID-19 positivity (on polymerase chain reaction [PCR] tests) and death rates. The precautionary measures taken for health care personnel working in the bone marrow transplant unit, compliance of personnel with these measures, and number of personnel who had COVID-19 (and their clinical status) were also analyzed.

Disease groups
Clinical severity of disease was classified as follows:9 (1) asymptomatic disease included patients with positive PCR test but no symptoms consistent with COVID-19; (2) mild illness included symptomatic patients (such as fever, cough, sore throat, headache, myalgia, nausea, vomiting, diarrhoea, and loss of taste and smell) who met the COVID-19 case definition criteria but had no dyspnea or radiological abnormality; (3) moderate disease included patients with pneumonia (evidence of acute respiratory failure during clinical evaluation or imaging, along with oxygen saturation ≥94% in room air); (4) severe illness included patients with severe pneumonia (oxygen saturation <94% in room air, PaO2/fraction of inspired oxygen <300 mm Hg, respiratory frequency >30 breaths/min, or lung infiltrations >50%); and (5) critical illness included patients with respiratory failure, septic shock, and/or multiorgan dysfunction.

Precautions for COVID-19 infection
Following the announcement of the first case in Turkey, the Pandemic Committee, which includes specialists in infectious diseases, chest diseases, emergency services, and intensive care, as well as hospital managers, was established in March 2020. In line with the recommendations of the hospital Infection Control and Pandemic Committees, training was organized for health care workers, who were divided into 2 teams to avoid interrupting the patient transfer process. Nonurgent stem cell transplantations postponed, and the risks of the pandemic were explained in detail to patients in the process of being transplanted; a separate consent form was signed for this aspect.

In addition to the existent infection control policy of our hospital, we established protocols to guide patients and staff in terms of preventing the transmission of COVID-19. As early as January 2020, the infection control team initiated daily monitoring of COVID-19 status. At the time of hospital admission, patients were screened in the doctor’s office using a standardized questionnaire, and those considered at risk for COVID-19 infection were transferred to a designated temporary quarantine area.

Based on the EBMT Working Party recom-mendations for acute myeloid leukemia (AML), all patients were screened for COVID-19 infection before starting chemotherapy. A risk-benefit assessment was performed for each patient to determine transplant suitability. Before deciding on allogeneic stem cell transplant, we discussed the indications on a case-by-case basis (Figur 1).

In the clinical unit, patients were initially admitted to negative pressure rooms. Patients with negative PCR tests were taken to transplant rooms, and hospital visits were restricted. Caregivers were not permitted to attend to hospitalized patients except in cases of medical necessity; in such cases, the number of caregivers was limited to one. Caregivers were informed about the precautions and rules related to COVID-19 (Figur 1). Inpatients, attendants, and health care workers were evaluated daily for COVID-19 symptoms. Posters about COVID-19 and the associated measures were placed in visible areas within the hospital. Training on infection control training was provided to all personnel (doctors, nurses, and cleaning staff) working in the hematology service, bone marrow transplant unit, and hematology laboratory during the COVID-19 pandemic. Training was provided at regular intervals according to national and international guidelines (Figur 1).

Face-to-face meetings were postponed, and essential meetings were held online. Telemedicine (ie, phone appointments) was used for nonemergency outpatient visits. Meetings intended to convey information to patients and donors were held online (via Skype, Teams, or Zoom) for some of the consent procedures (Figur 1).

Workers in the hematology service, bone marrow transplant unit, and hematology laboratory and apheresis workers were evaluated daily for COVID-19 symptoms, and PCR testing was performed weekly during periods when the pandemic intensified (Figur 1). Even if they had no symptoms, all health care workers who tested positive were placed in home quarantine for 14 days, except for bone marrow transplant center employees, who were quarantined for 21 days. In addition, all related and unrelated donors had to test negative for COVID-19 before health assessments and mobilization could begin.

A board was established by the hospital for the management of COVID-19-positive patients, and pandemic polyclinic, pandemic service, and inten-sive care units (ICUs) were treated as separate areas. A service-level agreement was signed between the stem cell transplant center and pandemic service (Figur 1). This agreement stated that a situation risk assessment was to be made by considering the presence of symptoms and time of the last contact of a patient transferred from the outpatient clinic or emergency department. Every symptomatic patient and donor were to be transferred to the pandemic outpatient clinic to provide samples (Figur 1).

Patients followed in the transplant polyclinic were to be sent to the pandemic outpatient clinic to be evaluated, and all necessary tests were to be performed when COVID-19 was suspected. Verbal and written communications necessary to distinguish these patients from other patients, and to give them priority, were to be provided by the transplant doctor.

If hospitalization of a suspected COVID-19 patient was necessary, the patient was to be admitted to the pandemic service until the PCR result was obtained and clinical suspicion was eliminated. In this process, the transplant doctor was to contribute to the follow-up and treatment of the patient through constant communication with the doctor of the pandemic service via telemedicine.

Any patient whose PCR test result was negative was to be transferred to the clinical unit for bone marrow transplant, and follow-up and treatment should be continued. Patients diagnosed with COVID-19 and treated in the pandemic service were to be transferred to the transplant unit after 2 consecutive negative results were obtained at least 14 days later, with an interval of 1 week.

Recover after transplant and rehabilitation at home were facilitated via telehealth, enabling early discharge from the hospital if it was considered that the patient would be safe and well-supported at home.

Molecular testing The collection of samples from patients under investigation for COVID-19 was based on the Centers for Disease Control and Prevention Interim Guidelines for Collecting and Handling of Clinical Specimens for COVID-19 Testing.10 Viral RNA was extracted from samples according to the manufacturer’s instructions. The EZ1 Advanced XL platform (Qiagen) was used for automated viral nucleic acid extraction processing, and the Rotor-Gene Q thermal cycler platform (Qiagen) was used for PCR assay runs. The Bio-Speedy R COVID-19 RT-qPCR Detection Kit version 2.0 (Bioeksen R&D Technologies), a reverse transcriptase-PCR kit, was chosen by the Turkish Ministry of Health and used throughout the COVID-19 pandemic.11

Data safety and management
Data of patients and donors were collected using the hospital information management system software Nucleus (version 9.30.11; Monad Software). The PCR products were accessed using Turunç version 1 software. The accuracy of all data was checked by a data control group established in accordance with JACIE.

Statistical analyses
This was a descriptive study, and frequency analyses were performed. Descriptive results were given as number of patients (%). Analyses were performed using SPSS software (version 25.0; IBM Corp).


Transplant activity and cellular therapy candidates
During the first 3 months of the pandemic, stem cell transplants were postponed, except for emergencies, according to the Ministry of Health and EBMT guidelines. Since the beginning of the pandemic, 140 patients had received stem cell transplants. There were 39 transplants (27.9%) in the first 6 months of the pandemic, 52 transplants (37.1%) in the second 6 months, and 49 transplants (35.0%) in the last 6 months. Of total transplants, 82 (58.6%) were autologous and 58 (41.4%) were allogeneic stem cell transplants.

Of the 20 patients whose transplant procedures were delayed in the first period, 12 patients (60%) were diagnosed with sickle cell anemia, 4 (20%) with myeloma, and 4 (20%) with lymphoma. No patient had their transplant delayed due to the pandemic in the second or third period.

However, transplant was delayed in 2 patients with AML who had positive COVID-19 PCR tests before transplant. One of these patients was in complete remission at the 4-month follow-up posttransplant, but the other patient died due to disease relapse 6 months posttransplant.

Another patient with a diagnosis of AML in the first period of the pandemic underwent transplant from a sibling donor. COVID-19 was diagnosed 12 days after the transplant. The patient was treated in the ICU for a diagnosis of severe pneumonia and was discharged after recovery. The patient was in complete remission at the first year follow-up posttransplant.

A patient with AML who had a stem cell transplant from a fully matched sibling donor died in the ICU as a result of severe COVID-19 pneumonia after the transplant. In the third analysis period, planned transplants were postponed in 2 patients with positive COVID-19 PCR results, as the preparation regimen could not be started.

Donor evaluations
Donor work-up, physical examinations, and mana-gement procedures required numerous adjustments due to the pandemic. In our center, bone marrow collection processes were suspended for 1 year, spanning the first and second periods of the pandemic. Only peripheral blood stem cells were collected from all donors during the first year of the pandemic. Polymerase chain reaction testing was performed in all donors before their health examination and on the day before mobilization. Stem cell collection was performed in donors whose COVID-19 PCR test was negative. With the use of stem cell apheresis methods, 55 (33.3%) peripheral blood cell collections were performed in the first period, 64 (38.8%) in the second period, and 46 (27.9%) in the third period. Unrelated stem cell collections continued through local (Turkey Stem Cell Coordination Center) and international registries. Between April 2020 and October 2021, work-up procedures for 136 unrelated donors were completed in our center with stem cells and cellular products delivered. Because of the uncertainty experienced in the first months of the pandemic, the stem cell products were delivered by pilots instead of couriers, particularly for international collections. This was recorded as a “planned deviation” from the relevant standard operating procedure. Stem cell collection was postponed for 1 month in a donor who had been prepared for nonrelative stem cell collection because of development of COVID-19.

To ensure that transplant activity was not interrupted, in accordance with our quality standards, the procedures for obtaining consent from donors were performed online, particularly in the first period. Through this method, informed consent was obtained from 7 donors.

Bone marrow transplant unit staff and visitors
During the pandemic, there were 52 staff members working at the bone marrow transplant center. In the first 6 months of the pandemic, 10 personnel were diagnosed with COVID-19, including 1 doctor, 2 nurses, 4 processing unit biologists, 1 apheresis unit technician, and 2 secretaries. One person developed severe pneumonia and needed intensive care. After the launch of the vaccination program by the Ministry of Health, the entire bone marrow transplant team was vaccinated with 2 doses of inactivated vaccines, followed by 2 doses of mRNA vaccines. After receiving all 4 doses of vaccine, 1 doctor and 1 apheresis unit employee were diagnosed with the COVID-19 delta variant. No bone marrow transplant center employee was absent as a result of COVID-19 infection.

Visitors were denied entry to the transplant unit, except for a single caregiver with a negative test, for severe patients. No changes in the patient’s relative caregiver were allowed during follow-up. Despite all the precautions taken, COVID-19 developed in 1 person accompanying an AML patient, and the patient died from severe infection.

Stem cell products
During the pandemic, in cases of allogeneic transplant from related donors, no cellular products were frozen to prevent possible cell losses. In the first period, no patient underwent an unrelated transplant. An unrelated transplant was performed in 3 patients with AML during the second period. The stem cell product of 2 of these 3 patients was cryopreserved and stored after being delivered by an international courier. In the third period, unrelated transplants were performed in 9 patients; none of the products were cryopreserved, and all products were infused fresh into the patient without freezing.

Quality management and accreditation activities
In terms of quality management activities, the impact of the pandemic was greatest during the first month. Weekly apheresis unit meetings could not be held in the first 3 months. Later, online meetings were held. Quality management meetings were postponed. Training could not be held in the first 3 months, but training activities resumed thereafter. In the first period, audit activities were completely suspended, such that internal and external audits could not be performed. In the second period, internal and external audits resumed. Although our center applied for a third JACIE accreditation, the onsite audit could not be undertaken. The compliance of both parties with the service-level agreement between the bone marrow transplant center and pandemic services was regularly audited (Figur 1).

During the period when all personnel of the cell processing unit were ill, support was received from other hospital personnel, deviating from the standard operating procedure for the transfer of basic products to the clinical unit. However, there were no adverse events related to the transfer of these products to the transplant unit.


The COVID-19 pandemic is still ongoing, and the ultimate global effects are unknown. Similar to the rest of the world, health authorities in Turkey have taken a series of measures to combat the pandemic. Despite all of the precautions taken, however, the numbers of confirmed cases and patients in need of intensive care treatment are of concern.2,3,12-14 In our hospital, a series of measures was adopted, including those prescribed generally by the Ministry of Health and others specific to our hospital.

JACIE develops and maintains global standards for the provision of quality medical and laboratory practices in cellular therapy. Based on these standards, JACIE offers accreditation to transplant programs to encourage health institutions and facilities to establish and maintain quality management systems for all of their activities and to engage in continuous improvement.4,15-17 The primary aim of the JACIE is to promote high-quality patient care and laboratory performance in terms of specimen collection and processing in transplant centers through an internationally recognized system of accreditation.15-17 Our adult stem cell transplant center is licensed by the Ministry of Health and is one of the few centers in the world to have JACIE reaccreditation.

Implementation of international quality standards in the field of cellular therapies will reduce negative impacts of critical processes on patients, donors, and products in the face of changing environmental conditions.18,19 The aim of our study was to analyze how accreditation affected the stem cell transplant processes of a clinic affected during a global pandemic that has had devastating consequences. To our knowledge, this single-center study is the first to report the effects of JACIE accreditation on clinical practice during a pandemic.

Soon after the World Health Organization declared COVID-19 a pandemic, the first cases were reported in Turkey.1 The national lockdown in our country only lasted for 3 months. Transplant activity was also interrupted during the panic, and uncertainty was experienced in all countries during their national lockdowns.20

Although the aim of this study was not to compare the transplant activity of our center with the period before the pandemic, a decrease in stem cell transplant activity was nevertheless noted, particularly in the first few months of the pandemic, due to postponement of transplants for many nonemergency patients. The guidelines of the EBMT regarding the pandemic were considered,21 and transplant was therefore avoided, particularly in patients with malignancies such as multiple myeloma and lymphoma and in patients with nonmalignant diseases such as sickle cell and aplastic anemia. Planned transplants from unrelated donors were also suspended. The national lockdown started in mid-March 2020 and persisted for 3 months, as stated above. With the decrease in the number of cases after the general closure (from the beginning of summer 2020), transplant activity restarted in our center. In addition, after vaccinations started in January 2021, our transplant center activity has also started to increase despite ongoing uncertainty regarding the duration of the pandemic, with the necessary precautions being taken.

The Baskent University Adana adult bone marrow transplant center started accreditation activities in 2010 and was awarded JACIE accreditation for the first time in 2012. The advantages of JACIE accreditation experienced by our transplant center for nearly 10 years, including during the pandemic period, are summarized in Table 1.

The socioeconomic difficulties created by the COVID-19 pandemic, extreme fragility of patients with hematological diseases, and existence of complex treatment processes have made it very difficult to provide services in the field of stem cell transplantation.22,23 Regardless of the level of developments in technology and scientific research, the health care capacity will be negatively affected during a pandemic, in particular emergency services, intensive care, and the service bed capacity of hospitals, which may become insufficient due to the increased wave of patients. Measures must also be taken so that other health problems are not neglected. These difficulties have been experienced by both middle-income countries and economically strong countries, all of which have been strongly affected by the pandemic.

The most important limitation of this study was the absence of a control group. Obviously, comparing our results with a non-JACIE accredited center or comparing the period before and after JACIE accreditation in the same center while the pandemic is ongoing could provide much more reliable infor-mation. Although many transplant centers in Turkey have made efforts to achieve JACIE accreditation, only 2 centers maintain this accreditation. Because of the lack of another accredited transplant center in Adana, Turkey, where our hospital is located, we reported study data from our center only.

There are many studies on how JACIE accreditation of centers that provide bone marrow transplant procedures affects their success.15-17 JACIE ac-creditation provides centers with flexibility in extraordinary situations, such as pandemic conditions. In this study, we share our best cellular therapy practices and management during a pandemic (Figur 1). We believe that the results of our study can serve as a guide for cellular therapy centers aiming to adopt a quality management system. We also believe that having JACIE accreditation in bone marrow transplant centers can keep all units operating under pandemic conditions.24


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DOI : 10.6002/ect.2022.0107

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From the 1Department of Physiology Department, the 2Adana Adult BMT Center, the 3Department of Infection Disease and Clinical Microbiology, the 4Department of Chest Diseases; the 5Department of First and Emergency Aid, the 6Department of Family Medicine, the 7Department of Biostatistics; and the 8Department of Microbiology, Baskent University Medical Faculty, Adana, Turkey
Acknowledgements: The authors have not received any funding or grants in support of the presented research or for the preparation of this work and have no declarations of potential conflicts of interest.
Corresponding author: Ilknur Kozanoglu, Baskent University Adana Dr. Turgut Noyan Research and Training Hospital, Hematology Laboratory, 01250, Adana, Turkey