Over the last few decades, hematopoietic stem cell transplantation (HSCT) has become an established, life-saving, and a curative treatment option for many indications, including hematological disorders and malignancies, immunodeficiencies, and metabolic disorders, both for adults and children. However, serious complications accompany its use, making HSCT a complex procedure with a dual challenge: curing the underlying disease and preventing relapse, while on the other hand, controlling potentially severe complications [1, 2].
HSCT patients are known to have a very complex pharmacotherapy. Treatment should be undertaken in a specialized unit by a fully dedicated and experienced multidisciplinary team. To ensure safe and effective care and to prevent and solve drug-related problems, a collaboration between clinical pharmacists (CP), clinical pharmacologists (P), and other members of the multidisciplinary team is of paramount importance .
The role of CPs in HSCT has been recognized for years in many parts of the world, including Europe [3,4,5]. However, it was only recently (2015) that European pharmacists gained more visibility. This was mainly as their role was officially recognized by the FACT-JACIE International Standards for Hematopoietic Cellular Therapy Product Collection, Processing, and Administration [6, 7]. Since then, more and more European CPs have been appointed to HSCT wards, making the HSCT CP new in the field.
Recently, in April 2018, an official Pharmacist Committee has been launched as part of the European Society of Blood and Bone Marrow Transplantation (EBMT). Its aim is to establish, structure, and develop scientific and educational activities designed for both CPs and Ps involved in the field of stem cell transplantation and cellular therapy, and to provide a network for communication .
This position statement paper reflects the recommendations by the members of the EBMT Pharmacist Committee, in which both CP/Ps are represented. Recently, the American Society for Blood and Marrow Transplantation (ASBMT) Pharmacy Special Interest Group, published a recommendation of HSCT clinical pharmacists’ activities and responsibilities in the United States and comprehensively reviewed the underlying evidence .
Although the current EBMT pharmacist statements and activities are mainly in line with the recommendations of ASBMT, some differences can be observed, the most important difference being the incorporation of both CP and P in the EBMT Pharmacist Committee.
To our knowledge, the situation concerning CP/Ps is not the same everywhere in Europe, concerning the educational background, further training, and responsibilities: clinical pharmacists have a degree from a pharmaceutical faculty with continuing education in clinical and/or hospital pharmacy. Whereas pharmacologists may have a degree from a medical school and therefore are physicians, with further training in pharmacology in some European countries, while in others, both pharmacists and physicians can attain a clinical pharmacology degree. Therefore, the pharmaceutical and clinical background of the members of the EBMT Pharmacist Committee helps in this highly interdisciplinary environment of stem cell transplantation.
However, unlike in the United States, there is not (yet) specific training or licensing for transplant CP/Ps. In contrast to the United States, there are fewer clinical pharmacists available in Europe, and therefore the extent and distribution of tasks are not comparable.
Taken together, this paper is intended to give advice for the roles and responsibilities of transplant CP/Ps and to advocate for this role within European transplant centers.
General standards of practice for CPs and their competencies have been developed and refined [9,10,11]. Besides the exact description of fundamental, desirable, and optimal activities, generally accepted standards for qualification, professional development, and the proactive involvement in research and science are included. According to these recommendations, CPs should possess the “knowledge, skills, attitudes and behaviors necessary to deliver comprehensive medication management in team-based, direct patient care environments” . Furthermore, therapeutic drug monitoring (TDM) for drugs with a narrow therapeutic window is performed by CPs and/or Ps, depending on the country. Clinical pharmacologists are mostly involved in research and patient care.
To measure and assess the quality of clinical pharmacy services, key performance indicators for hospital pharmacists have been determined, aiming to advance clinical pharmacy practice and improve patient care .
Roles and competencies
An overview of roles and competencies, with a distinction between “mandatory” and “optional” for EBMT CP/P involved in HSCT, is presented in Table 1.
Clinical pharmacy services (CPS) in a hospital setting aim to optimize pharmacotherapy during the entire stay, as well as at the transitions of care. They therefore improve medication safety. Several studies, beginning in the early 1990s, have shown the positive effects of CPS, regarding clinical and economic impact [12,13,14,15,16,17,18,19,20].
The CP/Ps should be involved in all steps of patient care, beginning with the pre-transplantation workup and admission to the hospital, the inpatient stay, and discharge. The main focus lies on medication review with respect to the selection of the most appropriate drug in the right dose at the right time, with respect to the patient’s individual conditions, e.g., comorbidities, organ dysfunctions, age, weight, or patient preferences. Within these activities, the CP/P identifies, addresses, and documents drug-related problems, performs medication reconciliation at transitions of care, and performs or supervises TDM of drugs with a narrow therapeutic window. An integral part of the CP/Ps work is the regular participation in multidisciplinary ward rounds and meetings.
A comprehensive description of CP/Ps mandatory and optional activities within patient care is given in Table 1.
Clinical skills of CP/Ps may be formally defined in a collaborative practice agreement  or collaborative pharmacy practice agreement between CP/Ps and the physician, stating which permission CP/Ps have to advise, adjust, and discontinue therapies within the signed contract. Examples of some (or all) of the clinical activities are described in Table 1.
Hospital pharmacy services
“The overarching goal of hospital pharmacists is to optimize patient outcomes through the judicious, safe, efficacious, appropriate and cost effective use of medicines”. This can be thought of as using the “five rights”: the right patient, the right drug, the right dose, the right route, and the right time . To improve medication safety, a hospital pharmacy is engaged in all areas of the medicine-use process in hospitals, including the selection, procurement, distribution and organization of the administration of medicines, the production and compounding, as well as monitoring of patient outcomes and quality assurance .
In the context of HSCT, where hazardous and high-risk drugs are prescribed and administered, the hospital pharmacy plays an important role in the preparation of ready-to-administer drugs and in the provision of specific information for the use and administration of drugs. Apart from the broad armamentarium of highly specialized and personalized drugs used in conditioning regimens and supportive care, pharmacists are more and more faced with advanced therapy medicinal products (ATMP) in future in both clinical trial and patient care settings. Expensive ATMPs are licensed as medicines (like chimeric antigen receptor T cells, CAR T cells), so pharmacists need to understand how to handle them safely whenever applicable. In addition, knowledge on the prevention and handling of specific side effects related to their use is of paramount importance . This also demands the active involvement of hospital pharmacists in terms of legal, administrative, and logistic issues, as well as their safe preparation and administration .
The use of electronic computerized physician order entry (CPOE) combined with a clinical decision-support system (CDSS) has been shown to significantly reduce prescription errors—especially if these systems are linked to the electronic patient record with patient-specific information, e.g., diagnoses, laboratory and clinical results, age, or allergies . With the use of CPOE/CDSS, all healthcare professionals have a rapid and non-stationary access to the patient’s current medication and further comprehensive drug information, usually including an automatic check of the right dose, drug–drug interactions, or double prescriptions. The connection of the CPOE/CDSS to a patient–individual logistic by the hospital pharmacy (unit-dose supply) in terms of a closed- loop medication administration (CLMA) process further improves medication safety and facilitates the correct documentation of drug therapy. Preferably, CPOE is connected to validation, preparation, and administration of chemotherapy.
Process of care
According to their active role within the multidisciplinary team, as being responsible for the correct usage of medication, HSCT CP/Ps should develop local guidelines and standard operating procedures regarding drug therapy for HSCT patients. According to their education and training, as well as the desirable connection to the hospital pharmacy, HSCT CP/Ps provide ideal prerequisites for these activities.
Pharmacotherapy has a central and pivotal role in HSCT. A variety of drugs are used in the course of treatment, including drugs for conditioning, graft-versus-host-disease (GvHD) prophylaxis, and supportive care, such as anti-infective and immunosuppressive agents.
Drug research is essential to improve patient outcomes. Research in the areas of (clinical) pharmacology, drug safety, formulation of pharmaceutical preparations, pharmacoepidemiology, and economics contributed to safe, more effective, and cost-effective use of drugs.
In particular, clinical pharmacological studies can improve treatment outcomes in HSCT patients [24, 25]. Efforts have been made to optimize dosing of drugs used in the pre-, peri-, and post-transplant phase based on population–pharmacokinetic approaches [26,27,28,29,30]. For example, exposure of busulfan, anti-thymocyte globulin, and mycophenolic acid has been associated with clinical outcome [24, 26]. In addition, research on the occurrence of specific features in HSCT patients might help to identify and to diminish risk factors, as, for example, iron overload . These types of studies are the basis for individualized dosing to improve clinical outcome, and are an important step forward in the field of HSCT.
Drug exposures are variable between patients, resulting in unpredictable effects. Variables such as age, body size, organ function, concomitant medications, and genetic variations can affect drug exposure [28, 32,33,34,35,36]. As such, in patients, receiving the same drug in the same dose outcomes may differ, due to variability in pharmacokinetics (PK) and pharmacodynamics (PD). This may lead to toxicity or subtherapeutic effects, and may jeopardize the overall success of the HSCT procedure. Therefore, research on pharmacokinetics and pharmacodynamics, including exposure–outcome relationships of drugs used in HSCT should be highly encouraged and pursued by CP/Ps.
Implications for clinical practice
Knowledge on pharmacokinetics and pharmacodynamics has two clinical applications: individualized dosing and TDM. The most important difference is the need for taking blood samples from the patient in order to perform TDM. With individualized dosing, the dose is adjusted based on individual patient characteristics, such as body weight, organ function, or cell counts [35, 37, 38]. TDM adjusts the dose based on individual pharmacokinetics, which are calculated using concentration samples. Furthermore, individualized dosing and TDM can be combined for maximum control. For both, thorough information is needed on both the PK (dose–exposure) and the PD (exposure–effect). Both strategies increase precision in reaching optimal drug exposures and finally result in improved clinical effectiveness.
Implications for clinical trials
A harmonized trial design in HSCT is pivotal to be able to compare results between studies. Current pharmaceutical studies, investigating drug versus placebo, drug versus drug, or multiple doses of the same drug mostly compare fixed dosages. This also applies for most studies comparing conditioning regimens or GvHD prophylaxis. With known variability between patients in exposure and thus outcome after comparable dosages of the same drugs, it would be very helpful to investigate exposures to drugs in trials. For example, a recent study investigated anti-thymocyte globulin (ATG) in a fixed dose versus placebo. Post hoc analyses revealed that absolute lymphocyte counts (a known predictor for ATG clearance and thus exposure) statistically interacted with the use of ATG on overall and progression-free survival .
Education and training
HSCT CP/Ps must have adequate education and training in hematology, oncology (dependent on the setting in adults and/or children), and cellular therapies, apart from their basic training. In Europe, however, there is no formal or recognized education program for HSCT pharmacists so far. Many collegues rely on in-practice training, which is in contrast to the United States, where the American College of Clinical Pharmacy offers specific courses for clinical pharmacists, including the oncology area, and the Board of Pharmaceutical Specialties, which grants a level of accreditation for the oncology pharmacy practice. Regular attendance at specialist conferences should be undertaken to maintain current knowledge.
In general, CP/Ps are involved in teaching activities, especially in university centers, to physicians, nurses, pharmacy personnel, and students.
On admission and during their stay in the hospital, patients can be instructed on how to take/administer their drugs. Pharmacists can educate the patients and give explanations on the pharmacology (mechanism of action, how to identify side effects, and what to do if these occur after discharge). Medication charts can be provided to aid and increase patients’ compliance [3, 40]. This also includes education for long-term surivors on possible drug-related late effects.
Quality and process improvement
Since the sixth edition of the FACT-JACIE Standards, the key role of the pharmacist has been recognized . Pharmacists shall be licensed to practice in the jurisdiction of the clinical program. An overview of training and knowledge of designated pharmacists is provided in the accreditation manual (e.g., hematology/oncology patient care, including the process of cellular therapy, adverse reactions, therapeutic drug monitoring, and monitoring for and recognition of drug interactions and dose adjustments in the case of organ dysfunction). Pharmacists should also be involved in the development and implementation of controlled documents related to pharmaceutical management of patients with cellular therapy. CPs shall participate in educational activities for a minimum of 10 h in the field of cellular therapy annually. The pharmacist should be involved in preparing for, and maintaining accreditation, which encourages closer collaboration in delivering safe care to patients [3,4,5, 41].
The number of HSCT has dramatically increased in the last decade . HSCT is a relatively expensive procedure and has been reported to have a major impact on the total hospital costs. Post-transplant complications, such as opportunistic infections and severe GvHD, have been shown to be significant cost drivers . Given the rapidly increasing healthcare costs worldwide, cost-control measures are required to ensure sustainability of national health systems. HSCT CPs can play a significant role toward reducing healthcare costs, through cost avoidance and cost savings.
Common clinical activities, such as medication reconciliation, medication review, therapeutic drug monitoring, or adherence follow-up, can prevent medication errors and minimize adverse drug events, thus reducing the length of stay and preventing hospital readmission, while improving patient outcomes . Also, anticipating drug shortage and facilitating drug access, for example, for compassionate use or high-cost medication, participate in cost avoidance by reducing the length of stay and preventing delays in hospital discharge .
Cost savings can be achieved through various interventions, such as discontinuation of unnecessary drugs, modification of the route of administration, or switching to less-expensive alternatives. CPs should participate in antimicrobial stewardship, which has a great potential for cost savings . In addition, they should be involved in decision-making of drug formularies and drug-utilization policies. CPs are well positioned to discuss pharmacoeconomic data, and favor the most cost-effective medicines. Unfortunately, pharmacoeconomic analyses remain scarce in the HSCT population, except for antifungal therapies  and stem cell mobilization protocols . As cost-effectiveness may differ depending on the population treated , CPs should be involved in cost-effectiveness studies specific to the transplant population. Finally, they should conduct pharmacoeconomic studies to demonstrate the positive impact of their interventions on both clinical and economic outcomes, and to support the expansion of clinical pharmacy within HSCT units.
The roles and competencies described above outline the knowledge and skills of CP/Ps involved in HSCT. This position statement paper reflects the recommendations by the members of the EBMT Pharmacist Working Committee and highlights the roles and competencies of clinical pharmacists and pharmacologists involved in HSCT.
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Members of the EBMT Working Group are listed at the end of the paper.
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Langebrake, C., Admiraal, R., van Maarseveen, E. et al. Consensus recommendations for the role and competencies of the EBMT clinical pharmacist and clinical pharmacologist involved in hematopoietic stem cell transplantation. Bone Marrow Transplant 55, 62–69 (2020). https://doi.org/10.1038/s41409-019-0538-9