Review Article

J Oncol Pharm Practice

2021, Vol. 27(3) 679–692
Impact of clinical pharmacy in oncology ! The Author(s) 2020
Article reuse guidelines:
and hematology centers: A systematic sagepub.com/journals-permissions
DOI: 10.1177/1078155220976801
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Cynara S Oliveira1, Mauriele P Silva1, Íngara K S P B Miranda1,

Rodrigo T Calumby2 and Renata F de Ara
ujo-Calumby1,3

Abstract
Background: Oncology and hematology is a complex and specific area that requires monitoring by a multidisciplinary
team capable of personalizing the treatment of each patient. Clinical pharmacy services have the potential to contribute
significantly to the effective and economical care of cancer patients.
Objective: To evaluate, synthesize and critically present the available evidence on the impact of the Clinical Pharmacy in
the treatment of patients with hematological cancer.
Method: A review was carried out on the bases PubMed/MEDLINE, LILACS and Google Scholar. The included studies
were: studies that evaluated the effects of pharmaceutical interventions in clinical in oncology and hematology services
and having as a population patient with hematological cancer.
Results: 17 studies were selected among 745 identified. 4.771 patients were included, with an average follow-up time of
15.3 months. Patients affected by some type of hematological cancer, undergoing chemotherapy treatment, showed
better adherence and continuity when accompanied by a clinical pharmacist, added to this professional in carrying out
interventions, provides control of symptoms such as cancer pain, nausea and constipation and, thus, contributes to
decrease the length of hospital stay.
Conclusion: The implementation of a Clinical Pharmacy service in oncology and hematology centers contributes
significantly to the effectiveness of pharmacotherapeutic treatment, treatment costs reduction, safety increase in the
use of medications and the patient’s quality of life.

Keywords
Hematology, oncology, clinical pharmacy, pharmaceutical care, drug-related problem
Date received: 27 May 2020; revised: 2 November 2020; accepted: 3 November 2020

Introduction
Cancer is one of the leading causes of death and dis-
ability in the world. Hematological Malignancies (HM)
represent an important group of tumors originating
from mutations in cells of the hematological tissue or
in the Lymphatic System. The three main types of HM
1
are: Leukemia (originating in the bone marrow and Department of Health, Pharmacy College, Unidade de Ensino Superior
de Feira de Santana – UNEF, Feira de Santana, Brazil
divided into myeloid or lymphoid); Lymphoma 2
Department of Exact Sciences, University of Feira de Santana, Feira de
(which do not originate from the lymphatic system Santana, Brazil
and are divided into Hodgkin and non-Hodgkin); 3
Federal University of Bahia – UFBA, Salvador, Brazil
and Multiple Myeloma (developed from plasma
Corresponding author:
cells).1 Worldwide estimates of HM incidence and mor- Renata F de Ara
ujo-Calumby, Av. Lu
ıs Eduardo Magalh~aes, Suba
e, Feira de
tality in 2018 were: Leukemia (437.033 new cases and Santana – BA 44079-002, Brazil.
309.006 deaths); Hodgkin’s Lymphoma (79,990 new Email: farm.renata@hotmail.com
680
cases and 26.167 deaths); Non-Hodgkin’s Lymphoma
(509.590 new cases and 248.724 deaths); and Multiple
Myeloma (159.985 new cases and 106.105 deaths).2
The oncology and hematology is a complex area in
healthcare that requires monitoring by a multidiscipli-
nary team capable of personalizing the treatment for
each patient. Therapeutic choices will depend on the
patient’s disease and clinical aspects such as age, pres-
ence of other diseases and ability to tolerate chemo-
therapy. There are many therapeutic protocols, which
include the association of chemotherapeutic agents,
immunotherapeutic agents, radiotherapy and, in some
cases, bone marrow transplantation.3,4 Most of the
antineoplastic drugs used in these protocols have high
toxicity and narrow therapeutic indexes, requiring dose
adjustments and supportive care to control infectious
and hemorrhagic complications. Beyond it, some
patients do not respond to treatment or are unable to
adhere to treatment.5,6
The oncology pharmacist plays an essential role in
the treatment of clinically complex patients.7,8 The
main contributions of clinical pharmacists in assisting
onco-hematological patients include: evaluating the
medical prescription regarding quantity, quality, com-
patibility, stability and interactions; supportive care
management, such as managing anti-infectious thera-
pies; assistance in the transition of care; evaluation of
patients regarding the toxicity of chemotherapies and
treatment effectiveness, in addition to tracking iatro-
genic effects; educating patients, caregivers, as well as
health professionals and interns; monitor, evaluate and
report results related to treatment to help improve clin-
ical practice.9–13 Such activities are essential to promote
patient safety when using antineoplastic agents and to
avoid unnecessary expenses with the use of ineffective
drugs for the patient or hospitalizations caused by
complications resulting from medication errors that
could be avoided.14–16
The implementation of a clinical pharmacy service
in oncology care units has been described as an impor-
tant strategy for reducing incorrect prescriptions, drug
interactions, negative effects, in addition to reducing
the number of hospitalizations and, consequently,
treatment costs and negative impacts on the patient’s
life and health.17,18 In the onco-hematology context,
many works have evaluated the impact of clinical phar-
macy services based on several outcome measures.
However, in current literature, there is an absence of
evidence-based research that analyzes and summarizes
clinical studies which assessed the impact of the clinical
pharmacy service in onco-hematology centers. To
address this gap, the objective of this work was to eval-
uate, synthesize and critically present the available evi-
dences of the impact of the Clinical Pharmacy in the
treatment of patients with hematological cancer.
Journal of Oncology Pharmacy Practice 27(3)
Materials and methods
Search strategy
The research question was formulated based on the
PICO strategy: population, intervention, control and
outcome.19 The following aspects were considered: i)
patients with hematological cancer; ii) the practice of
pharmacotherapeutic monitoring by pharmacists as the
intervention of interest; iii) not performing the service
as baseline; and iv) the results of the applied interven-
tions as outcome. Hence, this systematic review was
guided by the following question: What is the impact
of the implementation of Clinical Pharmacy services in
onco-hematology centers?
The PROSPERO and Cochrane databases were
used to identify any relevant systematic reviews on
the field. A comprehensive literature search was per-
formed using the PubMed/MEDLINE, Latin
American and Caribbean Literature in Health
Sciences (LILACS) and Google Scholar databases
from July 1999 to May 2020. Additional articles were
identified from the reference lists of the included stud-
ies. The research strategy included the use of terms:
{“Clinical Pharmacy” OR “Pharmaceutical care” OR
“Pharmacotherapeutic Follow-up”} AND
{{“Oncology” AND “Hematology”} OR “Onco-
hematology”}.
Selection criteria
The articles were considered for the study based on the
following inclusion requirements: i) original research
articles (e.g., regarding randomized controlled trials,
non-randomized controlled studies, cohort studies,
cross-over studies, and before-and-after studies) pub-
lished between 1999 and 2019; ii) published in
Portuguese, Spanish or English; iii) having evaluated
a clinical pharmacy service at an onco-hematology
center; and iv) having patients with hematologic
cancer as a population. The exclusion requirements
were: i) studies that did not consider the treatment of
onco-hematologic tumors; ii) articles with study
designs out of interest such as cases studies and litera-
ture review.
Data collection and analysis
The screening for the selection of eligible articles was
carried out considering the titles and abstracts to iden-
tify and exclude those that presented out of scope
methodological approaches, study interruption, results
without statistical data, or that dealt with themes
repeated by other articles as in literature reviews. The
articles of interest were tabulated by chronological
order of publication and type of study, in addition to
Oliveira et al. 681

specifying the sub-types of onco-hematological cancer,
country of origin and venue of publication.
The articles were investigated according to the out-
comes, such as: Drug-Related Problems (DRPs) and
interventions, humanitarian impacts (improvement of
quality of life and patient education and counseling)
and economic impacts (reduction of hospitalization
costs and cost of inappropriate therapies). All findings
were considered by three independent reviewers to
ensure consistency in execution of the review process.
Results
Study characteristics
By using the selected search terms, 745 articles were
found. Based on the inclusion and exclusion require-
ments adopted, 17 papers were selected for analysis.
The selection of the papers found, according to the
PRISMA protocol – Preferred Reporting Items for
Systematic reviews and Meta-Analysis), is outlined in
Figure 1. Table 1 provides a summary of the character-
istics of the selected studies and the main results
achieved in each of the studies.
The selected studies were carried out between 1999
and 2020 and evaluated patients of different national-
ities, such as: United States (n ¼ 5); Canada (n ¼ 3);
Spain (n ¼ 2); France (n ¼ 2); Singapore (n ¼ 1);
Taiwan (n ¼ 1); Morocco (n ¼ 1); Finland (n ¼ 1)
and Brazil (n ¼ 1). Few studies have presented
detailed patient1999 and 2020 and evaluated patients
of different nationalities, such as: United States
(sel3 months, ranging from 1 to 72 months. The
age of the patients was 0.6 to 63.9 years. Notice that
four studies did not report the age or other clinical
characteristics of the patients. The main types of
tumors presented by the patients being monitored
were: Chronic Myeloid Leukemia (CML) and
Lymphomas.
The selected studies had the common purpose of
describing and evaluating the impact of clinical phar-
macy services in onco-hematology clinics, but they also
discussed: the patients’ needs related to medications;
the role of the clinical pharmacist in the onco-
hematology service; the contributions of implementing
a face-to-face and remote pharmaceutical care model;
the adverse drug reactions; the medication adherence
profile and the patients’ quality of life and economic
impact of clinical pharmacist intervention.

Total articles found (n = 2217)

IDENTIFICATION

PubMed/MEDLINE LILACS Google scholar

(n = 1148) (n = 5) (n = 1220)
SCREENING

Records screened on titles and abstracts

(n = 74)

Inclusion criteria: (i) an original full-text article published between

1999 and 2020; (ii) be published in Portuguese, Spanish or
English; (iii) to have evaluated a clinical pharmacy service at an
oncology and hematology center (iv) to have patients with
hematological cancer as a population
ELIGIBILITY

Articles selected according inclusion criteria (n = 30)

Exclusion criteria: (i) articles repeated or that were not presented

with the researched theme: (ii) studies that did not consider the
treatment of onco-hematological tumors: (iii) articles with study
INCLUDED

designs that do not fit the proposals, such as cases and review
studies.

Articles selected for this systematic review (n = 17)

Figure 1. PRISMA flow for study selection through literature search in this work.
Table 1. Summary of the characteristics of controlled studies included in the systematic review.
Study year/country Study design (duration)
Taylor et al., 1999, Prospective impact
Canada26 assessment study
(3 months)
Shah, Dowell, Retrospective impact
Greene,2006, USA6 assessment study
(12 months)
Prot-Labarthe et al., Prospective impact
2008, Canada29 assessment study
(1 month)
Valgus et al., 2011, Prospective descriptive
USA20 and qualitative study
(18 months)
682
Patients Objectives Main clinical outcomes
58 Characterize the drug- During the study, 58 pediatric patients went to the Clinical Pharmacy service
related requirements of during the 12-month period of the study, aged 0.7–17.5 years (mean
patients with hemato- 9.4 years). The patients followed up were diagnosed with: acute lym-
logical tumors and phoblastic leukemia, acute non-lymphoblastic leukemia, non-Hodgkin’s
describe the pharma- lymphoma and chronic myeloid leukemia. The evaluation of pharmaco-
ceutical role in a pedi- therapy performed by pharmacists resulted in the identification of 165
atric hematology clinic. DRPs, of which 84% were potential DRPs, 91% in transplant patients. The
main causes of the identified DRPs were: safety due to the prescription of
a very high dose for the patient (27.1%); effectiveness by prescription of
very low dose for the patient (31.7%); and indication for untreated health
condition (13.6%) and adherence (11.6%).The interventions performed by
the pharmacist to solve or avoid problems related to medications were:
dose adjustment (31.7%); prescription of drugs prophylaxis of infections
and replacement of electrolytes (15.8%), in addition to educational actions
and strategies for promoting therapeutic adherence (13.6%).
423 Document and evaluate The study included 228 patients, an average of 35 patients per month, by a
the services of a hema- pharmacist, over a period of one year. The main adverse reactions pre-
tology/oncology clinical sented and monitored by pharmacists were: anemia, pain control, con-
pharmacy in the outpa- stipation/diarrhea and nausea / vomiting, responsible for 78% of the total
tient clinic. support care issues addressed. In addition to skin toxicity, nephrotoxicity,
infection, insomnia, mucositis, increased glucose levels and allergies,
thrombocytopenia and edema. 308 drug interventions were verified, 50%
related to care care and 32% to chemotherapy, including the addition of
drugs (41%), discontinuation of medication (23%), dose adjustment (21%)
and laboratory monitoring (10%).
29 Describe pharmacist During the study, 29 patients went to the clinical pharmacy service with
interventions in a mean age of 12.1 years. The patients followed up were diagnosed with:
hematopoietic stem cell acute lymphoblastic leukemia (34.5%) and Hodgkinia, pain control, con-
transplant pediatric stipation/diarrhea and nausea / vomiting, responsible for 78% of the total
unit. suppor, 23.8%), failure to receive drug or improper administration (89,
17%), untreated indication (92, 17.5%), subtherapeutic dosage (57, 10.9%),
supratherapeutic dosage (65, 12.4%) and drug without indication (76,
14.5%). In the study, 525 pharmaceutical interventions were collected
mainly regarding dose adjustment (33.1%) and drug monitoring (25.1%).
89 Describe the develop- For one year, the service monitored 89 patients, 186 interventions and 136
ment, implementation prescriptions. The most common interventions were dose adjustment,
and initial experience indication of medication, discontinuation of inappropriate medication for
with a program provid- the patient and management of adverse reactions (anemia, pain, consti-
ing clinical pation or diarrhea, nausea and vomiting) and patient education and
(continued)
Journal of Oncology Pharmacy Practice 27(3)
Table 1. Continued.
Study year/country Study design (duration) Patients Objectives Main clinical outcomes
pharmaceutical services
in hematology-oncology
clinics at a university
hospital.
Chan et al., 2012, Retrospective cohort 116 Describe services and The supportive health care developed by pharmacists were: use of granu-
Singapore25 study (12 months) research activities con-
ducted by clinical phar-
macists from a
lymphoma team will be
discussed.
Delpeuch et al., 2015, Prospective descriptive 489 Document and evaluate During the study, 489 adult cancer patients were followed up (mean
France5 and qualitative study the role of clinical
(6 months) pharmacy services in a
hematology/oncology
Department.
counseling. The focus of counseling was to promote therapeutic adher-
Oliveira et al.
ence and provide information to the patient on: ways of using therapeutic
agents, prevention and management of expected adverse effects, as well
as on the dangers, signs and symptoms of thrombosis. Thus, 63 educa-
tional interventions were performed and more than half the interventions
aimed at the use of antiemetics and the resolution of dosage calculation
errors and adjusting pain control regimes.
locyte stimulating factors for (prevention of febrile neutropenia caused by
myelosuppression resulting from the use of chemotherapy); use of pro-
phylactic antiemetics (to improve quality of life and prevent unnecessary
hospitalizations); prevention of tumor lysis (oncological emergency of fatal
potential caused by electrolyte disorders and renal dysfunction); thera-
peutic monitoring of high-dose drugs (such as methotrexate); improving
the use of resources; controlled infusion of drugs (such as rituximab for
the purpose of minimizing the risks of adverse reactions) and safety in the
use of drugs to prevent DRPs. Another fundamental care developed by
pharmacists was the management and evaluation of drug interactions
between chemotherapeutic agents and the use of alternative and com-
plementary therapies, such as the use of teas and herbal medicines. Most
of the interventions performed were on issues related to chemotherapy,
optimization of the use of antimicrobials and supportive care therapies.
Thus, as a result, pharmacotherapy was optimized (33.9%), followed by
the resolution of drug-related problems (26.2%) and improved workflow
(10.2%).
age ¼ 63 years). During the study period, 552 drug-related problems were
identified, including: inappropriate medication (20.6%), untreated indica-
tions (14.8%), drug interactions (14.3%), inadequate administrations
(14.1%), inadequate administrations (14.1%), underdosing (11.7%), lack of
monitoring (9.6%), overdose (8.9%), administration omissions (3.5%) and
side effects (2.5%). Interventions (n ¼ 552) led to treatment discontinu-
ations (26.2%), dose adjustments (21.5%), addition of drugs (16.9%),
alternative routes of administration (11.7%), substitution from one med-
ication to another (10.7%), therapeutic drug monitoring (10.3%) and
optimization of administration (2.6%). The majority (96%) of the inter-
ventions were accepted and implemented by the medical team. Most
drug-related problems involved anti-infective agents, while very few
concerned anti-cancer drugs. Thus, the integration of the clinical phar-
macist in an oncohematology department resulted in specific drug
683
(continued)
Table 1. Continued.
684

Study year/country Study design (duration) Patients Objectives Main clinical outcomes

interventions for 12.6% of prescriptions for adult patients hospitalized

Ribed et al., 2015, Prospective cohort study 249 Develop and evaluate a 249 patients participated in the study, who were evaluated in three clinical
Spain17 (6 months) comprehensive phar-
maceutical care pro-
gram for cancer
outpatients treated
with oral antineoplastic
agents.
Ruiz, Lemus, Prospective descriptive 16 Describe the implementa- The 16 patients selected to undergo pharmacotherapeutic follow-up, of
Echeverria, 2015, and qualitative study tion of a new model
Spain18 (51 months) face to face and remote
pharmaceutical care
with home delivery of
tyronsine kinase inhibi-
tors medicines for
patients with chronic
myeloid leukemia.
Lam, Cheung, 2015, Retrospective descriptive 56 Evaluate the impact of an The pharmacist helped promote adherence (88.6%) and results by building a
USA21 and qualitative study oncology pharmacist-
(72 months) managed oral antican-
cer therapy program on
oral medication adher-
ence in CML patients
versus usual care.
Kekale, Peltoniemi, Propective cross-sectional 120 Evaluate adverse drug This study evaluated 120 patients with CML, with a mean age of 57.8 years
Airaksinen,2015, study (6 months) reactions experienced
Finland22 by CML patients during
per oral tyrosine kinase
inhibitor treatment and
correlation of ADR
with cancer.
interviews over 6 months. Thus, during this period 275 medication errors
were recorded, with 362 interventions performed by the pharmacist.
There was a significant increase in therapeutic adherence in the group of
patients followed and the patients indicated a degree of satisfaction of
81.8% when asked about the services provided in the implemented
Pharmaceutical Care program.
which 5 of these patients choose to make contact by e-mail and 11 by
phone. This flexibility allowed us to pay attention focused on the patient’s
quality of life with continuous pharmaceutical monitoring, which made it
possible to detect interactions, problems related to drugs and the man-
agement of therapeutic adherence individually. On the other hand, the
monthly delivery of the medicine at home allowed to optimize the avail-
able resources of the pharmacy service, such as physical storage space and
improvement in the management of salaries.
close and trusting relationship with the patient and family, generated
through the implementation of the treatment plan, which consists of a
visit with a pharmacist oncology, where the patient will receive educa-
tional information about the disease and medications, enabling them to
identify, solve and prevent problems. Assistance to patients is also pro-
vided via e-mail and telephone call, facilitating access to guidelines, and
thereby reducing rates of non-adherence to treatment, which is one of
the main factors that contribute to treatment failure. The pharmacist
performed a continuous follow-up of 56 patients, a total of 567 phar-
maceutical interventions were documented based on a review of 3432
pharmacist meetings of 56 patients over a 6-year period. Thus, monitoring
and managing side effects (16.8%), detecting drug interactions (19.2%),
dose adjustment (14.5%), laboratory monitoring (35.3%), therapeutic
indication for untreated condition (13.1%) and others (1.2%).
and 52% were male. From the total number of patients evaluated, 97%
reported being suffering from at least one adverse reaction, which had a
negative influence on daily activities and treatment, thus, low adherence
to treatment with Imatinib in patients with CML is linked adverse reac-
tions. Among the adverse effects, the most cited were cramp (80%),
(continued)
Journal of Oncology Pharmacy Practice 27(3)
Table 1. Continued.
Study year/country Study design (duration) Patients Objectives
symptoms with medi-
cation adherence and
perceived quality of life.
Farias et al., 2016, Prospective impact 185 Implement a clinical phar-
Brazil27 assessment study macy service focused
(24 months) on the comprehensive
review of antineoplastic
drugs used in therapy of
hematological diseases.
Defoe, Jupp, Leslie, Prospective descriptive 272 Describe key activities
2017, Canada28 and qualitative study performed by a newly
(4 months) deployed clinical phar-
macist in an outpatient
pediatric hematology,
oncology, transplant
clinic.
Lucena et al., 2018, Retrospective descriptive 114 Determine risk criteria
USA30 and qualitative study specific to the malignant
(2 months) hematology and bone
marrow transplant
patients and to evaluate
the different types and
severities of interven-
tions made by
pharmacists.
Main clinical outcomes
edema (69%) and fatigue (50%). More than half of the patients felt that
Oliveira et al.
ADRs had a negative influence on their daily quality of life. A quarter of
the patients reported that the symptoms had a negative influence on
mood, general condition or pleasure in life. Patients who felt that their
symptoms negatively affected their quality of life suffered from an average
of eight different symptoms.
185 patients and more than 13 thousand prescriptions were followed, with a
106.5% increase in the detection of DRPs. The main underlying diseases of
patients with DRP were non-Hodgkin’s lymphoma, multiple myeloma and
acute lymphoid leukemia - possibly associated with the complexity of
their treatment regimens - and the main drugs related to DRP were
methotrexate, cyclophosphamide, cytarabine, asparaginase and filgrastim.
Thus, the majority of DRPs in both periods were considered clinically
significant (58% in the period without the Clinical Pharmacy service and
71% with the Clinical Pharmacy service) and among the main character-
istics of the DRPs, the adjustment of dose, duration treatment and dilu-
tion / concentration of the manipulated medication. Pharmacists
intervened mainly during the study by performing dose adjustment, drug
suspension, alteration of diluents / concentration of the manipulated drug,
and inclusion of drug therapy.
During the study, pharmacists treated 272 patients and recorded 1021
interventions such as medication review, advice, usage guidelines and
laboratory monitoring. It was also possible to observe a considerable
increase in the number of medication reconciliation performed (400%), in
the provision of adherence assistants for patients and their families
(132%) and adherence assessments (122%). Clinical pharmacists have
demonstrated an in-depth understanding of treatment regimens, and
among other interventions, can review medications with patients, manage
therapeutic drugs, identify drug interactions, help with treatment adher-
ence, provide medication advice, and thus identify and address some
barriers.
114 patients were included with a total of 793 interventions over the
duration of the study. Among the patients, 80 were identified as in high
risk and 34 as not in high risk. There were more interventions docu-
mented upon admission in the high-risk group (73 interventions) com-
pared with the not high-risk group (31 interventions). However, in a per
patient analysis, there was a similar number of interventions in both
groups. Specifically for the high-risk patients, there were a total of 326
interventions, with 21 of them made upon admission and 305 made during
hospital stay. In this case, the most common interventions were: thera-
685
peutic regimen change (36%), therapy discontinuation (16%), and
(continued)
Table 1. Continued.
686

Study year/country Study design (duration) Patients Objectives Main clinical outcomes

monitoring (16%). Beyond it, medication histories corresponded to only

5% of the interventions and the authors concluded that it suggests that
pharmacists may need to focus more on assessing and intervening on
patients. Moreover, interventions related to medication history were the
most prevalent upon admission (71%), while the most frequent during the
hospital stay were those related to modifying a therapeutic regimen
(38%), discontinuing therapy (16%), and monitoring (16%).
Chen, Wu and Huang Retrospective impact 1443 Evaluate the clinical and After the implementation of the Clinical Pharmacy service, the average
2019, Taiwan24 assessment study economic impact of hospitalization time decreased from 19.27 to 16.69 days. 826 pharma-
(12 months) clinical pharmacist ceutical interventions were performed which was significantly higher than
intervention in a hema- the period before the involvement of the clinical pharmacist
tology unit. (p < 0.00001). Among the active recommendations, there were recom-
mendations for the primary prophylactic use of posaconazole for patients
with acute myeloid leukemia undergoing remission-inducing chemother-
apy. As a result of these medication order interventions, detected pre-
ventable adverse events increased from 58 in the year prior to the
involvement of the clinical pharmacist to 230 thereafter. Moreover, the
cost savings was 5.75 times higher than the estimated before the intro-
duction of the service.
Wind et al., 2020, Retrospective impact 28 Implement and optimize a The plan-do-study-act (PDSA) quality improvement technique was imple-
USA31 assessment study pilot transitions of care mented to prospectively measure the success of interventions related to
(7 months) model for scheduled the improvement of service process transitions that occurred in various
chemotherapy admis- stages, including the development of standardized operational proce-
sions in patients with dures, electronic documentation medical records and education for the
hematologic multidisciplinary group of malignant hematology. Inadequate prescription
malignancies. of prophylactic antimicrobials and discharge antiemetics occurred for 78%
and 44% of patients, respectively. In addition, three PDSA cycles were
conducted resulting in improvements in multiple aspects such as: com-
munication regarding status of benefits investigations performed for
specialty medications prior to admission, resolution of these benefits
investigations at various time points, improvement in efficient use of the
electronic medical record for chemotherapy orders, and patient instruc-
tions for appropriate use of prophylactic antimicrobials.
Gr
egori et al., 2020, Retrospective qualitative 558 Evaluate clinical and finan- A total of 1970 interventions were performed corresponding to an average
France23 and descriptive study cial impact of pharma- of 3.5 interventions/patient. The main DRPs were: contra-indication/non-
(12 months) cist interventions in an conformity to guidelines (98, 15%), dosage problem (90, 14%), drug
ambulatory adult interaction (80, 12%) and improper prescription (78, 12%). The main
hematology-oncology interventions adopted were: Discontinuation or refusal to deliver (256,
department. 39%), dddition of a new drug (196, 30%), dose adjustment (95, 15%) and
(continued)
Journal of Oncology Pharmacy Practice 27(3)
Oliveira et al. 687

The selected studies presented different methodolog-

reduction was e390,480. The cost-benefit ratio of the clinical pharmacist

mainly: untreated indications (31.3%); overdose (17.1%); drug interactions

implemented by the team had a significant clinical impact on the patient:

88 (19.6%) with a very significant clinical impact and 71 (15.8%) with a
optimization of the dispensing/administration mode (52.8%). The cost

(12.4%) and underdosage (11.1%). The majority (98%) of the changes

ical designs, which made it difficult to match the results

The study included 526 patients. The pharmacist identified 450 DRPs,
and compare the reported outcomes. Most of the stud-
ies (n ¼ 9) were prospective. The studies had as meth-
odological design: the qualitative and descriptive
analysis (n ¼ 8), the impact assessment (n ¼ 6), the
cohort analysis (n ¼ 2) and the cross-sectional
approach (n ¼ 1).
All studies used the identification of DRPs and the
evaluation of the performed interventions as clinical
outcome measures. In addition, three studies
approached the humanistic impacts20–22 and two of
them discussed the economic impacts of interventions
was e3.7 for each euro invested.

carried out by pharmacists.23,24

Pharmacist intervention for Drug-Related problems

potential vital impact.
Main clinical outcomes

(DRPs)
All studies have shown that in the pharmacotherapy
assessment process, the identification of DRPs was
essential to ensure patient safety when using medica-
tions. Pharmacists have played a key role in evaluating
therapeutic outcomes, promoting therapeutic adher-
ence and identifying DRPs.
The pharmacotherapy evaluation performed by
pharmacy services in an

pharmacists resulted in more than 3,000 therapeutic

oncology department.
Document and evaluate

interventions and in the identification of approximately

the role of clinical

1,500 DRPs. The most frequently reported DRPs

regarded: safety, due to adverse reaction to the medi-
cation, very high dose prescription or drug interactions;
Objectives

effectiveness, by underdosing or lack of monitoring;

indication, for untreated health condition or adher-
ence.5,6,17,18,20–22,25–28
To handle or avoid DRPs, the main reported inter-
Patients

vention performed by the pharmacist was optimization

of administration,5,21,22,26,29 including: dose adjust-
526

ment; prescription of drugs; prophylaxis of infections;

replenishiment of electrolytes; substitution of medica-
tion; and therapeutic monitoring. The integration of
Study design (duration)

Retrospective observa-

the clinical pharmacist in an onco-hematology depart-

ment resulted in beneficial interventions to guarantee
safety in the use of medication for 12.6% of the pre-
(12 months)
tional study

scriptions of adult patients hospitalized with cancer.5

In that work, most DRPs reported involved anti-
infectious agents, while quite a few were related to anti-
neoplastic therapy.

Treatment adherence and education for Self-Care

Moukafih et al., 2020,
Table 1. Continued.
Study year/country

The implementation of a clinical pharmacy service in

onco-hematology clinics has contributed to the promo-
Morocco32

tion of therapeutic adherence and education for self-

care. The focus of counseling was to promote therapeu-
tic adherence and provide information on: ways of
using therapeutic agents, prevention and management
688
of expected adverse reactions, and the dangers, signs
and symptoms of thrombosis.
In this context, the work in20 carried out 63 educa-
tional interventions, which more than half were direct-
ed to the use of antiemetics, the resolution of dosage
calculation errors and to the adjustment of pain control
regimens. These interventions contribute to the individ-
ualization and monitoring of therapeutic regimes.
Additionally, it also benefits both the patient and the
health service by reducing hospitalization time and
unnecessary expenses, and helping to achieve the
goals established by the multidisciplinary team.
The treatment adherence of patients with chronic
myeloid leukemia who received Imatinib was described
in the study in.21 They reported that the pharmacist
helped promote adherence (88.6%) and better results
by building a close and trusting relationship with the
patient and family, through the implementation of a
treatment plan. It consisted of an appointment with
an oncology pharmacist, where the patient received
educational information about the disease and medica-
tions, enabling them to identify, solve and prevent
problems. The assistance to patients was also carried
out via e-mails and telephone calls, facilitating access to
guidelines, and thereby reducing treatment non-
adherence rates, which is one of the main factors that
contribute to the failure of therapy.
Another study was carried out in Finland, between
2012 and 2013, in eight hospitals with the aim of eval-
uating the Adverse Drug Reactions (ADRs) experi-
enced by patients with chronic myeloid leukemia
during oral treatment with tyrosine kinase inhibitor.
The authors reported that More than half of the
patients felt that ADRs had a negative influence on
their quality of life. Moreover, a quarter of the patients
reported that the symptoms had a negative influence on
mood, general condition or pleasure in life. Beyond it,
patients who felt that their symptoms negatively affect-
ed their quality of life suffered from of eight different
symptoms on average.22
Economic impact of pharmacist interventions
Two studies demonstrated that, after the introduction
of Clinical Pharmacy services at Oncology and
Hematology Centers, there was a significant increase
in interventions to reduce medication errors, prevent-
able adverse drug events and medication costs. In a
study carried out in France23 in 2020, the value repre-
sented by deprescriptions and exchanges for less expen-
sive drugs was e185,508. In turn, the value represented
by the addition of medicines and the replacement by
more expensive ones was e9,945. Beyond it, 109 (6%)
of all interventions regarded the revision of immuno-
therapy or chemotherapy regimen resulting in the
Journal of Oncology Pharmacy Practice 27(3)
reduction of e148,032 (84% of the total cost savings).
The total cost reduction represented ss expensive drugs
was e185,508. In turn, the value represented by the
addition of medicines and th average annual savings
produced a net benefit of e223,021 and the cost-
benefit ratio was . The total cost reduction represented
ss expensive drugs was
In another study carried out in Taipei24 in 2019,
reported that, after the implementation of the clinical
pharmacy service, the average hospitalization time
reduced from 19.27 to 16.69 days compared to the
period before the implementation of the service.
Thus, the cost savings was 5.75 times (NT$250,280a)
the estimated before the introduction of the service
(NT$37,080) by considering the switch from parenteral
to oral medications (main contributor) despite only
decreasing doses or frequency of medication.
Reviewed study limitations
The most common limitations of the selected studies
were: the small number of patients, unpaired distribu-
tion among the study groups, lack of standardization
of the instruments used to assess quality of life and the
incidence of adverse reactions, the short period of time
of evaluation. Moreover, the differences in methodol-
ogies hardened the pairing between studies for the
meta-analysis. These factors can result in low represen-
tativeness of the population and statistical and data
interpretation errors.
Discussion
Our findings represent unprecedented results in rela-
tion to the clinical outcomes of patients with hemato-
logical tumors that were evaluated by clinical
pharmacists, the role of the pharmacist in onco-
hematology services and the corresponding economic
impacts for the organizations. The selected articles
demonstrated significant impacts on health care for
patients with hematological tumors. It highlights the
importance of including the pharmacist in the assis-
tance team in the outpatient, hospital or community
environment. It allows addressing fundamental care
for the drug therapy management and monitoring for
the patients, detecting possible adverse reactions and
drug interactions.
Most of the studies selected in this review described
mainly the types of DRPs found as an indicator of the
pharmacy practice.5,6,20,26,27,32 Few studies have
reported the clinical outcomes of the identified DRPs,
the humanistic17,22,28 and economic
outcomes. 20,21,23,24,26,28
The selected studies described a large number of
DRPs identified. The work in27 reported that the
Oliveira et al.
detection and prevention of DRPs increased 106.5%
compared to the period when the clinical pharmacy
service was not offered to patients. The main underly-
ing diseases of patients with DRPs were: non-
Hodgkin’s lymphoma, multiple myeloma and acute
lymphoid leukemia. The related DRPs can be associat-
ed with the complexity of the treatment regimens and
the main drugs associated were: methotrexate, cyclo-
phosphamide, cytarabine, asparaginase and filgrastim.
Most DRPs in both periods were considered clinically
significant. The pharmacists intervened mainly during
the study of dose adjustment, suspension of drugs,
alteration of diluents/concentration of manipulated
medication and inclusion of drug therapy.
The hematological system is one of those affected by
the toxicity of the chemotherapy treatment. As
reported in the selected work, the main ADRs identi-
fied by pharmacists and responsible for 78% of the
interventions, were: anemia, constipation/diarrhea
and nausea/vomiting.6 In addition, the studies also
reported skin toxicity, nephrotoxicity, infection, insom-
nia, mucositis, increased levels of glucose, allergies,
thrombocytopenia and edema.5,6,20,26,27
The supportive health care conducted by pharma-
cists were: use of granulocyte-stimulating factors for
prevention of febrile neutropenia (caused by myelosup-
pression due to chemotherapy); use of prophylactic
antiemetics (to improve quality of life and prevent
unnecessary hospitalizations); prevention of tumor
lysis (potentially fatal oncological emergency, caused
by electrolyte disturbances and renal dysfunction);
therapeutic monitoring of high-dose drugs such as
methotrexate; controlled infusion of drugs such as rit-
uximab (for minimizing the risk of adverse reactions);
and safety monitoring in the use of drugs to prevent
DRPs. Additional fundamental care developed by
pharmacists were the management and evaluation of
drug interactions between chemotherapeutic agents
and the use of alternative and complementary thera-
pies, such as teas and herbal medicines. Hence, as a
result, pharmacotherapy optimization occurred
(33.9%), followed by the resolution of DRPs
(26.2%).25
The Clinical Pharmacy services contributed to the
individualization and monitoring of therapeutic
regimes, in addition to benefiting both the patient
and the health service by reducing hospitalization
time and unnecessary expenses. Consequently, it
helped achieving the goals established by the multidis-
ciplinary team.20,23,31
A study was carried out in Spain on a Clinical
Pharmacy service for patients with Chronic Myeloid
Leukemia, in which the patient received the medication
at home. It was focused on the quality of life, detection
of interactions and DRPs and the management of
689
adherence therapy individually. The monthly delivery
of the drugs at home allowed to optimize the available
resources of the pharmacy service, such as storage
space and improved management of expiration dates.
At the end of the study period, all participants contin-
ued to be monitored by the service.18 In a similar study,
carried out in the USA, the pharmacist helped in pro-
moting adherence (88.6%) and in the results by build-
ing a relationship of proximity and trust with the
patient and his family, generated through the imple-
mentation of a health care plan. It consisted of a visit
with an oncology pharmacist, where the patient
received information about the disease and medica-
tions, enabling them to identify, solve and prevent
problems.21
The assessment of ADRs experienced by patients
with CML and the correlation of ADR symptoms
with medication adherence and perceived quality of
life was described in a study conducted at eight hospi-
tals in Finland. The study reported 97% percent of
patients were suffering from at least one ADR.
Although, no correlation was found between adherence
and ADRs, half of the patients felt that ADRs had a
negative influence on their quality of life, affecting their
mood, general state or the pleasure of life.22
The research carried out by Ribed and collabora-
tors17 revealed the positive impact of Clinical
Pharmacy services for outpatients who indicated a
degree of satisfaction of 81.8% when asked about the
services provided in the implemented Pharmaceutical
Care program.
Drug reconciliation has been described as an impor-
tant tool in the clinical pharmacy. A study carried out
in Canada demonstrated a significant increase in the
number of medication reconciliation (400%), assis-
tance to patients and their families to promote therapy
adherence (132%) and adherence assessments
(122%).28
Clinical pharmacists have demonstrated an in-depth
understanding of treatment regimens and, among other
interventions, worked on reviewing medication, man-
aging therapeutic drugs, identifying drug interactions,
helping with treatment adherence, and providing med-
ication advice. Although specific data on the clinical
relevance of interventions conducted by pharmacists
have not been collected, the study demonstrated that
the integration of clinical pharmacists in an interdisci-
plinary clinic can improve patient safety in the use of
drugs, in addition to contributing to the reduction of
adverse events, hospitalization occurrences, and hospi-
talization time.21,27,28
The impact of an oncology pharmacist extends
beyond individual patient care, indirectly affecting
patient outcomes through activities such as the devel-
opment and implementation of safety guidelines and
690
policies for the use of medicines.19,33,34 As observed in
the literature described here, the implementation of a
clinical pharmacy service in oncology care units pro-
moted the reduction of errors resulting from incorrect
prescriptions, drug interactions, side effects, in addition
to reducing the number of hospitalizations and, conse-
quently, treatment costs and negative impacts on
patient’s life and health.35–39 In addition, the relation-
ship and trust between pharmacist and patients under-
going onco-hematology treatment was expanded,
through the practice of pharmaceutical care, positively
contributing to the quality of life of patients. Hence, it
allowed the increase of satisfaction, adherence to treat-
ment and the continuous expert guidance on the cor-
rect use of prescribed antineoplastic agents, as well as
the control of side effects and possible
interactions.17,18,40
In summary, the studies have reported the clinical
activities developed by pharmacists, such as: medica-
tion reconciliation, patient education, and economic
assessments, which are fundamental activities for pro-
moting patient safety when using medications.
Moreover, the studies discussed here presented results
that directly impacted the quality of health care, as well
as the quality of life of patients and the reduction of
treatment costs. Finally, the studies reported improve-
ment of symptoms in subsequent clinical appointments
(after intervention by the pharmacist), of therapeutic
adherence and in the prevention of DRPs.
Some limitations were found in the execution of this
review such as: i) the publication bias that can affect
the selection process of articles, since no study was
identified to show the negative impact of clinical phar-
macy services; ii) the selection bias, given some studies
might not be indexed in the researched databases; and
iii) it was not possible to carry out a quantitative sum-
mary analysis of the data due to the heterogeneity of
the population, interventions and results of the selected
studies.
Conclusions
In view of the evidences found in studies carried out in
different countries, the practice of Clinical Pharmacy
and Pharmaceutical Care has shown that cancer
patients accompanied by a clinical pharmacist,
showed higher adherence to treatment, control of
symptoms (e.g, cancer pain, nausea, constipation),
improvement in the quality of life, as well as in the
reduction and/or solution of DRPs. To the best of
our knowledge, this study is the first systematic
review that summarizes the different studies that deal
with the impacts of Clinical Pharmacy services in assist-
ing patients with onco-hematologic cancers.
Journal of Oncology Pharmacy Practice 27(3)
In general, the studies included in this review, con-
ducted in diverse places and contexts, concluded that
Clinical Pharmacy services contributed to the individ-
ualization and monitoring of therapeutic regimes. In
addition, it also contributed to the patient and the
health service by reducing hospitalization time and
unnecessary expenses, helping to achieve the goals
established by the multiprofessional team. Another rel-
evant care developed by pharmacists was the manage-
ment and evaluation of drug interactions between
chemotherapeutic agents and the use of alternative
and complementary therapies, such as teas and herbal
medicines.
Finally, we suggest that future longitudinal studies
can be carried out in order to clarify the impacts of
Clinical Pharmacy and Pharmaceutical Care on the
survival and quality of life of patients with onco-
hematological cancers. Such studies would be impor-
tant to describe the long-term results of Clinical
Pharmacy services.
Acknowledgements
The authors thank Caroline Argolo Brito Oliveira and
Lorena Silva Oliveira Nunes for the comments and sugges-
tions on the preliminary version of this work.
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
Funding
The author(s) received no financial support for the research,
authorship, and/or publication of this article.
ORCID iD
Renata F de Ara

ujo-Calumby https://orcid.org/0000-
0003-2475-5953
Note
a. NT$: New Taiwan Dollar.
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