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Do patients on oral chemotherapy have sufficient knowledge for
optimal adherence? A mixed methods study
European Journal of Cancer Care (Accepted October 2015)
A. Arber, A. Odelius, P. Williams, A. Lemanska, S. Faithfull
University of Surrey, Guildford, UK
ABSTRACT
A new treatment paradigm has emerged with many patients now receiving oral
chemotherapy as first line treatment for cancer. Treatment with oral chemotherapy
has resulted in reduced hospital costs, more autonomy for patients but with added
responsibilities for patient self-management.
Little is known about patient’s
knowledge following patient education to enable optimal adherence with oral
chemotherapy. A mixed methods study was carried out using a self-report
questionnaire to patients on oral chemotherapy for multiple myeloma followed by
semi structured interviews with patients at home. Analysis identifies high rates of
adherence (92.2%) with oral chemotherapy for multiple myeloma.
However
statistically significant knowledge deficits were identified, which were related to
patient ethnicity and to gender.
There is the potential for non-intentional non-
adherence with oral chemotherapy due to deficits in knowledge of oral chemotherapy.
Support at home needs to include primary care practitioners such as GPs, practice
nurses and pharmacists so that timely support is easily accessible especially in the
early phase of treatment.
Keywords: Patient information, Haematopoietic, oral chemotherapy
1
INTRODUCTION
As a result of innovative research in molecular biology and pharmaceutical advances
intravenous chemotherapies are now available orally to be used at all stages of cancer
treatment. Furthermore the use of long term oral maintenance therapy has contributed
towards cancer being managed as a chronic disease (Weingart et al. 2008). Systemic
anti cancer treatments taken orally offer a new treatment paradigm, which has resulted
in patients receiving outpatient ambulatory treatment, reducing hospital costs,
promoting autonomy and improving patient’s quality of life and survival (Regnier
Denois et al. 2011, Simonchowitz et al. 2010, O'Neill and Twelves 2002; De Mario
and Ratain 1998). Patients understandably prefer oral agents to intravenous therapy as
long as effectiveness is assured. Treatment with oral chemotherapy (OC) allows for
more freedom and the risks associated with venous access and intravenous infusion
devices are reduced (Liu. et al. 1997; Oakley et al. 2010). Nonetheless some patients
find the responsibility involved in self-management worrying and the reduced
opportunities for face to face communication with health care professionals is a
concern (Liu. et al. 1997). There are some risks with OC such as non-intentional
overdose and non-intentional non-adherence with therapy (Weingart et al. 2008).
However little is known about adherence and some studies provide conflicting
evidence (Chau et al. 2004; Hartigan 2003). Suboptimal adherence is reported as a
barrier to effective use of OC and addressing adherence is a priority when preparing
patients for treatment (Partridge et al. 2002).
There is a lack of consensus about safe medication practices and patient education for
OC, particularly information giving practices and monitoring of adherence (Weingart
et al. 2007). Standards related to information giving may not be consistent and it is
not known to what extent patient education strategies such as patient diaries are used
2
(Oakley 2005; Skalla et al. 2004). With the increased success of treatment for cancer
and the emergence of cancer as a chronic illness, personalized information is
considered important. Effective provision of information is essential so that OCs are
optimally adhered to and treatment remains optimal. Furthermore information
provision and care should be coordinated over time and continued through the care
pathway to care at home (Thorne et al. 2013). Managing OC at home requires a
transfer of treatment related work from healthcare professionals to patients which is
termed ‘self care’ and self-management (McCoy 2009). The patient autonomy
element of self-care requires responsible and safe practice from the patient to
manage the medications and communicate in a timely way with health professionals
when problems arise. For example providing a clear description of side effects and
symptoms and issues with adherence to the clinical team. So that treatment risks are
monitored and toxicities safely managed. Therefore patients including their carers
should understand how to administer the dosing schedule, how to adhere to the dosing
schedule and know when to report problems and complications such as toxicities to
clinical staff (Hartigan 2003; Oakley et al. 2010).
Patient education about OC usually occurs during a single hospital visit prior to
commencing treatment. During this hospital visit a great deal of information is
provided face to face by medical staff supported by clinical nurse specialists as well
as the provision of written information (Chau et al. 2004, Oakley 2005). In this
article the focus is on information provision for patients with multiple myeloma
(MM). Although MM is a relatively rare cancer the current gold standard antimyeloma treatment is with oral medications: namely Cyclophosphamide,
Thalidomide and Dexamethasone referred to as CTD. Oral agents targeting myeloma
cells are highly effective, and have contributed to myeloma becoming a chronic
3
disease which is treatable but not curable (Morgan et al. 2006). Furthermore the
survival rate for those with multiple myeloma over 5 years is increasing at the fastest
rate of all cancers in the UK (Cancer Research UK 2014). Younger patients have a
better prognosis than those who are older and MM is twice as common in black
people as in white people and Asians. The aim of the study was to identify patient’s
knowledge of their OC medications their adherence with their medication and to test
for relationships between age, gender and ethnicity in relation to knowledge of CDT.
METHODS
This is a mixed methods study consisting of a patient survey (n=64), and interviews
with two patients taking CDT. Self-report questionnaires (n=64) were given to
patients who were taking CTD therapy by clinical nurse specialists in three out-patient
clinics. The questionnaire had four sections related to confidence in taking oral
chemotherapy, knowledge of side effects of oral chemotherapy, knowledge of when
to take oral chemotherapy, what to do if side effects occurred and what to if a dose of
OC was missed. Demographic information was also collected. The questionnaire had
15 questions 13 of which were fixed choice with 2 open ended questions related to
satisfaction with written and verbal information giving. The in-depth interviews were
introduced later in the research process to further explore issues emerging from the
patient survey such as the practical aspects of managing the medications at home at a
distance from the hospital. Two patients who had completed survey questionnaires
agreed to be interviewed. The interviews were conducted around two main themes:
‘meaning of the illness and treatment’ and ‘information and support’. The two
patients (one male and one female) were recruited through one of the clinical nurse
specialists and were identified as the only patients with myeloma who were well
4
enough to be approached at the time, which also reflects the generally small
population of patients with myeloma. Both patients were interviewed in their homes
and as it turned out both patients had experienced problems in managing their dosing
schedule at home.
Data analysis of the survey was conducted using IBM SPSS version 22.0 (Armonk
NY). Statistical tests were used to explore associations between each of the scores
from questions derived from the knowledge related sections and demographic
features: gender, age, and ethnic group. To compare the difference in terms of their
knowledge scores in the subgroups of patients Kruskal Wallis, Mann-Whitney U-test
and Chi-square tests were used. The interviews were transcribed verbatim. Both
transcripts were coded manually and independently by two researchers using “a
general inductive approach” ( Thomas 2006: 237).
Ethical approval for the study was obtained from the University of Surrey Advisory
Committee on Ethics, as well as from the National Research Ethics Service (NRES)
and the lead Comprehensive Local Research Network (CLRN) with sign off from the
three haematological centres involved in the study.
The aim of the study is to understand how knowledgeable patients are in relation to
their OC medications and to understand the significance of age, gender, ethnicity and
adherence behaviours in relation to knowledge of CDT.
RESULTS
Data analysis is based on 64 returned questionnaires from three research sites and two
patient interviews. A summary of the demographic details of patients participating in
the survey is presented in Table 1. The sample was broadly representative of the age
range of the population affected by MM in the UK with most patients aged over 60
5
years (48, 75%). Black ethnicity is another risk factor for MM and 23.4% of patients
came from ethnic minority backgrounds including black Caribbean, black African,
Pakistani and Bangladeshi. Myeloma is twice as common in black people as in white
people and Asians (Cancer Research UK 2014). Most of the patients with non-white
ethnicity were from one hospital site (site 1).
Table 1 Patient demographics survey questionnaire
Patient Demographic information
Site
Site 1
Site 2
Site 3
Gender
Male
Female
Missing
Age
<60
≥60
Missing
Ethnicity
White British
Other
No. (%) (n= 64)
33 (51.6)
23 (35.9)
8 (12.5)
32 (50.0)
22 (34.4)
10 (15.6)
15 (23.4)
48 (75.0)
1 (1.6)
49 (76.6)
15 (23.4)
There were three acute hospitals with haematology out-patient clinics taking part in
the study. One hospital was in an inner city area and two were in suburban locations.
33 patients were from site 1, 23 patients were from site 2 and only 8 patients were
from site 3. Site 1 was an inner city hospital site with a very busy clinic seeing many
more patients than site 2 and 3 which were in suburban areas. Site 1 had the largest
proportion of ethnic minority patients (see Table 2 for more details).
Table 2 Age gender and ethnicity of patients
Age
Gender
Site
<60
≥60
Female
Male
1
9 (14.1%) 24 (38.1%) 15 (23.4%)
15 (23.4%)
2
5 (7.8%)
17 (26.6%)
3 (4.7%)
14 (21.9%)
3
1 (1.6%)
7 (10.9%)
4 (6.2%)
3 (4.7%)
Ethnicity
White British Other
22 (34.4%)
11 (17.2%)
19 (29.7%)
4 (6.3%)
8 (12.5%)
0 (0.0%)
Adherence to the medication
The World Health Organisation defines adherence as the extent to which a patient’s
behaviour corresponds with the recommendations from a healthcare professional
6
(WHO 2008). This is a very general definition however a more specific definition is
identified by the International Society for Pharmacoeconomics and Outcome
Research: “the degree or extent of conformity to the recommendations about day-today treatment by the provider with respect to the timing, dosage, and frequency” of
medicines (Cramer et al. 2008). Most authors use the term adherence as synonymous
with observance and compliance (Bassan et al. 2013).
Fifty-nine patients report
being adherent with their medications, where no doses of medications were missed
(92.2%). The same number of the patients stated that they knew when to take their
medication. Fifty-seven (89.1%) stated that they feel confident about taking their
medication. Only 4 (6.3%) people admitted that they found their medication
confusing. When asked if they understood how their medication worked 44 (68.8%)
people agreed that they understood how their medications worked. Out of these 44
people only one person admitted that they didn’t understand how the medication
worked at first but that they understood over time.
Knowledge of when to take OC
When asked about what time of day they should take their medications only 37
patients report accurate timing for all of their medications. This number represents
57.8% of patients that report that they take their medications correctly. The most
common error in understanding was in relation to Thalidomide; 10 patients (15.6 %)
reported taking this medicine in the morning rather than in the evening as
recommended. There was no statistically significant relationship found in relation to
age, gender and ethnicity and knowledge of when to take the medications. Two
patients were interviewed who were taking CTD therapy and described how
complicated it was. One of the patients interviewed describes being given
7
information about when to take the medications by the medical and nursing staff but
when she got home she reports how she had to call out the GP. The patient describes
how the GP ‘was very surprised at how complicated it was’. The patient describes
feeling overwhelmed by the regime: ‘they give you the most enormous bag [of
tablets]…they hand it to you as if, you know, now go away and you know, use it’.
This patient was reliant on her GP to help her sort out the dosing schedule as she felt
overwhelmed by the responsibility once she got home despite the education provided
to her in the hospital.
Knowledge of what to do if forget to take their OC
The participants were asked what actions they should take if they forget to take their
medications. Forty two (65.6%) patients gave the correct answer that they should take
the medicine as soon as they remember on the same day and/or ring the clinical nurse
specialist. No statistical significance was found related to age, gender and ethnicity
and what to do if they forget to take their medicines. However, three respondents
report unsafe practice such as taking a double dose of their OC the next day.
Knowledge of Side effects
It is very important that patients understand the difference between those problems
that arise that can be self-managed and those that need prompt reporting to a health
care team. Patient’s knowledge of who to contact should they experience serious side
effects related to their medications was variable. Most patients correctly identified
who to contact if they were feeling nauseous or sick despite taking anti-sickness drugs
(85.5%). When experiencing tingling in fingers or toes they generally knew who to
contact (82.3%). However only 46 (71.9%) patients knew who to contact if feeling
8
generally unwell but this went up to 52 (81.2%) if they had a high temperature. A
much smaller number of patients knew who to contact if developing constipation
and/or diarrhoea 42 (65.6%). Figure 1 summarises patient knowledge in relation to
who to contact if they experience side effects of therapy. A significant difference was
found regarding knowledge of who to contact if they experienced side effects and
gender, females were found to have a significantly worse mean rank than males and
this was found to be statistically significant (p=0.037).
Figure 1. Knowledge of who to contact if side effects experienced
Overall patient’s knowledge of side effects associated with CDT was found to be low.
Figure 2 summarises the knowledge of side effects known by patients. A significant
relationship was also found between knowledge about side effects and ethnicity
(p=0.007) with white British having a significantly higher mean rank score in this
area of knowledge compared to those from other ethnicities.
9
Figure 2 Knowledge of side effects assocated with CTD
Support with taking medications
Nearly a third of patients (31.3%) report that they rely on a partner or family member
to support them with taking their medications. Those living alone and without good
support have been found to be non-adherent with OC in other research (Noens et al
2009). Fifty four (84.4%) patients report using a number of tools to prompt them to
take their medications with 38 (59.4%) patients using a check list, 18 (28.1%) a
calendar, 12 (18.8%) a dosset box, 5 (7.8%) used their own records and 1 patient used
an alarm. However 10 (15.6%) did not use any aid to remind them to take their
medications. There was no statistically significant difference between gender, age or
ethnicity in terms of using a medicine organizing strategy or having a family member
helping with medications. Three people mentioned that it was so important to take
their medications that always remembered and never forgot to take them and did not
need to use an aid to remind them.
10
Figure 3 Strategies used to organise tablet taking
Difference between hospitals
The three hospital sites were compared using the Kruskal Wallis test. A significant
difference was found between the hospital sites in terms of knowledge about the
timing of medications (p=0.001) and who to contact when experiencing significant
side effects (p<0.001) with site 1 having the lowest mean rank for patient knowledge
and this site was significantly busier than the other two sites and had more patients
from ethnic minorities groups and more females.
DISCUSSION
Patient’s knowledge, understanding and retention of information about OC are linked
to adherence behaviour (Bassan et al. 2013). Although patients report high levels of
adherence with medications they also identify knowledge deficits that could
unintentionally affect adherence and lead to sub-optimal adherence. Atkins and
11
Fallowfield (2006) make a distinction between intentional non-adherence where a
decision is taken not to take medication and non-intentional non-adherence where a
patient misunderstands or forgets to take their medication. In this study there was
evidence that patients strived to take their medications in the way prescribed; however
there were some knowledge deficits that could lead to non-intentional non-adherence.
Patients despite reporting high rates of confidence in taking their OC were less well
informed about how their CDT therapy worked. Atkins and Fallowfield (2006)
suggest that further research should study the patients’ understanding of the mode of
action and benefits of OC from the patient perspective.
There is a requirement for patients to remember a great deal of complex information
about CDT which can be confusing. Patients therefore have many aspects of
information to recall following information giving especially during the first cycle of
therapy including managing life threatening side effects such as infection and sepsis,
when to take medications, modes related to food intake, and what to do if they forget
to take the medication or have problems with sickness and vomiting all key aspects of
optimal adherence. The results of this study suggest that patients may be at risk of
non-intentional non-adherence where they are non-adherent due to misunderstandings
or forgetfulness about timing their medication intake, which may lead to other
problems such as excessive sleepiness if Thalidomide is taken during the day rather
than at night as recommended.
Despite the fact that the patient education in OC stresses the seriousness of side
effects, which are repeated by health care providers (Oakley et al 2010), patients have
been found to avoid reporting symptoms through fears of interrupting dosing
schedules (Gerbrecht and Kangas 2004). Preoccupation with risks shape the way that
healthcare is delivered and how patient information is provided so risks can be
12
effectively managed. Stephenson et al. (2004) suggest that there is a lack of attention
to the patient’s ability to adhere with medication schedules and that this is a barrier to
the doctor and nurse-patient relationship. Patient knowledge of the side effects of the
CDT was surprisingly low. Patients are not as well-informed about side effects as
expected. It is crucial that the patients have a thorough understanding of expected
side effects and their perceptions of risk are assessed. Further evidence from this
study suggest that females and those from ethnic minority groups are less
knowledgeable about the side effects of CDT and therefore may be at higher risk of
sub-optimal adherence compared to white male patients. The current research
suggests that gender and ethnicity should be taken into account in patient education
activities related to OC. Site 1 had the busiest out-patient clinic but also the highest
number of female patients and highest number of those from ethnic minority groups
and patients from this site were significantly less knowledgeable about side effects
than those from the other two sites. As each site had one clinical nurse specialist it is
possible that the CNS at site 1 had less time than colleagues at other sites to provide
patient centred information due to the large number of patient coming through the
clinic.
Around 40% of patients with MM report problems with anxiety and depression with
patients suffering symptoms such as continual bone pain, body image changes such as
loss of height, fatigue and loss of energy resulting in a reduced quality of life
(Moliatossis et al. 2011). Greater use of screening for depression and anxiety is
important for those with MM as both patients in the interviews conducted describe
feeling ‘on the edge’ and low in mood. Psychological distress has been found to be
associated with non-adherence (Lebovits et al. 1990).
13
The number of prescribed medications has also been found to be relevant to
adherence with those having to take many medications developing routines to
promote adherence (Barron et al. 2007).
In this study most patients were
recommended to use a spreadsheet identifying when to take their medicines and this
was recommended on all the sites of the research. Despite this some patients did not
use any prompt to remind them to take their medications. More research needs to be
done to find which strategies work best for patients and to offer more patient centred
tools that are meaningful to patients. Some suggestions identified in the literature are
use of diaries (Oakley et al. 2010), pill boxes (Ruddy et al. 2009), text messaging
(Miloh et al. 2009), and electronic pill boxes for those will low levels of literacy
(Wolpin 2009). The Multinational Association for Supportive Care in Cancer
(MASCC) identified strategies for adherence using a tool that can facilitate adherence
behaviours. The tool helps to identify issues that help and hinder adherence and
promotes patient education strategies and can be found at www.mascc.org.
Study limitations
Patients self report is used in this study and it is well known that patients may
overestimate their adherence to please healthcare professionals and more reliable
methods are preferred such as electronic counting device or the medication event
monitoring system these have not been used in the present study and should be
considered in future studies of this kind (Haynes et al. 2005). The affect of adherence
with therapy over time remains unexplored in this study and this is a limitation. In
future studies it is recommended that patients are studied over time to collect
longitudinal data of knowledge and adherence behaviour over time. Only two patients
were interviewed about self-managing their CTD therapy, which is a limitation and is
14
a problem for transferability. In future studies a clearer foucs on community support
for patients on CTD is needed.
CONCLUSION
Care disparities in OC need to be recognised and a focus on high-risk individuals to
improve patient adherence. Patient education by healthcare practitioners is critical to
patient adherence with OC medications. Education should be extended to include not
only the patient (and family member) but also the GP, practice nurse and pharmacist
(O’Neil and Twelves 2002) as following information giving in the hospital setting
patients may still struggle with a complex regime once they are home and may need
to call on community support. However the monitoring of adherence remains the
responsibility of the specialist medical team supported by a named CNS. It is very
important that models of care for those taking oral therapy are researched and the
infrastructure to support adherence and self-management is developed. However the
infrastructure to support optimal adherence is reported to be lacking (Oakley et al.
2010). Innovative approaches to support patient’s self-management activities are
needed based on assessment of individual patient need, level of understanding and
assessment of risk. Professionals need to extend patient education activities to a
range of resources to help patients understand and recall OC education; including
technological innovations and prompting techniques such as text messaging and
supplementary ways of delivering information such as use of pictures (Linn et al.
2012), diaries (Oakley et al. 2010) as relying on standard techniques such as face to
face information giving and written handbooks are insufficient to enable thorough
knowledge and understanding for self management of OC.
15

Adherence needs to take a more central part in patient education activities
prior to and during treatment with OC

Special attention needs to be given to those from ethnic minority groups and to
females as they have lower scores in knowledge levels

Screening of high risk patients need to be carried out including monitoring of
anxiety and depression and additional support in the community such as from
pharmacists and GPs

Family support needs to be assessed and carers need to be involved in patient
education activities as well as patients

e health options could be used to prompt patients and cue them to take their
medication and report side effects promptly
ACKNOWLEGEMENTS
We would like to thank the patients who took part in the survey and interviews and all
the staff who supported the research at the three hospital sites. This study was made
possible by a generous grant from the charity Myeloma UK.
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