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Cancers: Symptom Clusters in Survivorship and Their Impact On Ability To Work Among Cancer Survivors

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cancers

Article
Symptom Clusters in Survivorship and Their Impact on Ability
to Work among Cancer Survivors
Joanna E. Fardell 1,2 , Sim Yee (Cindy) Tan 3,4 , Kim Kerin-Ayres 4 , Haryana M. Dhillon 5
and Janette L. Vardy 3,4, *

1 UNSW Medicine & Health, School of Clinical Medicine, UNSW Sydney, Sydney 1466, Australia;
j.fardell@unsw.edu.au
2 Western Sydney Youth Cancer Service, Westmead Hospital, Sydney 2145, Australia
3 Sydney Medical School, Faculty of Medicine and Health, University of Sydney, Sydney 2006, Australia;
sim.tan@sydney.edu.au
4 Concord Cancer Centre, Concord Repatriation General Hospital, Sydney 2139, Australia;
kim.kerinayres@health.nsw.gov.au
5 Psycho-Oncology Cooperative Research Group, School of Psychology, Faculty of Science,
University of Sydney, Sydney 2006, Australia; haryana.dhillo@sydney.edu.au
* Correspondence: janette.vardy@sydney.edu.au

Simple Summary: Lasting impacts and symptoms of cancer treatment can affect survivors’ daily lives.
We explored how symptoms and symptom clusters can impact the ability to work among 561 cancer
survivors previously diagnosed with breast, colorectal, and haematological malignancies, who were
on average 58 years old and 1.5 years since diagnosis. We found almost 35% of survivors reported
limitations in their ability to work. We identified three main symptom clusters: pain, emotional, and
cognitive symptoms. Survivors experiencing these symptom clusters were approximately 14–17%
more likely to report limitations in their work ability. Older survivors and those with more advanced
cancer stages were also more likely to experience limitations in their work ability. In conclusion, a
significant number of cancer survivors struggle to work due to their symptoms after treatment. Out
Citation: Fardell, J.E.; Tan, S.Y.; results suggest that by better understanding and managing these symptoms, survivors can have
Kerin-Ayres, K.; Dhillon, H.M.; improved opportunities to participate in work after their cancer treatment.
Vardy, J.L. Symptom Clusters in
Survivorship and Their Impact on Abstract: Background: Cancer survivors often experience a range of symptoms after treatment which
Ability to Work among Cancer can impact their quality of life. Symptoms may cluster or co-occur. We aimed to investigate how
Survivors. Cancers 2023, 15, 5119. symptoms and symptom clusters impact the ability to work among cancer survivors. Methods:
https://doi.org/10.3390/ We used symptom severity data and ability to work data routinely collected from cancer survivors
cancers15215119
attending a survivorship clinic after primary treatment with curative intent. We defined symptom
Academic Editors: Brenna clusters using single linkage and a threshold on the rescaled distances of <10. We then conducted a
C. McDonald, Diane Von Ah and logistic regression to examine how symptoms and symptom clusters were related to the ability to
Alexandre Chan work. Results: We analysed data from 561 cancer survivors, mean age 58 years and 1.5 years post
Received: 17 September 2023
diagnosis, with mixed diagnoses including breast (40.5%), colorectal (32.3%), and haematological
Revised: 18 October 2023 cancers (15.3%). Limitations to work ability were reported by 34.9% of participants. Survivors
Accepted: 20 October 2023 experiencing pain, emotional, and cognitive symptom clusters were 14–17% more likely to report
Published: 24 October 2023 limitations in their ability to work. Older survivors and those with a higher stage disease were
more likely to report limitations in their ability to work. Conclusion: A better understanding and
management of symptom severity and symptom clusters may help the sizable proportion of cancer
survivors experiencing symptoms to participate in work after treatment.
Copyright: © 2023 by the authors.
Licensee MDPI, Basel, Switzerland.
Keywords: cancer; work; survivor; symptoms; cognitive symptoms; anxiety; depression; pain; fatigue
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).

Cancers 2023, 15, 5119. https://doi.org/10.3390/cancers15215119 https://www.mdpi.com/journal/cancers


Cancers 2023, 15, 5119 2 of 11

1. Introduction
Many people surviving cancer experience a range of symptoms and complications
during and/or following their cancer treatment that may persist long-term and lead to
poorer health outcomes. This can include compromised physical functioning and psycho-
logical well-being, and the development of chronic illnesses, all of which can impact an
individual’s quality of life and survival [1–5].
Our own research in 385 early-stage cancer survivors attending their initial visit at
the Sydney Cancer Survivorship Centre Clinic found that approximately 12 months after
diagnosis, 56% of survivors reported five or more symptoms of at least moderate severity
(>=4/10) [3]. The most commonly reported symptoms were fatigue (45%), difficulty
sleeping (37%), pain (34%), sore hands or feet (30%), numbness or pins and needles (30%),
difficulties with thinking skills (concentration and memory [27.5%]), and mood disturbance
(anxiety [31%], depression [23%], and stress [45%]), with fear of cancer recurrence rated by
a clinical psychologist based on their consultation as 62% [3]. A second study comparing
the rates and severity of symptoms at the initial visit to their follow up visit, 12 months later,
found some improvement in pain, fatigue, and energy, but more than 20% of survivors still
had moderately severe fatigue, pain, or sleep disturbance, and 26%, particularly women,
continued to report five or more symptoms of at least moderate severity [6]. Others have
reported similar symptoms but at even higher rates five years after adjuvant treatment in
Asian and Australian cancer survivors: fatigue (67%), loss of strength (62%), pain (62%),
sleep disturbance (60%), and weight changes (58%) [7].
Similar to our finding of high rates of survivors with multiple symptoms, previous
research, which has been mainly conducted in breast cancer survivors, has documented
the co-occurrence of symptoms, also known as symptom clusters, in the years after treat-
ment, particularly for sleep, fatigue, and mood disturbance [8]. Symptom clusters have
been defined as consisting of two or more symptoms that are related to each other and
are considered to be relatively stable over time [9,10]. Other symptom clusters among
survivors include ongoing pain and symptoms associated with peripheral neuropathy,
cognitive impacts, and reduced physical activity [11–13]. Primary cancer site, disease stage,
or antitumor treatment have previously been found to predict the occurrence of symp-
tom clusters [14], but these associations with demographic and clinical variables are not
consistently found [15]. For example in a secondary analysis of 282 breast cancer patients
receiving chemotherapy or radiotherapy, Kim et al. [15] found no association of treatment
modality (chemotherapy vs. radiotherapy), age, employment status, disease stage, and
comorbid condition.
The reasons for symptom clusters include a common aetiology or biological pathway,
such as an inflammatory process and increased cytokines, immune processes, activation
of the sympathetic nervous system, and activation of the hypothalamic-pituitary–adrenal
axis [10,16]. However, attribution of a clear and single causal pathway is challenging due
to variable symptom cluster inclusions across papers (e.g., fatigue, pain, and depression
versus fatigue, pain, depression, and sleep disturbance) [10].
Reasons for not participating in work at pre-diagnosis levels are multifactorial [17,18].
Symptom burden can impact an individual’s ability to resume daily activities including
returning to work or the ability to achieve expected outcomes at work (for example,
completing tasks on time or to a level of previous proficiency). In addition to providing
an income, working or returning to work is often regarded as an important milestone for
cancer survivors as it is extrinsically linked to identity, self-esteem, and a sense of returning
to normalcy for those of working age [17,19]. However, up to 40% of cancer survivors either
do not return to work or do not go back to their pre-diagnosis level of employment [20].
A recent systematic review of 68 studies in cancer survivors who had completed primary
cancer treatment found a trend for higher symptom burden to be associated with poorer
work outcomes [21]. Fatigue, depression, and cognitive symptoms were found to be related
to poorer work performance, and issues with body image and oral dysfunction were
associated with a higher risk of unemployment [21].
Cancers 2023, 15, 5119 3 of 11

Cognitive symptoms (also referred to as cognitive impairment throughout the litera-


ture) are likely to contribute to work outcomes due to the requirements to utilise cognitive
skills at work (e.g., pay attention, complete tasks within an allotted time, remember to do
tasks, plan, organise, prioritise and review tasks) [17,22,23]. In a sample of 68 breast cancer
survivors who had returned to work, Von Ah et al. found perceived cognitive impairment
was associated with the ability to work, while clinical and demographic factors were not.
Similar results indicating a role for perceived cognitive impairment impacting markers of
work productivity (e.g., time management) and engagement were also found [18,24].
Self-report of cognitive symptoms have consistently been associated with emotional
symptoms of depression and anxiety, as well as fatigue [25,26]. For example, our analysis
of population level data (N = 10,337, with 691 (6.7%) with a history of cancer) found
moderate to high correlation between anxiety, depression and concentration difficulties
(correlations ranged r = 0.52 for anxiety and concentration difficulties, to r = 0.81 for anxiety
and depression), and approximately 9% of the population reported experiencing either
concentration difficulties and depression or concentration difficulties and anxiety [27].
However, few studies have considered the co-occurrence of cognitive symptoms, such as
attention and memory difficulties, in addition to other commonly co-occurring symptoms,
such as depression, anxiety, and fatigue, and its consequent impact on the ability to
work. Among a sample of 379 cancer survivors, Ehrenstein et al. [26] found self-reported
cognitive symptom (memory and executive function) trajectories were related to work,
fatigue, and depression. They found more cognitive symptoms which were stable over
time to be associated with older age, longer time after diagnosis before returning to work,
more quantitative work demands, and higher levels of depressive symptoms at baseline.
However, they did not investigate the co-occurrence of cognitive symptoms, fatigue, and
depression, and their compounding impact on work outcomes. Considering symptom
clusters that include cognitive difficulties, their impact on the ability to work is critical,
given (i) the likelihood of multiple symptoms being experienced due to cancer treatment
well into survivorship and (ii) the compounding negative impact of multiple symptoms on
quality of life and the ability to participate in work. Therefore, to address this gap in the
literature, this study aimed to (i) identify symptom clusters based on severity of symptoms,
and (ii) evaluate how these symptoms, including self-reported cognitive symptoms, were
related to work ability among a sample of cancer survivors.

2. Methods
2.1. Participants
Cancer survivors attending the Sydney Cancer Survivorship Centre multidisciplinary
team clinic between September 2013 (when the clinic opened) and October 2020, who
provided returning to work data and consented for their data to be used in research, were
eligible to participate in this research study. Eligibility for attending the Sydney Cancer
Survivorship Centre has been published [27] and includes an invasive cancer diagnosis,
completion of primary cancer treatment (generally including chemotherapy) for early-stage
cancer, or occasionally those with stage IV who have had potentially curative treatment,
such as resection of metastatic disease, and no evidence of a cancer recurrence. Exclusion
criteria for attending the clinic include currently undergoing primary treatment, with the
exceptions that patients with breast cancer may be receiving hormonal treatment and/or
targeted therapy such as trastuzumab, and patients with haematological malignancy may
be on maintenance treatment. Referrals for the Sydney Cancer Survivorship Centre are
accepted from medical oncologists, surgeons, and radiation oncologists [28].

2.2. Measures
Participants completed questionnaires either on paper or via online survey using
the REDCap survey function prior to attending the Sydney Cancer Survivorship Centre
clinic. The questionnaires included a comprehensive assessment of patient self-reported
Cancers 2023, 15, 5119 4 of 11

symptoms, quality of life, distress, and lifestyle factors [28]. For this analysis, we focused
on self-reported symptoms and the ability to work.
Participants’ demographics, including age and sex and clinical information, including
diagnosis, stage, treatment received, and time since treatment, were obtained from the
patient’s medical record.
Self-reported symptoms were selected from the Patient’s Disease and Treatment As-
sessment (PDTA) form [29]. The PDTA asks respondents to rate the severity of 47 symptoms
and aspects of wellbeing; we also added a memory question. Symptoms are rated from
0–10, with higher scores indicating greater symptom severity, and the following anchors
are provided: 0 indicating no trouble and 10 indicating the worst I can imagine. For this
analysis, we focused on symptoms commonly experienced during survivorship based on
our included cohort of survivors [3,6] and included the following: pain, fatigue, trouble
sleeping, numbness or pins and needles, diarrhoea, anxiety, depression, trouble concentrat-
ing, and problems with memory. Additionally, these symptoms were selected to ensure the
coverage of the commonly occurring symptom clusters grouped into physical symptoms
or psychological symptoms [14,30].
To determine whether participants were able to work, we used a single item from the
Functional Assessment of Cancer Therapy–General (FACT-G): “I am able to work (include
work at home)” [31]. Responses are on a 5-point Likert scale, ranging from 0 “not at all” to
4 “very much”. We dichotomised work ability as “limited ability to work” if the participant
responded 0 “not at all”, 1 “a little bit”, or 2 “somewhat”; work ability was categorised as
“able to work” if the participant responded 3 “quite a bit” or 4 “very much”.

2.3. Statistical Analysis


We conducted all statistical analyses using IBM SPSS Statistics version 27 (IBM Corpo-
ration, Armonk, NY, USA). We described our sample using means and standard deviations
for continuous variables and counts and proportions for categorical variables. We com-
pared participants’ work ability on demographic and clinical factors using chi-square
tests for categorical variables and ANOVA for continuous variables. Previous research
comparing statistical methods for identifying symptom clusters has found consistency
across a principal component analysis, exploratory factor analysis, and hierarchical cluster
analysis [30]. To address aim 1 and identify symptom clusters, we conducted a hierar-
chical cluster analysis. We defined clusters using single linkage and a threshold on the
rescaled distances <10, as previously recommended [30]. We operationalised symptom
cluster scores as the mean of the constituent symptoms. To address aim 2, we ran two
logistic regression models with ability to work as the dependent variable. In the first model,
we entered demographic variables and individual symptoms. In the second model, we
entered demographic variables and any symptom clusters we had previously identified
and individual symptoms. Factors were considered significantly associated with ability to
work when p < 0.05.

3. Results
Ability to work data were available from 561 cancer survivors who attended the
Sydney Cancer Survivorship Centre clinic. Table 1 provides the demographic characteristics
of the population used for this analysis. Participants were on average 58 years old and
1.5 years post diagnosis. Most were female (69.2%), and the most common diagnosis
was breast cancer (40.5%), followed by colorectal cancer (32.3%). Over a third (34.9%) of
participants reported limitations in their ability to work. There was no difference between
those who reported limited work ability and those able to work successfully based on
clinical and demographic factors in univariable analysis. However, those with limited
ability to work were more likely to report greater symptom severity than those who reported
no limitation to working at the time of their initial visit (Figure 1, all p values ≤ 0.001).
Fatigue did not differ significantly between those with limited work ability and those able
to work (p = 0.177).
2023, 15, x FOR PEER REVIEW 5 of 11
Cancers 2023, 15, 5119 5 of 11

0.001). Fatigue Table


did not differ significantly
1. Participant between
demographics those with
and symptoms for limited work
the whole ability
sample and
and whether participants
those able to work (p = 0.177).
were able to work or were limited in their ability to work .g

Table 1. Participant demographics


Total Sample (nand symptomsLimited
= 561) for the whole sample (n
Work Ability and whether participants
= 196) Able to Work (n = 365)
were able to work or were limited in their ability to work g.
Age (SD) 58.0 (13.4) 60.5 (12.8) 56.6 (13.6)
Range Total Sample (n = 561)18–91 Limited Work Ability (n = 196) Able to Work (n = 365)
D) Female sex 58.0 (13.4) 338 (69.2%) 60.5 (12.8) 140 (31.1%) 56.6 (13.6) 248 (63.9%)
ange Years since diagnosis (SD)
18–91 1.5 (2.0) 1.5 (1.6) 1.5 (2.1)
e sex 338 (69.2%) 140 (31.1%) 248 (63.9%)
Median 1.0
since diagnosis (SD) 1.5 (2.0) 1.5 (1.6) 1.5 (2.1)
75th Percentile 1.0
Median 1.0
Tumour type
5th Percentile 1.0
ur type Breast 227 (40.5%) 77 (33.9%) 150 (66.1%)
reast Colorectal 227 (40.5%) 181 (32.3%) 77 (33.9%) 68 (37.6%) 150 (66.1%) 113 (62.4%)
olorectal Haematological 181 (32.3%) 86 (15.3%) 68 (37.6%) 28 (32.6%) 113 (62.4%) 58 (67.4%)
aematological
Other a 86 (15.3%) 67 (11.9%) 28 (32.6%) 23 (34.3%) 58 (67.4%) 44 (65.7%)
ther a b 67 (11.9%) 23 (34.3%) 44 (65.7%)
Stage
b
I 83 (14.8%) 23 (27.7%) 60 (72.3%)
83 (14.8%) 23 (27.7%) 60 (72.3%)
II 180 (32.1%) 59 (32.8%) 121 (67.2%)
180 (32.1%) 59 (32.8%) 121 (67.2%)
III IV
andc resected IV c 279 (49.7%) 106 (38.0%) 173 (62.0%)
I and resected 279 (49.7%) 106 (38.0%) 173 (62.0%)
Treatment received
ment received
urgery d Surgery d 469 (83.6%) 469 (83.6%) 166 (35.4%) 166 (35.4%) 303 (64.6%) 303 (64.6%)
hemotherapy e
Chemotherapy e 478 (85.2%) 478 (85.2%) 165 (34.5%) 165 (34.5%) 313 (65.5%) 313 (65.5%)
adiotherapy f f 235 (41.9%) 79 (33.6%) 156 (66.4%)
Radiotherapy 235 (41.9%) 79 (33.6%) 156 (66.4%)
Notes: a Other cancer types includes lung (n = 20), upper gastrointestinal (n = 36), and other diagno-
a Other cancer types includes lung (n = 20), upper gastrointestinal (n = 36), and other diagnoses (n = 11);
Notes:
ses (n = 11); b missing 19; c n = 40 with Stage IV disease at diagnosis; d missing 11; e missing 8; f missing
b missing 19; c n = 40 with Stage IV disease at diagnosis; d missing 11; e missing 8; f missing 12; g able to work
12; g able to workwas was defined
defined as having
as having responded
responded “quite “quite
a bit” ora“very
bit” or “very
much” much”
to the item to theable
“I am itemto“I am (including work at
work
able to work (including work at home)”; limited work ability was defined as those having responded
home)”; limited work ability was defined as those having responded “not at all”, “a little bit” or “somewhat”.
“not at all”, “a little bit” or “somewhat”.

Fatigue
Pain
Anxiety
Trouble Sleeping
Symptom

Trouble concentrating
Problems with my memory
Numbness or pins and needles
Depression
Diarrhoea
0 2 4 6 8 10
Mean symptom severity

Able to work (N=365) Limited work ability (N=196)

Figure 1. Mean symptom severity rating. Higher scores out of 10 indicate greater severity.
Figure 1. Mean symptom severity rating. Higher scores out of 10 indicate greater severity.
Cancers 2023, 15, x FOR PEER REVIEW 6 of 11
Cancers 2023, 15, 5119 6 of 11

3.1. Symptom Clusters


3.1. Symptom Clustersclusters at a rescaled distance of <10 (see Figure 2). At the lower
We determined
threshold, clusters
We determined were identified
clusters as an emotional
at a rescaled distancecluster
of <10(anxiety and2).
(see Figure depression), a cog-
At the lower thresh-
nitive cluster (attention and memory), or a combined emotional–cognitive symptom clus-
old, clusters were identified as an emotional cluster (anxiety and depression), a cognitive
ter.
cluster (attention and memory), or a combined emotional–cognitive symptom cluster.

Figure
Figure 2.
2. Dendrogram
Dendrogram showing
showing symptom
symptom clustering using single
single linkage
linkage as
aspreviously
previouslydescribed
described[29].
[29].
3.2. Factors Associated with Returning to Work
3.2. Factors
In ourAssociated withregression
first logistic Returning to Work we entered demographic and clinical variables
model,
into Intheourmodel with individual
first logistic regressionsymptoms to determine
model, we entered demographicthe factors
and associated with the
clinical variables
ability
into thetomodel
work with
after individual
cancer (Table 2). The overall
symptoms modelthe
to determine fit was significant
factors associatedandwith
accounted
the
for 33.3% of the variance 2 (17) = 133.25, p < 0.001). Of the
ability to work after cancerin self-reported
(Table workmodel
2). The overall abilityfit(χwas significant and accounted
demographic
for 33.3% of the and clinicalinvariables
variance entered,
self-reported workweability
found(χ older
2(17) participants
= 133.25, p <were
0.001).less
Oflikely
the to
be able to work
demographic and(OR: 0.964,
clinical 95%CI:entered,
variables 0.944–0.985).
we foundParticipants with Stage
older participants wereIII less
andlikely
resected
Stage
to be ableIV disease
to workwere
(OR: less likely
0.964, to be
95%CI: able to work
0.944–0.985). comparedwith
Participants to those
Stagewith Stage
III and I disease
resected
Stage IV disease
(OR 0.385, 95%CI: were less likely to
0.168–0.883). be able to of
Symptoms work compared
pain, to those withand
fatigue, depression, Stage I diseasewith
problems
(OR
memory0.385,were
95%CI: 0.168–0.883).
significantly Symptoms
associated of pain,
with fatigue,
the ability todepression,
work, withand problems
those reporting withmore
memory were significantly
severe symptoms less likely associated
to be able with the ability to work, with those reporting more
to work.
severe Insymptoms
our secondless likelyregression
logistic to be able model
to work.(Table 3), we entered demographic and clinical
variables into the model with the above identified symptom clusters and any remaining
symptoms not included in a cluster to determine the factors associated with the ability to
work after cancer. Again, the overall model fit was significant and accounted for 31.6%
of the variance in self-reported ability to work (χ2 (17) = 130.04, p < 0.001). Similar to the
results of the first logistic regression model, older participants and those with Stage III and
resected/treated Stage IV disease were less likely to be able to work. Participants reporting
more severe pain, higher cognitive symptom cluster scores (i.e., more severe memory and
attention symptoms on average), and those with higher emotion symptom cluster scores
(i.e., more severe anxiety and depression symptoms on average) were less likely to be able
to work.
Cancers 2023, 15, 5119 7 of 11

Table 2. Logistic regression with work ability as the dependent variable and clinical and demographic
variables and symptoms as independent variables.

OR 95% C.I Lower 95% C.I Upper p-Value


Participant age at survey completion 0.964 0.944 0.985 0.001
Sex 0.841 0.471 1.502 0.558
Tumour type
Breast (reference) - - - -
Colorectal 0.918 0.432 1.951 0.823
Haematological 0.264 0.031 2.226 0.221
Other 0.989 0.403 2.431 0.981
Stage
Stage I (reference) - - - -
Stage II 0.578 0.266 1.256 0.166
Stage III and resected Stage IV 0.385 0.168 0.883 0.024
Treatment
Surgery 0.306 0.042 2.212 0.241
Chemotherapy 0.875 0.413 1.854 0.728
Radiotherapy 1.125 0.627 2.021 0.693
Symptoms
Pain (all and anywhere) 0.833 0.748 0.928 0.001
Numbness or pins and needles 0.934 0.858 1.016 0.111
Fatigue (tiredness) 0.889 0.786 1.006 0.062
Trouble sleeping 1.037 0.933 1.152 0.501
Diarrhoea 0.969 0.857 1.094 0.609
Anxiety (feeling worried) 0.977 0.843 1.132 0.759
Depression (feeling sad) 0.865 0.748 0.999 0.049
Trouble concentrating 1.097 0.947 1.271 0.217
Problems with memory 0.798 0.702 0.907 0.001

Table 3. Logistic regression with work ability as the dependent variable and clinical and demographic
variables and symptom clusters identified using a rescaled distance of <10 as independent variables.

OR 95% C.I Lower 95% C.I Upper p-Value


Participant age at survey completion 0.962 0.943 0.982 0.000
Sex 0.777 0.442 1.367 0.382
Tumour Type
Breast (reference) - - - -
Colorectal 1.069 0.516 2.214 0.858
Haematological 0.480 0.072 3.185 0.447
Other 1.177 0.490 2.828 0.715
Stage
Stage I (reference) - - - -
Stage II 0.491 0.231 1.045 0.065
Stage III and resected Stage IV 0.331 0.148 0.740 0.007
Cancers 2023, 15, 5119 8 of 11

Table 3. Cont.

OR 95% C.I Lower 95% C.I Upper p-Value


Treatment
Surgery 0.468 0.080 2.736 0.400
Chemotherapy 0.981 0.482 1.997 0.958
Radiotherapy 1.108 0.631 1.947 0.721
Symptoms
Pain (all and anywhere) 0.830 0.747 0.921 0.000
Numbness or pins and needles 0.927 0.855 1.005 0.068
Fatigue (tiredness) 0.909 0.807 1.024 0.117
Trouble sleeping 1.055 0.954 1.166 0.295
Diarrhoea 0.969 0.861 1.091 0.603
Emotional symptom cluster 0.858 0.764 0.965 0.010
Cognitive symptom cluster 0.864 0.765 0.975 0.018

4. Discussion
In our sample of 561 cancer survivors with mixed diagnoses who were attending
a large survivorship multidisciplinary team clinic in Sydney, Australia, around 35% of
survivors reported limitations in their ability to work. Reported symptom severity differed
between those reporting limitations in their ability to work and those not reporting limi-
tations in their ability to work after cancer. The factors that were significantly associated
with increased odds of being able to work included younger age, early-stage disease, and
less severe pain, emotional, and cognitive symptoms.
Our results are consistent with those of other studies showing impacts on work
engagement and participation among cancer survivors [17,18,21,24,32]. Previous research
has documented an associated impact on financial well-being, with survivors not able
to work reporting reduced earnings [14,22,32]. The flow-on effect to overall quality of
life is likely complex and age-dependent. Cancer survivors may reduce work hours or
start retirement earlier than otherwise planned due to positive (i.e., cancer has caused a
refocus on personal values such as spending more time with loved ones) and negative
(i.e., the lasting symptoms of cancer treatment prohibit work and impact overall quality
of life) impacts of cancer [17]. Our results do not tease apart these bidirectional impacts
and future research is warranted. However, the average age of our sample was below the
Australian retirement age (>65 years of age), and our results may reflect changed work
plans, further highlighting the importance of assessing for lasting symptom impacts after
cancer treatment is finished.
Similar to previous research, we found emotional or psychological symptoms of anxi-
ety and depression clustered together, and cognitive symptoms of attention and difficulties
with memory were clustered together [30,33]. Our results are important in highlighting
that the ability to work after cancer is impacted by multiple symptoms, in addition to
survivor age and disease stage. While these symptoms are self-reported, the presence
of these symptoms was associated with returning to work. These results may reflect im-
pacts on the capacity to fulfil work duties as highlighted by others [34]. In a sample of
1562 people with mixed diagnoses of advanced cancer, both on and off treatment, four
symptom clusters were reliably identified using different statistical methods and included
tense–worry–irritable–depressed (emotional cluster), fatigue–pain, nausea–vomiting, and
concentration–memory (cognitive cluster) [30]. This study also found the emotional cluster
was the strongest predictor of overall quality of life, in contrast to other identified clus-
ters [30]. As cognitive symptoms, depression, and fatigue may all be relatively stable over
Cancers 2023, 15, 5119 9 of 11

time [26], this further highlights the importance of addressing psychosocial aspects in
symptom cluster management [30] to help improve work outcomes for cancer survivors.

5. Implications for Cancer Survivors and Clinical Practice


We found older survivors and those with a higher stage of disease were at particular
risk of not achieving their work goals and therefore may also be at a potentially increased
risk of financial toxicity. Considering symptom presence (particularly pain and cognitive
and emotional symptoms), severity, and any potential clustering or compounding effects
during survivorship clinical encounters, particularly for older survivors and those with a
higher stage disease, may be particularly helpful to support survivors in achieving their
work-related goals. Although treating a symptom in isolation may miss the full impact on
overall quality of life during survivorship, conversely, focusing on reducing the severity of
one symptom may reduce or prevent escalation of the other symptoms [35]. As such, it is
recommended that clinicians screen for the presence of multiple symptoms and determine
if a sentinel symptom exists within a symptom cluster [10], as this may be amenable to an
evidence-based intervention.
A review of previous intervention research for symptom clusters has found inter-
ventions often targeted one symptom only [10], though some studies have reported im-
provements in symptoms, in addition to the primary symptom targeted [36]. In a pilot
randomised controlled trial with 86 patients with advanced lung, prostate, colorectal, or
gynaecologic cancers receiving treatment, a two week audio-recorded and delivered train-
ing program of twelve relaxation, imagery, or distraction exercises reduced the severity of
the pain, fatigue, and sleep disturbance symptom cluster at two weeks post intervention,
compared to a waitlist control group [35]. However, no impact was observed on symptom
interference with daily life [35].

6. Strengths and Limitations


Previous research has largely focused on breast cancer survivors, and a strength of
our study is the inclusion of a large sample of survivors with mixed cancer diagnoses
and stages; however, there are several limitations worth noting. We used a single item
measure of the ability to work and the experience of symptoms. While these questions
are used in current clinical encounters and serve as a reasonable screen of symptoms [37]
and the ability to work, research studies employing a more comprehensive assessment of
the presence of multiple symptoms and their severity, in addition to validated measures
of the ability to work, are warranted [37]. To address this gap clinically, at the Sydney
Cancer Survivorship Centre clinic, we have recently started collecting more information on
patients’ work status, changes in their working plans since their cancer diagnosis, and their
ability to work after cancer.

7. Conclusions
We found that almost 35% of cancer survivors attending a survivorship clinic reported
limitations in their ability to work and that this was associated with age, stage of disease,
and the presence of multiple symptoms including pain and emotional and cognitive
symptoms. A better understanding of symptom severity and clusters, and reducing
symptom burden after cancer treatment, may support survivors to better engage in work.
Future research on work engagement and the ability of cancer survivors to work should
seek to further explore and address the whole person context, including symptom burden
and benefits and barriers to work after cancer, to better understand and support cancer
survivors in achieving their work goals.

Author Contributions: Conceptualization, J.E.F. and J.L.V.; data curation, S.Y.T. and K.K.-A.; formal
analysis, J.E.F.; methodology, J.E.F. and J.L.V.; resources, S.Y.T. and K.K.-A.; writing—original draft,
J.E.F. and J.L.V.; writing—review and editing, J.E.F., S.Y.T., K.K.-A., H.M.D., and J.L.V. All authors
have read and agreed to the published version of the manuscript.
Cancers 2023, 15, 5119 10 of 11

Funding: Joanna E. Fardell is a Maridulu Budyari Gumal (SPHERE) Cancer CAG Senior Research
Fellow and is supported by a Cancer Institute NSW Research Capacity Building Grant (2021/CBG003).
Janette L. Vardy is supported by a National Health Medical Research Council Investigator Grant
[APP1176221].
Institutional Review Board Statement: The study was conducted according to the guidelines of the
Declaration of Helsinki and approved by the Sydney Local Health District—Concord General Repa-
triation Hospital Human Research Ethic Committee—(HREC/14/CRGH/23, approved 6 May 2014).
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.
Data Availability Statement: Data are available on reasonable request from the author.
Conflicts of Interest: The authors declare no conflict of interest.

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