Psychological impact of lymphoma on adolescents and young adults: not a matter of black or white
J Cancer Surviv
Psychological impact of lymphoma on adolescents and young adults: not a matter of black or white
F. M. Drost 0 1 2 3 4 5
F. Mols 0 1 2 3 4 5
S. E. J. Kaal 0 1 2 3 4 5
W. B. C. Stevens 0 1 2 3 4 5
W. T. A. van der Graaf 0 1 2 3 4 5
J. B. Prins 0 1 2 3 4 5
O. Husson 0 1 2 3 4 5
0 Department of Medical Oncology, Radboud University Medical Centre , Nijmegen , The Netherlands
1 Comprehensive Cancer Centre the Netherlands (CCCN), Netherlands Cancer Registry , Eindhoven , The Netherlands
2 CoRPS - Centre of Research on Psychology in Somatic Diseases, Department of Medical and Clinical Psychology, Tilburg University , Tilburg , The Netherlands
3 Department of Medical Psychology, Radboud University Medical Centre , PO Box 9101, 6500 HB Nijmegen , The Netherlands
4 The Institute of Cancer Research and Royal Marsden NHS Foundation Trust , London , UK
5 Department of Haematology, Radboud University Medical Centre , Nijmegen , The Netherlands
Purpose The purpose of the study is to examine differences in perceived impact of cancer (IOC) between adolescents and young adults (AYAs; 18-35 years at cancer diagnosis), adults (36-64 years) and elderly (65-84 years) with a history of (non-)Hodgkin lymphoma. Furthermore, to investigate the association of socio-demographic, clinical and psychological characteristics with IOC; and the association between IOC and health-related quality of life (HRQoL) among AYAs only. Methods This study is part of a population-based PROFILES registry survey among lymphoma patients diagnosed between 1999 and 2009. Patients (n = 1.281) were invited to complete This manuscript has been prepared in accordance with the style of the journal, and all authors have approved its contents. This manuscript is not being considered for publication elsewhere and the findings of this manuscript have not been previously published.
Adolescent and young adult oncology; Impact of cancer; Lymphoma; Health-related quality of life
In The Netherlands, each year approximately 4000 people are
diagnosed with non-Hodgkin lymphoma (NHL) and 400 with
Hodgkin lymphoma (HL) [
]. Advances in early cancer
detection, diagnosis, and treatments have noticeably improved
survival rates of patients with lymphoma [
]. The 5-year
survival rates range from 48–76 % (NHL) to 95 % (HL),
depending on type and stage of tumour, treatment, and age of
the patient [
]. In 2013, there were approximately 5800
patients living with a history of HL and 30,000 with NHL [
As the survival rate is increasing, attention is more and
more given to the long-term consequences (e.g. fatigue,
depression) and late effects (e.g. infertility and second cancers)
of cancer and its treatment. These effects can have a negative
influence on health-related quality of life (HRQoL) [
addition, cancer survivors also perceive specific positive and
negative impact of cancer (IOC) on their lives. In a positive
way, cancer survivors can develop more empathy and health
awareness, or a positive self-evaluation after their cancer .
On the other hand, cancer can influence life in a negative way,
by appearance and body change concerns, and by worrying
]. Development of the IOC questionnaire was spurred by the
need to measure unique aspects of survivorship not addressed
by existing HRQoL measures [
]. Whereas HRQoL measures
generally focus on physical, cognitive, social and emotional
functioning, the IOC measure addresses the unique issues,
problems and changes that long-term survivors ascribe to their
cancer experience (e.g. the survivors ‘health awareness’, the
‘meaning of cancer’ and how the experience changed the
IOC may be age-specific [
5, 10, 11
]. Each phase in life is
characterized by developmental milestones or typical life
]. For example, elderly people (>65 years at
diagnosis) generally have to deal with a decline in physical
functioning, less social support, isolation and comorbid conditions
]. In contrast, adults (36–64 years at diagnosis) more
often have concerns about unemployment, financial issues
and family matters [
], while adolescents and young
adults (AYAs; 18–35 years at cancer diagnosis) are in a
challenging period where they face major life tasks, such as
establishing their personal identity, creating intimate relationships,
gaining independence and starting careers and families
]. A cancer diagnosis at AYA age can significantly
disrupt or delay ac hieving these mile ston es .
Understanding age-related differences in IOC can contribute
to the development of age-appropriate psychological
interventions and personalized care. Therefore, the primary aim of the
present study was to compare the IOC between AYA, adult
and elderly cancer survivors. Other study objectives were to
(1) investigate the influence of AYA characteristics on IOC
and (2) examine the association between IOC and HRQoL
Setting and population
This study is part of a longitudinal population-based
survey among lymphoma survivors registered within the
Netherlands Cancer Registry (NCR) in the South of
The Netherlands. The NCR records data of all patients
newly diagnosed with cancer in the southern part of
The Netherlands, an area with 2.3 million inhabitants.
The NCR was used to select all patients diagnosed with
NHL and HL between January 1, 1999 and January 1,
2009. We included patients aged ≥18 years at time of
diagnosis, with all subtypes of indolent (including
chronic lymphocytic leukaemia-like) and aggressive B
cell NHL and HL as defined by the International
Classification of Diseases for Oncology-3 codes
]. Deceased patients were excluded by linking the
NCR database with the Central Bureau for Genealogy.
Ethical approval for the study was obtained from the local
certified Medical Ethics Committee of the Maxima
Medical Centre Veldhoven.
Data collection took place in 2009 and was done within
]. PROFILES is a registry for the study of
the physical and psychosocial impact of cancer and its
treatment from a dynamic, growing population-based cohort of
both short- and long-term cancer survivors. PROFILES is
linked directly to clinical data from NCR. Details of the data
collection method have been previously described [
from the PROFILES registry are available for
noncommercial scientific research, subject to study question,
privacy and confidentiality restrictions, and registration (www.
In May 2009, patients between 6 months and 10 years after
diagnosis were included in the study. In November 2009,
patients diagnosed between May and August 2009 were also
invited to participate to broaden the number of short-term
Sociodemographic and clinical characteristics
Clinical information was available from the NCR that
routinely collects data on tumour characteristics, primary treatment
and patients’ background characteristics including sex and
date of birth. Comorbidity at time of survey was assessed
using a modified version of the Self-Administered
Comorbidity Questionnaire assessing the prevalence of 14
comorbidities including heart disease, stroke, high blood
pressure, COPD/asthma, diabetes, stomach disease, kidney
disease, liver disease, anaemia, depression, thyroid disease,
osteoarthritis, back pain, and rheumatoid arthritis [
Selfdesigned questions on educational level and marital status
were added to the questionnaire.
Impact of cancer
The 41-item IOCv1 was used in this study to measure specific
positive and negative IOC among long-term cancer survivors
]. Patients could indicate their level of agreement on
each statement from 1 (strongly disagree) to 5 (strongly
agree). The questionnaire was missing one item of the
‘negative self-evaluation’ subscale by mistake. This missing item
was imputed by the mean score of the ‘negative
self-evaluation’ subscale for each participant separately. A more recent
and comprehensive scaling of the IOCv1 questionnaire
yielded the 37-item IOCv2 . A valid algorithm was used
to convert the IOCv1 item responses into IOCv2 item scores
]. Two main summary IOC scales could be formed, a
positive (α = 0.74) and a negative (α = 0.82). The total scale
scores were calculated by averaging the item scores. Higher
scores on the positive and negative impact summary scales
indicate greater positive and negative impacts of cancer,
respectively. The two summary scales could be further
subdivided into eight subscales. The four positive subscales
comprise: altruism/empathy, health awareness, meaning of
cancer and positive self-evaluation. The negative subscales
are appearance concerns, body change concerns, life
interferences and worry.
Health-related quality of life
The validated Dutch version of the EORTC QLQ-C30 was
used to assess HRQoL. The questionnaire includes five scales
on physical (α = 0.79), role (α = 0.89), emotional (α = 0.90),
cognitive (α = 0.73) and social functioning (α = 0.79); and a
global health status/quality of life scale (α = 0.92). Answer
categories range from 1 (not at all) to 4 (very much). After
linear transformation, all scales range in score from 0 to 100.
A higher score means a better HRQoL [
Analyses were performed using Statistical Package for the
Social Sciences version 22 (SPSS), Chicago, IL, USA and
two-sided p values of <0.05 were considered statistically
significant. Differences in demographic and clinical
characteristics between respondents, non-respondents and cancer
survivors with unverifiable addresses and between the three age
groups (AYA, adults, elderly) were compared using
chisquare and analysis of variance (ANOVA), where appropriate.
ANOVAs were performed to investigate mean
differences between the age categories of lymphoma survivors
(independent variable) and the IOCv2 total and subscale
scores (dependent variables). To counteract the problem
of multiple comparisons (type-1 error), Bonferroni
correction was used (p < 0.001).
Multiple linear regression analyses were used to compare
AYA lymphoma survivor characteristics (independent
variables) and the mean IOCv2 summary and subscale scores
Additionally, multiple linear regression analyses were
performed to investigate the independent association between
IOCv2 total and subscales, and the HRQoL subscales for the
AYA sample. All demographic and clinical variables were
included as confounders; this was determined a priori based
Clinical and sociodemographic characteristics
Of the 1281 Dutch lymphoma survivors who met the
eligibility criteria and received a questionnaire, 861 (67 % response
rate) completed it.
A comparison of respondents, non-respondents and
survivors with unverifiable addresses, indicated that
nonrespondents were older, more recently diagnosed or less often
diagnosed with stage I disease, when compared to survivors
with unverifiable addresses and respondents.
Of all respondents, 11 % was AYA (18–35 years at
diagnosis), 59 % adult (36–64 years at diagnosis) and 30 % elderly
(65–84 years at diagnosis).
AYA survivors were more often diagnosed with HL and
more often with stage II disease and treated more often with a
combination of chemotherapy and radiotherapy, when
compared to older lymphoma survivors. Additionally, AYAs
reported fewer comorbid conditions, were married less often,
and more often had a higher educational level and a job
compared to adult and elderly lymphoma survivors (Table 1).
Associations between age and IOC
Significant differences in IOC between the age groups were
o b s e r v e d o n t h e p o s i t i v e i m p a c t s u m m a r y s c a l e
(F(2798) = 11.54, p < 0.001, eta2 = 0.03) and on the positive
subscales ‘health awareness’ (p < 0.001), ‘meaning of cancer’
(p = 0.001) and ‘positive self-evaluation’(p < 0.001). No
significant differences between the age groups were found on
negative IOC (Table 2). Sub analyses for HL survivors only
showed the same mean scale scores only statistical
significance of these findings could not be determined due to the
small number of elderly with HL (n = 10; data not shown).
Associations between AYA characteristics and IOC
Female AYAs scored significantly higher on the negative
impact summary scale and on the subscales ‘appearance
concerns’ and ‘positive self-evaluation’ compared to AYA males.
AYA (18–35 years), Adults (36–64 years), Elderly (65–84 years): age at time of diagnosis
NHL non-Hodgkin lymphoma, HL Hodgkin lymphoma education levels included low no/primary school, medium
lower general secondary education/vocational training, or high pre-university education/high vocational training/
a Patients under active surveillance and receive no therapy
AYA survivors with a partner scored higher on the negative
impact summary scale and ‘body change concerns’. AYAs
with more comorbidities reported more impact on ‘appearance
concerns’ and AYA survivors with elevated psychological
distress scored significantly higher on all IOCv2 scales, except
for the positive impact summary scale and the subscales
‘meaning of cancer’ and ‘positive self-evaluation’ (Table 3).
Associations between IOC and HRQoL among AYA lymphoma survivors
After adjusting for sociodemographic and clinical factors, the
negative impact summary scale was negatively associated
with all HRQoL scales (Table 4). The positive impact
summary scale was negatively associated with the EORTC
QLQC30 subscale ‘Emotional functioning’, which was mainly
caused by the items of the IOC subscales ‘altruism/empathy’
and ‘health awareness’.
This study showed that AYA, adult and elderly (non-)Hodgkin
lymphoma survivors experienced different types of positive
and negative IOC. Our results are in line with those of
previous studies among lymphoma survivors, which showed that
younger survivors had higher positive impact scores
compared to older survivors [
]. The positive IOC among
AYAs is reflected in more ‘health awareness’ (e.g. better
self-care), ‘meaning of cancer’ (e.g. giving direction in life)
and ‘positive self-evaluation’ (e.g. considering oneself to be a
role model). An explanation could be that AYAs make use of
more active and adaptive coping mechanisms and might be
more resilient compared to older cancer survivors [
Resilience is described as a personality profile characterized
by ‘positive adaptation’ after a stressful life event [
Moreover, studies show that younger cancer survivors report
higher levels of post-traumatic growth [
], which refers
to a set of positive changes occurring as a result of coping with
a traumatic event like cancer. AYAs might experience more
personal growth after their cancer experience compared to
older cancer survivors as they are more likely to give direction
in life and report adequate health competence after a cancer
experience . On the other hand, contrary to cancer
survivors, healthy older adults are more resilient than young adults
In contrast to previous studies [
5, 11, 29
], showing that
younger cancer survivors had higher negative impact scores
when compared to older survivors, our results showed no
significant differences for negative impacts of cancer between
the three age groups. One possible explanation could be that
the majority of lymphoma survivors did not undergo invasive
or surgical treatments and they experienced, for example, less
‘body change concerns’ or ‘appearance concerns’ compared
to survivors treated for other types of cancer. Another
explanation could be that the IOC questionnaire lacks important
age-specific concerns. Development of more age-specific
questionnaires will make it possible to accurately identify
IOC and prioritize the perceived age-specific needs of cancer
Female AYAs scored significantly higher on the negative
IOC, compared to young men. This gender difference is
largely consistent with previous studies on long-term cancer
survivors of all ages [
]. A possible explanation could be the
presence of higher rates of psychological distress in the female
population in general, as opposed to men [
]. This sex
difference may reflect a difference in willingness to report
distress among men, but could also occur because women
tend to use more emotional coping styles [
negative IOC among female AYAs is reflected in more
‘appearance concerns’ compared to men. This is in line with the
literature which shows that especially young women, report
more experiences associated with cancer-related appearance
and body image concerns, than young men cancer survivors
]. For example, women are more aware of their looks, and
may feel more disfigured than men. On the other hand, female
AYAs reported higher scores on the positive subscale ‘positive
self-evaluation’. This means that young women consider
themselves as a cancer survivor and/or role model, and may
feel a sense of pride from surviving cancer. A possible
explanation for this finding could be the tendency of women to
NHL non-Hodgkin lymphoma, HL Hodgkin lymphoma; Education levels included low = no/primary school, medium = lower general secondary
education/vocational training, or high = pre-university education/high vocational training/university
HADS Hospital Anxiety Depression Scale
*p < 0.05; **p < 0.01
score higher on post-traumatic growth. This explanation
suggests that men and women differ in their responses to a
traumatic (cancer) experience [
]. Moreover, an American study
found that the post-traumatic growth scores of severely
traumatized women were twice as high as those of traumatized
men. It suggests that these events have greater effect on
women, in that women may be more capable than men of learning
or benefiting from difficult life experiences like surviving
The majority of AYA cancer survivors in this study
reported that having more psychological distress in general life
results in higher scores on the negative IOC summary scale.
This was reflected in more ‘appearance concerns’, ‘body
change concerns’, ‘life interferences’ and ‘worry’. On the
other hand, more psychological distress had a more positive
impact on the positive subscales ‘altruism/empathy’ and ‘health
awareness’. One possible explanation for this conflicting
finding could be that cultural differences between lymphoma
survivors living in the USA (where the IOC questionnaire was
developed) and Dutch lymphoma survivors affected the IOC
]. Living in different cultures creates other
psychological resources that influence health. Since the sense of
personal control is more prevalent in North America than in
Europe, American survivors are more likely to alter
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perceptions of the cancer experience in a more positive way
]. To give an example, the subscale ‘health awareness’ is
seen as something positive in t he USA, while in
The Netherlands, we may experience it as something more
]. Moreover, the conflicting finding that AYAs
with elevated levels of distress experience both negative and
positive IOC may indicate the coexistence of the unique
negative and positive influences of cancer further in life. This
gives reason to belief that mental health is not a single
continuum with negative impacts (distress) on one, and positive
impacts (growth) on the other side, but rather represents a
bivariate construct with two separate dimensions [
AYA cancer survivors with a partner scored significantly
higher on the negative IOC summary scale and the subscale
‘body change concerns’, compared to AYAs without a partner.
This finding seems very age-related, as previous studies on the
general cancer population of all ages show that having a
partner reduces the negative impacts of cancer [
]. A first
possible explanation could be that AYAs are in a vulnerable
phase of life, in which intimate and sexual relationships are
evolving. Especially cancer residual symptoms like ‘body
change concerns’ and altered body image could have a more
negative impact on AYAs with a partner when compared to
AYAs without a partner . Feelings of being unattractive,
different or imperfect, or possible impairments in social skills
could be barriers for a romantic relationship and may lead to
more negative impacts of cancer [
]. Second, AYAs are in a
phase of life in which plans for having children may arise.
Especially AYAs with a partner may worry about infertility
concerns after their cancer treatment, more than AYAs without
a partner. Previous research shows that more than fifty percent
of AYAs with a partner reported that their cancer experience
had a negative impact on their plans for having children [
Third, AYA cancer survivors with a partner may experience
feelings of guilt and shortcoming, because they Bdragged^
their partner into a medical situation with an uncertain future.
Discordant feelings between the AYA cancer survivors and
their partner could arise and have a negative impact on the
survivors life [
]. These factors may contribute to higher
negative IOC scores among AYAs with a partner.
Consistent with other studies [
], our findings indicate
that an individual’s perception of the positive and negative
IOC on various life domains is related to their functional and
global health status. Especially the negative IOC is of
influence and is significantly associated with HRQoL. These
findings provide evidence for the notion that negative experiences
may be more heavily related to overall well-being and
functioning than positive experiences of cancer among AYAs. A
possible explanation could be the fact that perceived negative
outcomes may be more heavily weighted in determining
psychological adjustment than positive change [
as female AYAs, AYAs with elevated levels of distress, and
AYAs with a partner reported higher levels of negative IOC,
they are considered a Bhigh-risk^ population of having a lower
HRQoL. Especially these groups of AYA lymphoma
survivors should be screened for their HRQoL and should be more
intensively guided by health care practitioners.
This study has a few limitations. First, although
information was present concerning demographic and clinical
characteristics of the non-respondents and survivors with
unverifiable addresses, it remains unknown why non-respondents
declined to participate in the study. Secondly, it cannot be ruled
out that part of the differences in IOC subscale scores between
the age groups are a result of the differences in tumour types
diagnosed (and accompanied treatment regimens) between
younger and older patients. Older patients more often have
indolent NHL with a wait and see policy (and therefore
probably more late effects of the cancer itself), while younger
patients more often have aggressive NHL or HL and therefore
receive a combination of chemo- and radiotherapy. However,
sub analyses for HL survivors only showed the same mean
IOC scale scores as for the total lymphoma sample, indicating
that our results are mainly caused by age. Third, the
crosssectional design of our study limits the determination of causal
associations between the study variables. Fourth, although the
IOCv1 and v2 scales showed good psychometric properties
among the whole age range, both do not include domains
related to developmental issues (e.g. lagging behind healthy
peers; difficulties to return to school or problems with getting
a job) which are particularly important for AYAs. Fifth, no
data were available of healthy AYAs as the IOC is a
cancerspecific measure. The question remains whether young people
in general experience more positive outcomes than older
people or that our results indicate a cancer-specific effect of age
]. Sixth, the study results cannot be generalized for the total
AYA population as Hodgkin’s disease has a relatively good
prognosis, what may give a more positive indication,
compared to other types of cancer.
To promote the positive IOC among AYAs, future research
in the area of cognitive and behavioural interventions (e.g.
cognitive re-framing) is needed to determine if positive
reinterpretation of a negative traumatic event could subsequently
lead to adequate resilience skills and coping mechanisms,
more positive growth, improved HRQoL and thereby possibly
indirectly diminishing the negative IOC. For example, to
improve the coping mechanisms of AYAs, psychological
interventions directed at positive reframing of cancer should see
the cancer experience as an opportunity to negotiate new
challenges, re-evaluate life goals and priorities, and enhance
selfknowledge may be particularly relevant and effective,
especially for younger survivors. Additionally, recommended
psychosocial intervention programs could include among others
positive peer support, as well as psychoeducational
interventions and therapies that focus on engaging cancer patients and
facilitating change, by encouraging patients’ flexibility to
accept what cannot be altered and committing themselves to
what can be achieved (e.g. ‘Acceptance and Commitment
]. On the other hand, to diminish or prevent
negative IOC, health care providers may offer age-appropriate
information to AYAs [
], which may help them to get a
more coherent understanding of their illness [
51, 60, 61
To conclude, this study highlights the importance of the
specific IOC of AYAs according to their life phase, as
compared to adults and the elderly lymphoma survivors. To
address the unique needs of AYAs, research should focus on
developing questionnaires and interventions more coherent
to the age of the cancer survivor. Randomized intervention
studies with large samples that focus on psychosocial
outcomes are needed to establish evidence-based
psycho-oncological interventions for AYAs. Healthcare practitioners need
to become aware of the specific age-related impacts of cancer
and developmental issues that AYA, adult and elderly
lymphoma survivors are dealing with, even years after diagnosis. By
keeping this in mind, healthcare practitioners can contribute to
a better HRQoL and a more adaptive and supportive
healthcare system for the lymphoma survivors.
Compliance with ethical standards All procedures performed in
studies involving human participants were in accordance with the ethical
standards of the institutional and/or national research committee and with
the 1964 Helsinki Declaration and its later amendments or comparable
Conflict of interest The authors declare that they have no competing
Informed consent Informed consent was obtained from all individual
participants included in the study.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a link
to the Creative Commons license, and indicate if changes were made.
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