Breast Cancer Research and Treatment

https://doi.org/10.1007/s10549-018-4894-8

EPIDEMIOLOGY

Sexual health in long-term breast cancer survivors

Sara V. Soldera1,2 · Marguerite Ennis3 · Ana E. Lohmann4 · Pamela J. Goodwin4

Received: 9 July 2018 / Accepted: 14 July 2018

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
Purpose Sexual dysfunction is reported in women with breast cancer (BC). It is unclear whether symptoms persist over time
as data comparing long-term survivors to controls are lacking. We compared sexual functioning in long-term breast cancer
survivors (BCS) to controls and determined the impact of adjuvant therapy on sexual health.
Methods A cohort of women with localized BC (1989–1996) was prospectively followed. BCS and controls (2005–2007)
completed self-reported questionnaires. Sexual health was measured with the Sexual Activity Questionnaire (SAQ). Vaso-
motor, gynecological, and bladder symptoms were scored using the Menopausal Symptom Scale. Regression analysis was
used to compare groups, with adjustment for age and secondly menopausal status.
Results BCS (n = 248, 87%) and controls (n = 159, 95%) completed the SAQ at a median time from diagnosis of 12.5 years.
BCS were older (62 vs 59 years, p = 0.0004) and more likely to be menopausal (94 vs 86%, p = 0.0025). Sexual activity did
not differ significantly between BCS and controls, but when adjusted for menopausal status, pre/peri-menopausal BCS were
less likely to be sexually active than pre/peri-controls (odds ratio OR 0.12, p = 0.012). In those sexually active, no significant
differences were noted on the SAQ Pleasure, Discomfort, and Habit scales. BCS reported worse gynecological symptoms
and pre/peri-menopausal patients had more bladder complaints (standardized effect size 0.36 p = 0.002 and 1.11, p = 0.011).
Adjuvant treatments were not significantly associated with sexual function, but BCS treated with chemotherapy reported
worse gynecological symptoms.
Conclusion Sexual health and uro-genital symptom counseling should be provided to BCS, particularly pre/peri-menopausal
patients, even at long-term follow-up.

Keywords Breast cancer · Sexual function · Chemotherapy · Endocrine therapy · Survivorship · Sexual Activity
Questionnaire

Introduction

Electronic supplementary material The online version of this Over the last decades, the number of breast cancer survi-
article (https​://doi.org/10.1007/s1054​9-018-4894-8) contains vors (BCS) has increased [1]. Improved outcomes in this
supplementary material, which is available to authorized users. population are in part attributed to more effective adjuvant
* Sara V. Soldera therapies [2]. While increasing cure, treatments inflict sub-
Sara.Soldera@usherbrooke.ca stantial symptom burden on patients. Given improvement
in outcomes, survivorship issues including long-term ther-
1
Department of Hematology and Oncology, CISSS apy-related toxicities have become increasingly important.
Montérégie Centre/Hôpital Charles‑Lemoyne, Centre Affilié
de l’Université de Sherbrooke, Greenfield Park, Canada
Sexual health in particular is now recognized as an area of
2
concern for BCS [3, 4] and an aspect of care that is often
Lunenfeld Tanenbaum Research Institute, Mount Sinai
Hospital, University Health Network, University of Toronto,
overlooked by healthcare professionnals [4].
Toronto, Canada Several studies have reported significant sexual dysfunc-
3
Applied Statistician, Markham, Canada
tion in the few years following diagnosis [5–13]. It remains
4
unclear whether this effect persists over time, as high qual-
Division of Medical Oncology and Hematology, Division
of Clinical Epidemiology, Department of Medicine,
ity long-term data are sparse and conflicting [14–16]. Dis-
Lunenfeld‑Tanenbaum Research Institute, Mount Sinai tinguishing changes in sexual health related to the normal
Hospital, University of Toronto, Toronto, Canada

13
Vol.:(0123456789)

aging process versus those associated with BC diagnosis
and treatment is also a challenge. Sexually activity declines
and sexual complaints increase with advancing age [17]. To
date, few studies have investigated sexual function in BCS
compared to healthy controls and most were limited by small
numbers and comparison to historical data [13, 16, 18, 19].
The impact of adjuvant treatments on sexual health remains
controversial with varying reports on the effect of chemo-
therapy and hormonal agents [5, 6, 9, 10, 14, 16, 18, 20–28].
The primary aims of this study are threefold: (1) to
evaluate sexual health in long-term BCS compared to aged-
matched controls, (2) to determine the impact of chemother-
apy and endocrine therapy on sexual functioning, and (3) to
compare related symptoms such as gynecological, vasomo-
tor, and bladder complaints between groups to potentially
explain the source of any differences in sexual function.
Methods
Study population
A cohort of women with newly diagnosed localized BC was
recruited from three metropolitan hospitals at the University
of Toronto between 1989 and 1996 and followed prospec-
tively for disease outcomes [29]. This cohort was previously
described [29]; it included English-speaking women aged
< 75 years with completely resected localized invasive BC
(T1-3, N0-1, M0). Exclusion criteria included the use of
neoadjuvant chemotherapy, presence of serious coexisting
medical conditions, and living more than 1 h from a study
site. Information regarding diagnosis, stage, pathology, and
treatments and cancer outcomes was obtained from medical
records.
Survivors were re-contacted from 2005 to 2007 and those
without distant BC recurrence or a new cancer diagnosis
were enrolled in a survivorship study. Between 2007 and
2008, a control group was recruited among women under-
going screening mammograms at one of the three centres.
Those with a history of invasive cancer or undiagnosed
abnormalities on screening mammogram were excluded. To
the extent possible, controls were age-frequency matched to
the BCS. For the current study, we included all long-term
BCS and controls who completed the Sexual Activity Ques-
tionnaire (SAQ) in the survivorship study.
Study questionnaires
The SAQ [30], a validated standardized tool, was used to
assess the frequency of sexual activity and three dimen-
sions of sexual function: pleasure (SAQ-P), discomfort
(SAQ-D), and habit (SAQ-H), with higher scores indicat-
ing greater pleasure, discomfort, and greater frequency of
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Breast Cancer Research and Treatment
sexual activity than usual, respectively (Table S3). Vaso-
motor, gynaecological complaints, and bladder symptoms
were evaluated based on the Menopausal Symptom Scale
of the Breast Cancer Prevention Trial Symptom Check List
in which symptoms are graded from 0 to 4 of increasing
intensity (Table S3) [31, 32]. Specific items consisted of
hot flashes and night sweats (vasomotor subscale), vagi-
nal dryness, genital irritation, and pain with intercourse
(gynaecological subscale), difficulty with bladder control
while laughing or crying and difficulty with bladder control
at other times (bladder symptom subscale).
Statistical analysis
Subject and treatment-related characteristics were reported
as frequencies or means with standard deviations (SD)
and compared using t tests and Chi square tests. Despite
matching, BCS and controls differed in terms of age and
menopausal status. Given that premature menopause is a
well-documented risk of adjuvant chemotherapy in younger
women and has been demonstrated to contribute to sexual
dysfunction, we adjusted only for age in our primary analy-
ses and added adjustment for menopausal status in second-
ary analyses. We compared the sexual activity of BCS and
controls using logistic regression with odds ratios (OR) as
summary measures. For other outcomes, we used linear
regression with standardized effect sizes (StES) calculated
as the regression-adjusted difference relative to controls,
divided by the SD of the controls. Age was modelled as
a quadratic polynomial to allow for curved relationships.
Adjustment for menopausal status included testing for an
interaction between it and subject type. For adjuvant treat-
ment (hormone therapy, chemotherapy, both, neither), an
omnibus test of any difference between treatment groups and
controls was examined before looking at individual compari-
sons. p values ≤ 0.05 were called significant.
The research ethics committee at the Mount Sinai Hospi-
tal approved this study and all participants provided written
informed consent.
Results
Patient demographics
Between 1989 and 1996, 535 women newly diagnosed
with BC participated in the original cohort. Two hundred
and eighty-five survivors were enrolled into the survivor-
ship study a median of 12.5 years after diagnosis (range
9.4–17.6 years, Fig. 1) [29]. Enrolled survivors were similar
to the remaining cohort except for lower body mass index
(BMI) and cancers of lower T and N stage, as expected.
Of the participating survivors, 248 (87%) completed the
Breast Cancer Research and Treatment
Fig. 1  Consort diagram
Newly diagnosed BC
(n=535)
Breast cancer survivors
(n=285)
BCS completed SAQ (n=248)
SAQ forming the group under study. 37 survivors who did
not complete the SAQ were older on average (mean 65 vs
62 years p = 0.041). One hundred and sixty-seven non-BC
controls were also enrolled into the survivorship study with
158 (95%) completing the SAQ.
Disease and treatment related characteristics of BCS are
summarized in Table 1 and survivorship participant charac-
teristics are described in Table 2. Despite matching for age,
breast cancer survivors were slightly older and more likely to
be post-menopausal than controls (mean age 62 and 59 years
p = 0.0004; 94 and 86% post-menopausal, p = 0.0025).
Sexual health
After adjusting for age, no difference in sexual activity
between BCS and controls was found, (adjusted OR 0.68,
p = 0.073, Supplementary Table S1). The most common rea-
sons for lack of sexual activity are listed in Supplementary
Table S2. Sexual activity seemed to decline in both groups at
a similar rate with advancing age (Fig. 2a). In those sexually
active, no significant age-adjusted differences were noted on
the SAQ-P, SAQ-D, and SAQ-H subscales (Fig. 2b), with
adjusted standardized effect sizes (StES) of 0.08 (p = 0.56)
for SAQ-P; 0.21 (p = 0.14) for SAQ-D and − 0.09 (p = 0.49)
Excluded
Distant Recurrence (n=33)
Death (n=123)
Other cancer (n=28)
Moved away (n=14)
Declined parcipaon (n=29)
Unable to locate (n=23)
Non-breast cancer controls
(n=167)
Non-breast cancer controls
completed SAQ
(n=159)
for SAQ-H. Age itself explained a significant amount of the
variation in SAQ-D but not in SAQ-P or SAQ-H.
When adjustment was made for menopausal status, there
was a significant interaction between subject type and meno-
pausal status for sexual activity (p = 0.024, Fig. 3a), with
pre/peri-menopausal BCS less likely to be sexually active
than pre/peri-controls (OR = 0.12, p = 0.012) while no dif-
ference in sexual activity was seen between postmenopausal
groups (OR = 0.78, p = 0.28). For the SAQ subscales, adjust-
ment for menopausal status was not significant.
Menopausal symptoms
BCS reported higher age-adjusted scores (greater symp-
toms) than controls on the gynecological symptom scale
(StES 0.36 p = 0.0024, Fig. 2c) with vaginal dryness being
of particular concern (age-adjusted StES 0.41 p = 0.0007).
BCS also reported higher scores on the bladder symptom
scales (age-adjusted StES 0.27 p = 0.045) while vasomotor
complaints were not significantly different between groups
(age-adjusted StES 0.07 p = 0.5).
When further adjustment was made for menopau-
sal status, a significant interaction was noted for the
bladder symptom scale (p = 0.049, Fig. 3b) with pre/
peri-menopausal BCS reporting worse scores than pre/
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 Breast Cancer Research and Treatment

Table 1  Disease-related characteristics overall and according to adju- Discussion

vant treatment in breast cancer survivors
Variable BCS BCS by adjuvant treatment Overall, our study found that BCS report similar rates of
(n = 248) sexual activity compared to controls with activity decreas-
None Horma Chemoa Both
(n = 84) (n = 67) (n = 71) (n = 26) ing with age in both groups. Sexually active women report
statistically similar scores on all SAQ subscales (pleas-
T (n, %)
ure, discomfort, and habit). Furthermore, adjuvant therapy
1 155 (63) 69 (82) 50 (75) 26 (37) 10 (39)
did not impact these outcomes. This suggests a natural
2 64 (26) 8 (10) 13 (19) 33 (47) 10 (39)
decline in function in part associated to advancing age.
3 8 (3) 0 (0) 0 (0) 5 (7) 3 (11)
Interestingly, adjustment for menopausal status revealed
X 21 (8) 7 (8) 4 (6) 7 (10) 3 (11)
that pre/peri-menopausal BCS are significantly less likely
N (n, %)
to be sexually active than pre/peri-menopausal controls
Negative 191 (77) 83 (99) 63 (94) 33 (46) 12 (46)
and report persistently worse bladder symptoms. We also
Positive 57 (23) 1 (1) 4 (6) 38 (54) 14 (54)
found that gynecological complaints, in particular vaginal
ER/PR (n, %)
dryness, are more pronounced in BCS even over a decade
Positive 176 (71) 50 (60) 54 (81) 50 (70) 22 (85)
after diagnosis, particularly in those treated with prior
Negative 34 (14) 11 (13) 5 (8) 18 (25) 0 (0)
chemotherapy. These findings may represent the effect of
Missing 38 (15) 23 (27) 8 (11) 3 (5) 4 (15)
accelerated vaginal atrophy due to treatment-induced hor-
Surgery (n, %)
monal changes and explain in part greater sexual dysfunc-
Mastectomy 61 (25) 18 (21) 11 (16) 23 (32) 9 (35)
tion in pre/peri-menopausal patients.
Lumpectomy 187 (75) 66 (79) 56 (84) 48 (68) 17 (65)
The rate of sexual activity in our study was in line with
Radiation (n, %)
normative data in which 72 women aged 56–65 years
Yes 69 (28) 25 (30) 14 (21) 22 (31) 8 (31)
with a strong family history of BC or from the general
No 179 (72) 59 (70) 53 (79) 49 (69) 18 (69)
population completed the SAQ (59.7% sexually active,
BCS breast cancer survivor, chemo chemotherapy, ER estrogen recep- SAQ-P median score 11, and SAQ-D median score 1) [30].
tor, horm hormonal therapy, PR progesterone receptor Sexual activity in BCS has also been examined in past
a
Chemotherapy consisted of cyclophosphamide, methotrexate, and studies with conflicting results. Ganz et al. [14] investi-
fluororacil (76%) and cyclophosphamide, adriamycin/epirubicin, and gated sexual health in BCS in a longitudinal QOL study.
5-fluorouracil (23%) and hormonal therapy consisted of tamoxifen
Approximately 6 years after diagnosis, women reported a
significant decline in frequency of sexual activity without
any change in the frequency of dyspareunia, sexual inter-
peri-menopausal controls or the other subjects combined est, or body image, leading the authors to conclude that
(StES 1.11, p = 0.011 and 1.15 p = 0.003, respectively). these changes were likely associated with normal aging.
Raggio and colleagues [15] investigated sexual mor-
bidity in a cross-sectional study of 83 BCS at a median
Adjuvant therapy of 7 years from diagnosis and found that 48% of women
had been sexually active during the past 4 weeks and that
After adjusting for age, there were no significant differ- 60% of sexually active participants met criteria for sex-
ences in the rates of sexual activity in BCS relative to con- ual dysfunction as per the Female Sexual Function Index
trols according to different adjuvant treatments (omnibus (FSFI), representing worse sexual function compared to
test p = 0.39), nor in the SAQ subscales (Supplementary previously published norms for healthy post-menopausal
Table S1). Gynecological symptoms, particularly “vaginal women. Reported sexual activity was in line with our
dryness” and “difficulty with bladder control when laugh- results (45%) and given that sexual function was assessed
ing or crying,” differed between adjuvant treatment groups with a different measuring tool, it is hard to interpret these
and controls with highest scores in patients who received results. The FSFI has not been formally compared to the
chemotherapy (gynecological scale StES 0.52, p = 0.0022; SAQ, but has been found to have more adequate psycho-
vaginal dryness StES 0.58, p = 0.0004 and laughing or cry- metric properties and coverage of various dimensions of
ing, StES 0.46, p = 0.014). sexual function, which could explain in part their reports
In the subset of menopausal patients, further analyses of relatively higher rates of sexual dysfunction compared
were performed adjusting for age, time since menopause, to our results [33].
and current use of exogenous hormones to investigate Finally, Davis et al. [16] conducted a study of meno-
the impact of these factors on sexual health; results were pausal symptoms in BCS who had not received prior
unchanged.

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Breast Cancer Research and Treatment

Table 2  Characteristics of breast cancer survivors at long-term follow-up and non-breast cancer controls
Variable BCS Controls p1 BCS by adjuvant treatment
(n = 248) (n = 159)
None Horm Chemo Both Omnibus p2
(n = 84) (n = 67) (n = 71) (n = 26)

Age, year
Mean (SD) 62 (8.1) 59 (7) 0.0004 63 (8.3) 66 (8.1) 57 (5.5) 59 (6.4) < 0.0001
BMI
Mean (SD) 26 (4.6) 25 (4.5) 0.079 26 (4.7) 26 (4.2) 27 (4.8) 26 (5.3) 0.15
Menop status
Pre/peri (%) 14 (6) 23 (15) 0.0025 7 (8) 3 (4) 4 (6) 0 (0) 0.027
Post (%) 234 (94) 136 (85) 77 (92) 64 (96) 67 (94) 26 (100)
Age at menop
Mean (SD) 48 (5.2) 50 (4.8) 0.0031 50 (5.3) 49 (5.9) 46 (3.9) 46 (3.9) < 0.0001
Exogenous ­hormones3
Yes (%) 9 (4) 24 (18) < 0.0001 4 (5) 4 (6) 1 (2) 0 (0) 0.0002
No (%) 225 (96) 112 (82) 73 (95) 60 (94) 66 (98) 26 (100)
Employment
Full-time (%) 92 (37) 75 (47) 0.044 34 (41) 17 (25) 30 (42) 11 (42) 0.053
Other* (%) 156 (63) 84 (53) 50 (59) 50 (75) 41 (58) 15 (58)
Marital status
Other** (%) 89 (36) 50 (31) 0.36 32 (38) 26 (39) 21 (30) 10 (39) 0.62
Married (%) 159 (64) 109 (69) 52 (62) 41 (61) 50 (70) 16 (61)
Living situation
Alone (%) 54 (22) 35 (22) 21 (25) 18 (27) 11 (16) 4 (15)
Partner only (%) 106 (43) 67 (42) 0.87 42 (50) 37 (55) 20 (28) 7 (27) 0.0002
Partner/kids (%) 51 (20) 37 (23) 10 (12) 5 (8) 28 (39) 8 (31)
Other (%) 37 (15) 20 (13) 11 (13) 7 (10) 12 (17) 7 (27)

BCS breast cancer survivors, both chemotherapy and hormonal therapy, BMI body mass index, chemo chemotherapy, horm hormonal therapy,
LTFU long-term follow up, menop menopausal, SD standard deviation
*Part time/retired/unemployed
**Single/widowed/divorced
1
p value for t test or Chi square test that outcomes for BCS and controls are equal
2
p value for the omnibus test that outcomes for all four treatment groups plus the control group are equal
3
Current use of estrogen/progestin among post-menopausal subjects

chemotherapy (mean 5.8 years since diagnosis) compared
to community controls and established that cancer survi-
vors reported higher scores (greater dysfunction) on the
vasomotor and sexual domains of the Menopause-Specific
Quality of Life Questionnaire (MenQOL). Of note, the
MenQOL sexual domain explores sexual desire, vaginal
dryness, and avoidance of intimacy.
There are several limitations to our study. Information
regarding sexual function prior to BC diagnosis and treat-
ment is lacking. Additionally, despite age matching, BCS
and controls differed in terms of age and menopausal status.
This difference was addressed by adjusting data according to
these two important variables. Several questions also remain
unanswered. Median age in our sample (62 years) limited
the study of sexual health in younger BCS. Furthermore, as
aromatase inhibitors were not widely used at the time of our
initial cohort, our results are restricted to adjuvant endocrine
treatment with tamoxifen.
Conclusion
Long-term sexual health was similar in post-menopausal
BCS and controls with similar decline in sexual activity with
increasing age, however, pre or peri-menopausal patients
report lower rates of sexual activity and greater bladder
symptoms. Adjuvant chemotherapy is associated with more
frequent gynecological symptoms over a decade after BC
diagnosis. BCS should, therefore, be counseled about sexual
function and gynecological symptoms during routine medi-
cal visits, particularly those who remain pre/peri-menopau-
sal at long-term follow up. Interventions aimed at improving

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 Breast Cancer Research and Treatment

(a) Probability of being sexually active

N = 407
1.0
Subject-type P = 0.072
0.8
0.6
0.4

Red: BC survivor
0.2

Black: Control
0.0

40 50 60 70 80

Age

(b) SAQ Pleasure factor SAQ Discomfort factor SAQ Habit factor
N = 207 N = 207 N = 207

3.0
6

Subject-type P = 0.56 Subject-type P = 0.14 Subject-type P = 0.49

15

2.0
4
10

Red: BC survivor

1.0
2

Black: Control
5

0.0
0

40 50 60 70 80 40 50 60 70 80 40 50 60 70 80

Age Age Age

(c) BCPT Gynecological symptom scale BCPT Bladder symptom scale BCPT Vasomotor symptom scale
N = 407 N = 407 N = 407
4

Subject-type P = 0.0024 Subject-type P = 0.045 Subject-type P = 0.5

3

Red: BC survivor
2

Black: Control
1

1
0

40 50 60 70 80 40 50 60 70 80 40 50 60 70 80

Age Age Age

Fig. 2  Sexual activity (a) and function (b) in breast cancer survivors and non-breast cancer controls as per the Sexual Activity Questionnaire
(SAQ), and vasomotor, gynecological, and bladder symptoms (c) as per the BCPT Symptom Check List

13
Breast Cancer Research and Treatment

(a) Probability of being sexually active (b) BCPT Bladder symptom scale
N = 407 N = 407
Interaction P = 0.024 Interaction P = 0.049

4
1.0

Pre/peri Pre/peri
0.8

Post Post

3
BC survivor BC survivor
Control Control
0.6

2
0.4

1
0.2
0.0

0
40 50 60 70 80 40 50 60 70 80

Age Age

Fig. 3  Sexual activity (a) and the BCPT bladder symptom scale (b) in breast cancer survivors and non-breast cancer controls, after adjustment
for age and menopausal status including an interaction between subject type and menopausal status

uro-gynecological health could further improve sexual func-
tion and quality of life in this population.
Funding This work was supported by The Breast Cancer Research
Foundation and Hold ‘EM For Life Translating Research Discoveries
Into Breast Cancer Cures. The study sponsors have no role in the design
of the study, the collection, analysis, and interpretation of the data, the
manuscript writing, or the decision to submit for publication.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Ethical approval The research ethics committee at the Mount Sinai
Hospital approved this study. All procedures performed in studies
involving human participants were in accordance with the ethical stand-
ards of the institutional and/or national research committee and with
the 1964 Helsinki declaration and its later amendments or comparable
ethical standards.
Informed consent Written informed consent was obtained from all
individual participants included in the study.
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