CLIMACTERIC 2009;12:404409

Climacteric symptoms in women

undergoing risk-reducing bilateral
salpingo-oophorectomy
A. Benshushan, N. Rojansky, M. Chaviv, S. Arbel-Alon, A. Benmeir, T. Imbar and
A. Brzezinski
The Hebrew-University Hadassah Medical School, Department of Obstetrics and Gynecology,
Jerusalem, Israel
Key words: MENOPAUSE, RISK-REDUCING BILATERAL SALPINGO-OOPHORECTOMY, CLIMACTERIC SYMPTOMS

ABSTRACT
Background The most effective strategy for prevention of ovarian and breast cancer in
high-risk women is bilateral salpingo-oophorectomy. The inevitable consequence of the
procedure is early menopause with the associated climacteric symptoms. Little is known
about the nature of the symptoms in women who undergo risk-reducing bilateral
salpingo-oophorectomy.
Objectives To compare the nature, frequency, severity, duration, and overall effects of
climacteric symptoms in a group of women who underwent preventive bilateral
salpingo-oophorectomy as compared to women who experienced natural menopause.
Methods Forty-eight women at high risk for ovarian cancer who had risk-reducing
bilateral salpingo-oophorectomy were compared to 60 postmenopausal women who
had natural menopause. The participants were interviewed about their climacteric
complaints, thoughts and feelings regarding the surgical procedure and their general
well-being. The climacteric symptoms were evaluated by a modified Greene Climacteric
Scale.
Results Surgical menopause, as compared to natural menopause, was associated with
more severe psychological, vasomotor and somatic climacteric symptoms (total score
17.36 vs. 8.65, respectively, p 5 0.001) and more significant sexual dysfunction (1.848
vs. 0.900, respectively, p 5 0.01). On a 010 scale, the satisfaction rate from the
surgical procedure was 8.23 + 2.21. The surgery did not affect the perceived quality of
life (p 0.347) and decreased the score of anxiety and cancer fear (from 7.75 + 3.31
preoperatively to 2.94 + 3.08 postoperatively, p 5 0.001).
Conclusions Risk-reducing bilateral salpingo-oophorectomy as compared to natural
menopause is associated with more severe climacteric symptoms. However, the
procedure does not interfere with the overall perceived quality of life and improves
the perception of cancer risk.

Correspondence: Professor A. Brzezinski, Hadassah University Hospital, Department of Obstetrics and Gynecology, EinKerem, Jerusalem, 91120 Israel

ORIGINAL ARTICLE
2009 International Menopause Society
DOI: 10.1080/13697130902780846

Received 29-10-2008
Revised 22-01-2009
Accepted 27-01-2009

Prophylactic salpingo-oophorectomy and climacteric symptoms

INTRODUCTION
Climacteric symptoms adversely affect womens
quality of life and occupational functioning during
the menopause transition1,2. Vasomotor symptoms (i.e. hot flushes, night sweats and palpitations), psychological symptoms (i.e. dysphoria,
anxiety, irritability, instability, sleep disorders and
decreased libido) and urogenital atrophic symptoms are the early signs of estrogen deficiency.
Most women experience some climacteric symptoms (predominantly vasomotor symptoms) for 6
months to 2 years3,4. During natural menopause,
the onset of these menopausal symptoms is often
gradual over a period of a few months and they
resolve in 8590% of women within 45 years5. It
is a common clinical observation that, following
surgical menopause, these symptoms appear
abruptly and may be more severe in their intensity
and frequency, but this clinical observation has
not been adequately validated. There is also not
enough information about the attitudes and
tolerance of the climacteric symptoms by women
who undergo prophylactic bilateral salpingooophorectomy (BSO) as a measure to prevent
reproductive malignant tumors. We therefore
examined retrospectively the type, severity and
duration of climacteric symptoms in a group of
women who had preventive BSO as compared to
women who underwent natural menopause.

MATERIAL AND METHODS

One hundred and eight women were included in
this retrospective analytic study. We have compared a group of patients who underwent riskreducing BSO at The Hadassah-Hebrew
University Medical Center to a group of women
with natural menopause who attended the
menopause clinic in the same time period.
The study group consisted of 48 women who
underwent risk-reducing BSO and who agreed to
participate in the study. Thirty-three of them were
premenopausal at the time of risk-reducing BSO
and 15 were postmenopausal. The control group
included 60 postmenopausal women who visited
our gynecologic menopause clinic for various
climacteric complaints or for routine check-up
and had been amenorrheic for at 6 months.
Hormone therapy (HT) users were excluded from
this survey since women at risk for ovarian cancer
mainly avoid the use of HT, due to concern about
a possible additional risk of breast cancer.
We constructed a questionnaire which included
demographic and gynecologic data, information

Climacteric

Benshushan et al.
on the results of the surgery, and menopausal
symptoms at four time points: 1 month, 6 months,
and 1 year after the surgery or the womans last
menstrual period, and at the time of interview. We
have used a modified Greene Climacteric Scale6,7
for this evaluation. The questionnaires were
completed at an interview (performed by a
qualified single interviewer) after obtaining
informed consent for the survey. A few of
the questionnaires were filled via telephone
interview.

Statistical analysis
The w2 test was used to compare qualitative or
categorical variables. The T test was used for the
quantitative variables. The paired T test was used
to compare variables before and after within each
group. For evaluation of climacteric symptoms
over time, we used repetitive measures based on
the Greene Climacteric Scale7. The menopausal
symptoms were divided into three subgroups:
vasomotor symptoms, psychological symptoms,
and somatic symptoms (e.g. vaginal dryness).
The Greene Climacteric Scale score for each
subgroup at a given time was calculated by a
summation of grades given for each variable (0,
no symptoms; 1, mild symptoms; 2, moderate
symptoms; 3, severe symptoms). The results
presented for each subgroup are an evaluation of
the severity of the symptoms.
The data were analyzed using the Statistical
Package for Social Science (SPSS Base).

RESULTS
The demographic and clinical characteristics of
the study and the control groups are presented in
Table 1. These characteristics varied significantly
between the groups (e.g. mean age, time from last
menstrual period, personal and family history of
breast/ovarian cancer, and percent of BRCA
mutation carriers).
Fifteen women were excluded from the symptoms analysis due to being postmenopausal at the
time of risk-reducing BSO. Table 2 presents the
summary of the overall incidence of climacteric
symptoms in the study group and in the controls.
The psychological symptom scores were significantly higher in the study group at all time
points as compared to the control group (at time
of interview: 9.0606 vs. 3.9167, respectively,
p 0.001) (Table 3 and Figure 1).
The somatic symptoms were significantly different at 6 months (after cessation of menses or

405

Prophylactic salpingo-oophorectomy and climacteric symptoms

Benshushan et al.

Table 1 Demographic and clinical characteristics of the study and control groups. Data are given as
mean + standard deviation or percentage

Age (years)
Number of children
Time since LMP (years)
History of regular periods
Family history of ovarian/breast cancer
Family history of colon/uterine cancer
Personal history of breast cancer
BRCA mutation carriers
Hysterectomy

Study

Control

p Value

50.83 + 7.52
2.96 + 1.5
5.63 + 5.53
83.30%
79.20%
27.10%
50.00%
52.10%
50.00%

58.06 + 5.43
2.8 + 1.07
7.879 + 5.78
95%
26.70%
13.30%
6.70%
0%
8.30%

50.001
0.540
0.053
0.059
50.001
0.073
50.001
50.001
50.001

LMP, last menstrual period; BSO, bilateral salpingo-oophorectomy

Table 2 Overall prevalence of menopausal symptoms
in the risk-reducing bilateral salpingo-oophorectomy
group and the controls. Data are given as % of the total
number of women in each group
Symptom

Study Control p Value

Heart beating
quickly/strongly
Feeling tense or nervous
Difficulty in sleeping
Excitable
Attacks of panic
Difficulty in
concentrating
Feeling tired/lack of energy
Loss of interest in
most things
Feeling unhappy
or depressed
Crying spells
Irritability
Feeling dizzy or faint
Pressure/tightness
in head/body
Parts of body feel
numb/tingle
Headaches
Muscle and joint pains
Loss of feeling in
hands or feet
Breathing difficulties
Hot flushes
Sweating at night
Loss of interest in sex
Vaginal dryness
Urinary incontinence

18.8

30.0

0.321

68.8
87.9
25.0
18.8
37.5

49.2
60.0
18.6
8.5
35.6

0.072
0.005
0.590
0.185
1.000

75.8
56.3

55.0
28.8

0.048
0.013

59.4

28.8

0.007

43.8
50.0
28.1
31.3

16.9
30.5
28.8
28.8

0.006
0.075
1.000
0.814

15.6

18.6

0.781

43.8
25.0
15.6

22.0
25.4
13.6

0.030
1.000
0.764

15.6
87.9
97.0
84.4
69.7
18.8

6.8
78.0
71.7
54.2
57.6
28.8

0.269
0.277
0.002
0.005
0.273
0.325

the risk-reducing BSO) (0.9483 for the study

group vs. 2.5455 for the control group, p 0.025)
and 1 year (1.1034 for the study group vs. 2.5938

406

for the control group, p 0.038) (Table 3 and

Figure 2).
The vasomotor symptom scores were significantly more severe in the risk-reducing BSO group
as compared to the controls (at time of interview:
3.94 vs. 2.05, respectively, p 5 0.001) (Table 3
and Figure 3).
We noticed a statistically significant difference
in sexual dysfunction at all time points in favor of
the control group (e.g. at time of interview: 1.85
vs. 0.90, respectively, p 5 0.01) (Table 3 and
Figure 4).
Data on the quality of life and satisfaction from
the risk-reducing BSO surgical procedure are
presented in Table 4. In 10.4% of the cases, there
were complications (mostly minor, e.g. local
infections, fever and minor bleeding). One case of
postoperative deep vein thrombosis was noted. The
overall satisfaction rate (on a 010 scale) was 8.23.
The perceived quality of life of the women
undergoing the operation decreased after the
surgical procedure (8.08 as compared to 8.52
preoperatively), but this difference did not reach
statistical significance (p 0.34).
As expected, the concern about ovarian cancer
decreased significantly after surgery (2.94 vs. 7.75
preoperatively, p 5 0.001) (Table 4).

DISCUSSION AND CONCLUSIONS

These results indicate that risk-reducing BSO as
compared to natural menopause is associated with
significantly higher prevalence and severity of
menopausal symptoms, which appear more
abruptly. Women who underwent the surgical
procedure and who were premenopausal at the
time of the operation were particularly vulnerable
to psychological distress; however, risk-reducing
BSO caused a significant decrease in anxiety and
fear of cancer risk.

Climacteric

Prophylactic salpingo-oophorectomy and climacteric symptoms

Benshushan et al.

Table 3 The scores in the Greene Climacteric Scale

over time in the two groups
Mean score
Time after
LMP/surgery

Control
group

Study
group

p Value

Psychological score
At 1 month
At 6 months
At 1 year
Time of interview

2.389
3.551
3.896
3.916

4.697
8.818
9.687
9.060

0.022
0.001
50.001
0.001

Somatic score
At 1 month
At 6 months
At 1 year
Time of interview

0.694
0.948
1.103
1.783

1.151
2.545
2.593
2.515

0.206
0.025
0.038
0.290

Vasomotor score
At 1 month
At 6 months
At 1 year
Time of interview

2.220
2.724
2.551
2.050

2.363
4.181
4.451
3.939

0.772
0.003
50.001
50.001

Sexual dysfunction score

At 1 month
0.186
At 6 months
0.241
At 1 year
0.568
Time of interview
0.900

0.727
1.515
1.806
1.848

50.01
50.01
50.01
50.01

8.940
17.061
18.539
17.364

0.034
50.001
50.001
50.001

Total score
At 1 month
At 6 months
At 1 year
Time of interview

5.491
7.465
8.120
8.650

Figure 2 The somatic scores in the Greene Climacteric

Scale of the two groups

LMP, last menstrual period

Figure 3 The vasomotor symptom scores in the Greene

Climacteric Scale of the two groups

Figure 1 The psychological scores in the Greene

Climacteric Scale for the two groups

Figure 4 The sexual dysfunction scores in the Greene

Climacteric Scale of the two groups

Some of our results are consistent with previous

reports. Madalinska and colleagues8 reported
that women who underwent risk-reducing BSO
had worse somatic symptoms (p 5 0.001) and

increased sexual dysfunction (p 5 0.05) than

matched controls. Similar to our findings, riskreducing BSO was associated with fewer breast
and ovarian cancer worries (p 5 0.001) and more

Climacteric

407

Prophylactic salpingo-oophorectomy and climacteric symptoms

Table 4 Pre- and postoperative attitudes and perceptions of 48 women who had risk-reducing bilateral
salpingo-oophorectomy (on a 010 scale). Data are
given as mean + standard deviation
Satisfaction
Regret
Pre-operative quality of life
Postoperative quality of life
Pre-operative ovarian cancer worry
Postoperative ovarian cancer worry

8.23 + 2.21
0.77 + 2.25
8.52 + 2.59
8.08 + 2.88*
7.75 + 3.31
2.94 + 3.08**

*, No significant difference from pre-operation,

p 0.34; **, significantly different from pre-operation,
p 5 0.001

favorable cancer risk perception (p 5 0.05).

Eighty-six percent of the women in that study
would choose risk-reducing BSO again, and 63%
would recommend it to a friend with familial risk
of ovarian cancer. Fry and colleagues9 also found
that preventive BSO was associated with poorer
emotional and social functioning as compared to a
group of women who chose to have routine
screening follow-up and to avoid BSO. There
was also a trend towards more significant somatic
menopausal symptoms. Our study adds important
information to these findings by indicating that the
increased climacteric symptoms in women who
undergo risk-reducing BSO do not seem to
interfere with their overall perceived quality of life.
Meiser and colleagues10 found that, when performed postmenopausally, preventive BSO had no
negative impact on the womens libido and sexual
function. The participants reported that the procedure had decreased concern about cancer risk.
Consistent with our findings, Elit and colleagues11 and Robson and colleagues12 also reported
that the perceived risk for developing ovarian
cancer decreased significantly after surgery. However, Robson and colleagues12 reported that a
significant proportion of women who had riskreducing BSO (20.7%) continued to report
ovarian cancer-specific worries despite surgery.
As indicated, our patients were not using HT.
One report evaluated the effects of HT on similar
group of women. Madalinska and colleagues13
evaluated through a questionnaire, the endocrine

Benshushan et al.
symptoms and sexual functioning of 450 high-risk
women who had participated in a nationwide,
cross-sectional, observational study. They report
that 36% of the women had undergone riskreducing BSO and 64% had opted for conservative
follow-up. In the risk-reducing BSO group, 47% of
the women were current HT users. They found
significantly fewer vasomotor symptoms than in
non-users (p 5 0.05). However, compared with
premenopausal women who preferred follow-up,
oophorectomized HT users were more likely to
report vasomotor symptoms (p 5 0.01). HT users
and non-users reported comparable levels of sexual
functioning. They concluded that, although HT has
a positive impact on surgically induced vasomotor
symptoms, it may be less effective than is often
assumed. Symptom levels remain well above those
of premenopausal women undergoing screening,
and sexual discomfort is not alleviated by HT.
We are aware that our study has certain
limitations which necessitate further investigation
of the subject. The main limitations of study are
its retrospective analysis and the fact that the data
on climacteric symptoms were self-reported and
thus affected by recall bias. This may cause underor over-estimation of prevalence and severity of
the symptoms. However, we believe that this bias
may only marginally affect our results since
women usually remember vividly their climacteric
symptoms. This assumption was recently validated by the demonstration of strong correlations
between most estrogen exposure indices and selfreports14.
In conclusion, risk-reducing BSO as compared
to natural menopause is associated with more
severe somatic as well as psychological climacteric
symptoms. However, the surgical procedure does
not seem to interfere with the overall perceived
quality of life and improves the perception of
cancer risk which most women find worth the
burden of the symptoms.
Conflict of interest

Nil.

Source of funding
Supported in part by a
private donation from Mrs Rosalind Bassin of
Long Beach, CA, USA.

References
1. McKinlay SM, Brambilla DJ, Posner J. The
normal menopause transition. Maturitas 1992;
14:10315

408

2. Bachmann GA. Vasomotor flushes in menopausal women. Am J Obstet Gynecol 1999;180:

S31216

Climacteric

Prophylactic salpingo-oophorectomy and climacteric symptoms

3. Freeman EW, Sammel MD, Lin H, et al.
Symptoms associated with menopausal transition and reproductive hormones in midlife
women. Obstet Gynecol 2007;110:23040
4. Woods NF. Symptoms during the perimenopause: prevalence, severity, trajectory, and significance in womens lives. Am J Med 2005;
118:S1424
5. Kronenberg F. Hot flashes: epidemiology and
physiology. Ann NY Acad Sci 1990;592:5286
6. Greene JG. A factor analytic study of climacteric
symptoms. J Psychosom Res 1976;20:42530
7. Greene JG. Constructing a standard climacteric
scale. Maturitas 1998;29:2531
8. Madalinska JB, Hollenstein J, Bleiker E, et al.
Quality-of-life effects of prophylactic salpingooophorectomy versus gynecologic screening
among women at increased risk of hereditary
ovarian cancer. J Clin Oncol 2005;23:68908
9. Fry A, Busby-Earle C, Rush R, Cull A. Prophylactic oophorectomy versus screening: psychosocial
outcomes in women at increased risk of ovarian
cancer. Psycho-Oncology 2001;10:23141

Climacteric

Benshushan et al.
10. Meiser B, Tiller K, Butow P, et al. Psychological
impact of prophylactic oophorectomy in
women at increased risk for ovarian cancer: a
prospective study. Psycho-Oncology 2000;9:
496503
11. Elit L, Epslen MJ, Butler K, Narod S. Quality of
life and psychosexual adjustment after prophylactic oophorectomy for a family history of
ovarian cancer. Familial Cancer 2001;1:14956
12. Robson M, Hensley M, Barakat R, et al. Quality
of life in women at risk for ovarian cancer who
have undergone risk-reducing oophorectomy.
Gynecol Oncol 2003;89:2817
13. Madalinska JB, van Beurden M, Bleiker EM,
et al. The impact of hormone replacement
therapy on menopausal symptoms in younger
high-risk women after prophylactic salpingooophorectomy. J Clin Oncol 2006;24:3576
82
14. Lord C, Duchesne A, Pruessner JC, Lupien SJ.
Measuring indices of lifelong estrogen exposure:
self-report reliability. Climacteric 2009;12:387
94

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