Trends in Bilateral Oophorectomy at the Time of Hysterectomy for Benign

Disease in a Tertiary Hospital in Manila

Jahnen Calugan-Tanamal, MD; Sharon Arevalo-Capule, MD

INTRODUCTION

Ovarian cancer is the most common cause of cancer death attributable to gynecologic

malignancies, with estimated 21,880 new cases and 13,850 deaths in the United States in 2009. 1

For the general population of women, the lifetime risk of developing ovarian cancer is around

1.4%; the lifetime risk of dying from ovarian cancer is approximately 1.0%.2

Prophylactic oophorectomy frequently done with hysterectomy was associated with a

greater than 90% reduction in the risk of ovarian cancer, (relative risk [RR] = 0.04; 95%

confidence interval [CI], 0.01–0.16) with an average follow-up of 9 years.3 However, recent

studies have shown that prophylactic oophorectomy without an urgent medical indication

decreases a woman's long-term survival rates substantially and has other serious adverse effects.4

A recent study showed a decreased incidence of ovarian cancer with performance of bilateral

salpingooophorectomy in women undergoing benign hysterectomy without a family history of

ovarian cancer from 0.33% to 0.02%.5

Hysterectomy is a common surgery among women in the United States second only to

women in childbirth by cesarean section delivery, with approximately 600,000 performed

annually. Majority was performed for benign cases with an option of retaining the ovaries but

newer percentage of concomitant oophorectomy increased from 25%-73%, between 1965 and

2004. In the United States, 1 in 3 women can be expected to have a hysterectomy by age 60.6

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 Studies show evidences suggesting premature loss of ovarian function due to

bilateral oophorectomy performed before natural menopause and or before 40 years old, is

associated with several negative outcomes. Factors showed increased risk of cardiovascular

disease, premature death, cognitive impairment or dementia, Parkinsonism, osteoporosis and

bone fractures, decline in psychological well-being, and decline in sexual function. With

estrogen treatment, there is no total prevention of the negative effects, 7-9 while other studies are

implying that there are no correlation of menopausal status and these outcomes. 6, 10 Thus despite

the probable benefits in reducing ovarian cancer, routine prophylactic oophorectomy at the time

of hysterectomy in premenopausal women has continued to be controversial.

Decision making in doing prophylactic oophorectomy at the time of hysterectomy is now

complicated that it requires the patient and physician to consider numerous aspects. The

American College of Obstetricians and Gynecologists in 1999, stated that “prophylactic

oophorectomy should be based not only on the patient’s age but also on other factors that weigh

individual risk for developing ovarian cancer against the loss of ovarian function”.11 In 2008,

they changed their recommendation to “strong recommendation should be given to retaining

normal ovaries in premenopausal women who are not at increased genetic risk of ovarian

cancer.”12

SIGNIFICANCE OF THE STUDY

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 This research work was undertaken to enhance knowledge on trending developments in

bilateral oophorectomy at the time of hysterectomy for benign diseases and its significance for

upcoming practitioners’ practice in making proper decision and management.

OBJECTIVES

General Objectives

To distinguish patient characteristics associated with bilateral oophorectomy or removal

of remaining ovary at the time of benign hysterectomy, and to establish trends in the

performance of oophorectomy from 2009-2013.

Specific Objectives

The purpose of the study is to assess the trends in oophorectomy at the time of benign

hysterectomy in Adventist Medical Center Manila for the years 2009 to 2013.

Specifically it wants to find out the answers to the following questions:

1. What is the trend in deciding for oophorectomy in Adventist Medical Center Manila?

2. Is age a factor in deciding for oophorectomy?

3. Is financial insurance a factor in deciding for oophorectomy?

4. Is pre-operation diagnosis a factor in deciding for oophorectomy?

5. Is the type of hysterectomy a factor in performing oophorectomy?

Hypotheses:

This study is being conducted with the following hypotheses:

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 1. There is a decreasing trend of oophorectomy during hysterectomy for benign

gynecologic disease in Adventist Medical Center Manila.

2. The patient’s age and financial insurance status are significant factors in deciding for

oophorectomy.

3. The pre-operational diagnosis and type of hysterectomy are significant factors in

deciding for oophorectomy.

MATERIAL AND METHODS

Study Design

This research is a cross sectional analysis using the recorded data of patients admitted at

Adventist Medical Center Manila who had undergone bilateral oophorectomy at the time of

benign hysterectomy during the year 2009 to 2013.

Inclusion criteria

The study includes women aged 18 years or older undergoing hysterectomies for benign

gynecologic conditions during the year 2009 to 2013.

Exclusion Criteria

Hysterectomies performed for gynecologic malignancies (ICD-9-CM diagnosis codes

179-184.9) and obstetric indications (ICD-9-CM diagnosis codes 640-679) were excluded.

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Methodology

A research protocol was submitted to the research and ethics committee of the institution

and was given exempt status. Comprehensive data gathered in the medical records of the

institution was accessed from the year 2009-2013 for collection of patients and treatment

information for every outpatient or emergency admission and hospital discharge.

Demographic data was created for every entry including age, type of insurance (Private,

Philhealth, self-pay/no insurance, charity), reason for admission by diagnosis-related group

codes, primary and secondary diagnoses. Subjects taken were de-identified, omitting the patient

names and medical number.

Clinical predictors of hysterectomy, including vaginal bleeding, endometriosis, ovarian

cyst, leiomyomas and pelvic organ prolapse were identified using their respective International

Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes.

Cases were identified in the years 2009-2013, using the ICD-9-CM procedure codes 68.3

68.5 (hysterectomy). Each admission that resulted in hysterectomy was included in the study and

was further analyzed for presence of bilateral oophorectomy, including removal of the remaining

ovary, utilizing ICD-9-CM procedure codes 65.3 – 65.6. Hysterectomies performed for

gynecologic malignancies (ICD-9-CM diagnosis codes 179-184.9) and obstetric indications

(ICD-9-CM diagnosis codes 640-679) were excluded.

The statistical data were summarised in a table for cross sectional analysis. The Pearson’s

X2 was used to test the independence of the variables namely insurance type, age range,

diagnosis and hysterectomy type. Cuzick nonparametric test for trend was used to calculate the P
for trend across ordered groups.

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RESULTS

A total of 319 hysterectomies were performed for benign gynecological conditions from

the year 2009-2013. Of these, 206 (64.58%) had concomitant bilateral oophorectomy and 27

(8.46%) had unilateral oophorectomy. Table 1 shows the demographic information of patients in

the study. The average age of women undergoing hysterectomy was 46.9. The youngest patient

was age 29 (n=1), G3P3, who underwent abdominal hysterectomy with bilateral oophorectomy

for abnormal uterine bleeding secondary to endometrial and endocervical polyp with multiple

leiomyoma. The oldest patient, on the other hand was age 77 who underwent abdominal

hysterectomy with bilateral oophorectomy for postmenopausal bleeding secondary to

endometrial hyperplasia and leiomyoma. Majority of women undergoing either hysterectomy

alone, with concomitant bilateral or unilateral oophorectomy, had Philhealth insurance (60.46%,

66.02% and 70.37% respectively), had a primary pre-operative diagnosis of leiomyoma (70.37%,

62.62% and 81.48%), and underwent abdominal hysterectomy (93.4%).

No Oophorectomy Bilateral Oophorectomy U

TABLE 1: Baseline Characteristics by (TAH / TVH) (TAHBSO / TVHBSO / LAP+BSO) (
Oophorectomy Status n = 86 n = 206 n
(26.96%) (64.58%)

Age (years)

<40 27/86 (31.4%) 14/206 (6.8%)

40-49 55/86 (63.95%) 105/206 (50.97%)

50-54 2/86 (2.32%) 47/206 (22.82%)

55-64 0 26/206 (12.62%)

65 or older 2/86 (2.32%) 14/206 (6.8%)

Financial Insurance*

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 Self-pay/No insurance 19/86 (22.09%) 44/206 (21.36%)

Philhealth 52/86 (60.46%) 136/206 (66.02%)

Private 22/86 (25.58%) 68/206 (33.01%)

Charity 7/86 (8.14%) 12/206 (5.82%)

Pre-operational diagnosis**
Leiomyomas (primary diagnosis) 63/86 (73.26%) 129/206 (62.62%)

Leiomyomas (secondary diagnosis) 4/86 (4.65%) 9/206 (4.37%)

Endometriosis (primary diagnosis) 0 7/206 (3.4%)

Endometriosis (secondary diagnosis) 1/86 (1.16%) 3/206 (1.46%)

Prolapse 8/86 (9.3%) 11/206 (5.34%)

Abnormal Uterine Bleeding 34/86 (39.53%) 82/206 (39.81%)

Endometrial hyperplasia (primary diagnosis) 9/86 (10.46%) 16/206 (7.77%)

Endometrial hyperplasia (secondary diagnosis) 2/86 (2.32%) 2/206 (0.97%)

Adenomyosis (primary diagnosis) 0 2/206 (0.97%)

Adenomyosis (secondary diagnosis) 2/86 (2.32%) 4/206 (1.94%)

Endometrial polyp (primary diagnosis) 2/86 (2.32%) 8/206 (3.88%)

Endometrial polyp (secondary diagnosis) 3/86 (3.49%) 14/206 (6.8%)

Ovarian Cyst (primary diagnosis) 0 21/206 (10.19%)

Ovarian Cyst (secondary diagnosis) 1/86 (1.16%) 42/206 (20.39%)

Hysterectomy type Hysterectomy Hysterectomy + BSO

Abdominal 78/86 (90.7%) 193/206 (93.69%)

Vaginal 8/86 (9.3%) 11/206 (5.34%)

Laparoscopic 0 2/206 (0.97%)

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 Figure 1 demonstrates the rate of oophorectomy at the time of benign hysterectomy from

2009 to 2013. Based on Cuzick nonparametric test for trend, the pattern is more of a quadratic

nature rather than a linear pattern (Figure 2) and that the change is not significant (P value =

0.6117).

Figure 1. Rate of Oophorectomy at the Time of Benign Hysterectomy

by Year and
Hysterectomy Type
* Percentages add up to more than 100% because some patients had more than one insurance. **
80
Percentages add up to more than 100% because some patients had more
TAH than one pre-operational
TAHBSO
diagnosis. TAHUSO TVHBSO
TVH LAPHSY+BSO
60
Rates (%)

40

20

0
2009 2010 2011 2012 2013

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 Figure 2. Cuzick’s trend test as ploted

Table 2 shows the crosstabulation of oophorectomy status by cluster and year. Using

the Bonferroni method the proportions per year for each cluster do not differ significantly

at 0.05 level.

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10
 Figure 2 shows the odds ratio of patients undergoing bilateral oophorectomy at the time

of benign hysterectomy stratified by age younger than 50 and 50 years old and above.

Figure2. Odds ratio of undergoing bilateral oophorectomy at the time of benign

hysterectomy stratified by age younger than 50 and 50 years old and above.

38

30

23
less than 50
Number of cases

50 yo and older
15

0
2009 2010 2011 2012 2013

Table 3. Pearson’s Chi-Square Test of Oophorectomy Status Stratified by Age

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 A Pearson chi-square test was applied to test whether age is a factor in deciding for

oophorectomy and found to be statistically significant, X2 (8, N = 319) = 65.00, p < 0.00, using

an alpha level of 0.05. As indexed by Cramer’s statistic, the strength of the association was 0.32.

This reflects primarily the fact that patients below 50 years of age are more likely have

undergone TAH/TVH or TAHUSO and less likely to undergo TAHBSO/TVHBSO/LAP+BSO

than expected. Patients with ages 50 and above more likely have undergone

TAHBSO/TVHBSO/LAP+BSO and less likely to undergo TAH/TVH or TAHUSO than

expected. Thus, the alternative hypothesis on age as a factor is accepted with a P value of <0.00.

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Table 3. Pearson’s Chi-Square Test of Oophorectomy Status Stratified by Financial

Insurance Status

A Pearson chi-square test was applied to test whether financial insurance status is a factor

in deciding for oophorectomy and found to be not statistically significant, X2 (6, N = 396) =

2.86, p < 0.83, using an alpha level of 0.05. As indexed by Cramer’s statistic, the strength of the

association was only 0.06. Thus, the alternative hypothesis on financial insurance status as a

factor is rejected with a P value of < 0.83.

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Table 4. Pearson’s Chi-Square Test of Oophorectomy Status Stratified by Pre-operational
Status

14
 A Pearson chi-square test was applied to test whether pre-operation diagnosis is a factor

in deciding for oophorectomy and found to be statistically significant, X2 (26, N = 538) = 65.38,

15
p < 0.00, using an alpha level of 0.05. As indexed by Cramer’s statistic, the strength of the

association was 0.25. This reflects primarily the fact that patients with pre-operation diagnosis of

Leiomyomas (primary diagnosis), Prolapse, and Endometrial hyperplasia (primary diagnosis) are

more likely to have undergone TAH/TVH as expected. Patients with pre-operation diagnosis of

Endometriosis (primary diagnosis) and Ovarian Cyst (primary diagnosis) are more likely to have

undergone TAHBSO/TVHBSO/LAP+BSO as expected and patients with pre-operation

diagnosis of Endometriosis (secondary diagnosis), Adenomyosis (primary diagnosis),

Endometrial polyp (primary diagnosis), and Ovarian Cyst (secondary diagnosis) are more likely

to have undergone TAHUSO as expected. Thus, the alternative hypothesis on pre-operational

diagnosis as a factor is accepted with a P value of < 0.00.

Table 5. Pearson’s Chi-Square Test of Oophorectomy Status Stratified by Type of

Hysterectomy

A Pearson chi-square test was applied to test whether the type of hysterectomy is a factor

in deciding for oophorectomy and found to be not statistically significant, X2 (4, N = 319) =

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4.65, p < 0.33, using an alpha level of 0.05. As indexed by Cramer’s statistic, the strength of the

association was only 0.09. Thus, the alternative hypothesis on the type of hysterectomy as a

factor is rejected with a P value of < 0.33.

DISCUSSION:

Oophorectomy has long been shown to be the most effective method for lowering risk for

ovarian cancer in high-risk women. However if performed before menopause it leads to early

menopause, but in post-menopausal women, oophorectomy is less likely to trigger new

menopausal symptoms. 14

Our study revealed a quadratic rather than a linear pattern of change (Figure 2) and that

the change is not significant (P value = 0.6117) compared to earlier studies in other countries

which showed a linear decline 2, 15 In contrast to the study done by Novetsky et al2 who reported

10.4% decrease in 2001 to 2006 and that of Whiteman et al17 with 5.5% decrease in 2000 to

2004, and to that of Lowder et al16 done in 1979 to 2004 in the United States wherein there in an

increased proportion of oophorectomies performed at the time of benign hysterectomy, our study

showed a quadratic pattern in the rate of oophorectomy in women younger than age 50. The

proportions per year for each cluster however, do not differ significantly at 0.05 level.

A little over half of the women who underwent vaginal hysterectomy (57.9%) had

bilateral oophorectomy. This is supported by the data that oophorectomy can be safely performed

in more that 85% of vaginal hysterectomies in the studies by Davies et al18, Sheth SS19, and Sizzi

et al20. Novetsky et al’s2 study showed otherwise wherein there was significantly less (17%)

oophorectomy done among vaginal hysterectomies. All the laparoscopic cases (n=2) had

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oophorectomy which was again contrary to that of Novetsky et al’s2 study which showed only

50.4% with a relative reduction rate of 16%.

In contrast to the previous study by Jacoby et al21 wherein oophorectomy was more

common in white women and those who were not insured, our study showed a similar findings

with that of the study done by Novetsky et al’s2 wherein more oophorectomies were done among

women with Philhealth and private insurance (63.5%).

Over the course of the study, women in both clusters (younger than age 50 and 50 years

old and above) had no significant increase or decrease in oophorectomy rates. This may be

attributed to the compliance of the health practitioners to the recommended guidelines by the

different societies under the Philippine Obstetrical and Gynecological Society (POGS). This

result is contrary to the study of Novetsky et al2 wherein there was a significant decline in

oophorectomy rates between the years 2002 and 2003 and between 2005 and 2006 (decrease of

2.5% and 3.4% respectively). This was attributed to the release of the result of the Women’s

Health Initiative randomized controlled trial in July 2002 concluding that the overall health risk

of combined estrogen and progestin hormone therapy (HT) exceeded the benefits.22 Since that

time, recommendations for the use of HT have changed,23 resulting in a decrease in its use,24,25

with a 40% decrease in HT prescriptions by July 2003. The decrease in bilateral salpingo-

oophorectomy observed may be result of practitioners’ unwillingness to prescribe HT, leading to

an increase in ovarian retention.2

The largest increase in the overall bilateral oophorectomy rate occurred in 2013 with

4.37% increase compared to the year 2012 and the previous years. This may be due to the

increase in the hysterectomy cases done in the said year.

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 Our study has several limitations like the financial status in general, educational status,

personal and/or family history of breast, gynecologic or colon cancer were not considered as

predictive factors. Our study is based only on our institution and may not be generalisable to

other populations.

In summary, this study has shown no significant increase or decrease in all oophorectomy

rates across all age groups at the time of benign hysterectomy. The patient’s age and pre-

operational diagnosis are significant factors in deciding for oophorectomy while financial

insurance and type of hysterectomy does not.

CONCLUSION:

The trend of performing oophorectomy during benign gynecologic conditions did

not significantly change over the five-year study period. It is concluded that patient’s age and

pre-operational diagnoses were considered to be factors in performing oophorectomy at the time

of hysterectomy for benign gynecologic conditions but not the type of hysterectomy and the

patient’s financial insurance status.

RECOMMENDATION:

A follow-up study is recommended with the consideration of financial and educational

status, family and/or personal history of breast, gynecologic or colon cancer as predictive factors

in deciding for oophorectomy.

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