https://doi.org/10.6118/jmm.

20010
J Menopausal Med 2020;26:159-164
pISSN: 2288-6478, eISSN: 2288-6761
ORIGINAL ARTICLE

Effect of Hysterectomy on Ovarian Reserve in the Early

Postoperative Period Based on the Type of Surgery
Sungwook Chun, Yong Il Ji
Department of Obstetrics and Gynecology, Inje University Haeundae Paik Hospital, Inje University College of Medicine, Busan, Korea

Objectives: This study aimed to evaluate the influence of simple hysterectomy on the ovarian reserve based on the type of surgery.
Methods: Eighty-six premenopausal women between 31 and 48 years who underwent hysterectomy for benign gynecologic disease
without additional adnexal surgery at a university hospital participated in this study. Seventy-one patients underwent laparoscopy-
assisted vaginal hysterectomy (LAVH), and 15 patients underwent abdominal hysterectomy (AH). Blood samples were obtained from all
study participants on preoperative day and 3 days after the operation to determine the anti-Müllerian hormone (AMH) levels.
Results: The postoperative reduction of the mean serum AMH level in the LAVH group (0.42 ± 0.76 ng/mL) was greater than that in
the AH group, although the difference was not statistically significant (0.01 ± 0.60 ng/mL) (P = 0.053). The mean baseline AMH level
(2.59 ± 2.33 ng/mL) was significantly reduced to 2.24 ± 2.08 ng/mL at 3 days after hysterectomy, and the mean rate of decline of AMH
levels after surgery was 13.61% ± 30.81%. In subgroup analysis based on the type of surgery, the mean serum AMH level decreased
significantly after surgery in the LAVH group, but no significant changes were found in serum AMH levels before and after the surgery in
the AH group.
Conclusions: These preliminary results suggest that simple hysterectomy affects the early postoperative decline of ovarian reserve,
and these results might vary depending on the type of surgery.

Key Words: Anti-Müllerian hormone, Hysterectomy, Ovarian reserve

INTRODUCTION conditions [3].

Hysterectomy is known as one of the most common
Ovarian reserve refers to the size of the non-growing surgical procedures performed [7]. Some authors have
or resting primordial follicle population in the ovaries reported that hysterectomy, even if the ovaries are
[1,2], and it represents the potential ovarian function preserved, might antedate ovarian failure [8-10], but
at a given time point [3]. Among a variety of methods whether ovary-sparing hysterectomy influences ovarian
used to assess ovarian reserve (including serum follicle- reserve postoperatively remains unclear [3,11-15]. In
stimulating hormone [FSH] and inhibin B level as- addition, studies regarding the difference of the influ-
sessments [1,3]), anti-Müllerian hormone (AMH) is ence of hysterectomy on ovarian function based on the
known to be the most improved and informative mark- type of surgery are still lacking.
er among these ovarian reserve tests [3-6]. Particularly, This study aimed to assess the effect of simple hyster-
serum AMH measurement is helpful for counseling ectomy with ovarian conservation on the serum AMH
patients regarding ovarian reserve change after gyne- level based on the type of surgery.
cologic surgical interventions for benign gynecologic

Received: April 10, 2020 Revised: August 6, 2020 Accepted: August 14, 2020
Address for Correspondence: Yong Il Ji, Department of Obstetrics and Gynecology, Inje University Haeundae Paik Hospital, 875 Haeun-daero,
Haeundae-gu, Busan 48108, Korea
Tel: 82-51-797-2020, E-mail: [email protected], ORCID: https://orcid.org/0000-0002-1030-6105

Copyright © by The Korean Society of Meno­pause

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/).

159
Sungwook Chun and Yong Il Ji

MATERIALS AND METHODS rior and posterior mucosae are closed by interlocking
suture.
Participants
This study was approved by the Institutional Review AH
Board (IRB) of Inje University Haeundae Paik Hospital After skin incision and entrance into the peritoneal
(IRB No. 129792-2014-091), and the written informed cavity, both the round ligaments and infundibulopelvic
consent was waived by the IRB. Patients aged 31 to ligaments are clamped, incised, and ligated using Vicryl
48 years with regular menstrual cycles undergoing suture. The bladder flap is dissected, and both uterine
hysterectomy for benign gynecologic disease without arteries are clamped twice, incised, and double suture-
additional adnexal surgery between January 2011 and ligated on the isthmic portion. After anterior entrance
December 2013 at Inje University Haeundae Paik Hos- into the vagina, the uterus is excised by completely
pital participated in this study. Those who underwent circumscribing the cervix. The vaginal vault is closed
radical or laparoscopic radical hysterectomy for ma- with locking suture with Vicryl. After controlling pelvic
lignancy were excluded. Additional exclusion criteria floor bleeding, pelvic peritonization is performed, and
were as follows: history of previous uterine or adnexal the abdominal wall is closed layer by layer.
surgery for gynecologic pathology (except cesarean sec-
tion); suspicion of ovarian malignancy based on clinical Measurement of serum AMH levels
or ultrasonographic evidence; any hormone treatment Serum samples were collected on preoperative day
during the previous 6 months; or menopause symp- and 3 days after scheduled hysterectomy from all sub-
toms or oligo-amenorrhea. The present study included jects in obedience to the Declaration of Helsinki guide-
86 patients; 71 and 15 patients underwent laparoscopy- lines. The serum AMH levels were determined using
assisted vaginal hysterectomy (LAVH) and abdominal the AMH Gen II assay (Beckman Coulter, Brea, CA,
hysterectomy (AH), respectively. USA). The intra- and inter-assay coefficients of varia-
tion were both < 5.0% with the lowest detection limit of
Operative techniques 0.08 ng/mL.
All types of hysterectomy, including LAVH and AH, The formula for the rate of decline of AMH levels is as
were performed by the same gynecologist who has follows:
been engaged in laparoscopic surgery with more than [(preoperative AMH – postoperative day 3 AMH) /
10 years of experience. No additional procedures on the (preoperative AMH)] × 100.
adnexa, including oophorectomy, ovarian cystectomy,
or salpingectomy, were performed in any of the partici- Statistical analyses
pants in this study. Statistical analyses were performed using IBM SPSS
Statistics (ver. 25.0; IBM, Armonk, NY, USA). All data
LAVH were presented as mean ± standard deviation. Dif-
After three-trocar insertion with carbon dioxide (CO2) ferences of clinical variables between LAVH and AH
gas insufflation and entrance to the peritoneal cavity, group were assessed using unpaired t tests for continu-
the round ligaments and peritoneum of both sides are ous variables and chi-square statistics for categorized
dissected and coagulated using monopolar forceps. data, and pre- and postoperative serum AMH levels
Subsequently, the ovarian ligaments and salpinges were were compared using paired samples t tests. A one-
cut bilaterally with the LigaSure device (Medtronic, sample t test was used to determine the statistical sig-
Minneapolis, MN, USA). A circular incision is made nificance of the rate of decline of AMH levels. For all
around the region approximately 2 cm from the exter- analyses, P < 0.05 was considered significant.
nal cervical os, and the vaginal wall is dissected. After
entry of the anterior peritoneal reflection, the posterior RESULTS
peritoneal sac is opened between the uterosacral liga-
ments. The uterosacral and cardinal ligaments are in- Table 1 showed the baseline clinical characteristics
dividually clamped, divided, sutured, and ligated using of the study participants. No significant differences
Vicryl suture (Ethicon, Somerville, NJ, USA). After the were observed in the clinical variables between the two
uterus is removed through the vaginal canal, the ante- groups.

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 Ovarian Reserve Change after Hysterectomy according to Type of Surgery

Table 1. Comparison of baseline clinical characteristics between the two study groups according to the type of surgery
Variable LAVH group (n = 71) AH group (n = 15) P value
Age (y) 43.67 ± 3.32 43.73 ± 2.58 0.950a
Height (cm) 158.46 ± 5.46 157.57 ± 4.79 0.559a
Weight (kg) 59.29 ± 8.32 61.75 ± 8.47 0.317a
2
Body mass index (kg/m ) 23.57 ± 2.82 24.83 ± 2.94 0.121a
Surgical indications 0.360b
Bleeding (including HMB) 31 (43.7) 7 (46.7)
Pain (including dysmenorrhea) 20 (28.2) 3 (20.0)
Mass itself (or pressure symptoms) 11 (15.5) 5 (33.3)
CIN 3 7 (9.9) 0
Others 2 (2.8) 0
Preoperative serum AMH levels (ng/mL) 2.69 ± 2.46 2.12 ± 1.56 0.397a
Data are presented as mean ± standard deviation or number (%).
LAVH: laparoscopy-assisted vaginal hysterectomy, AH: abdominal hysterectomy, HMB: heavy menstrual bleeding, CIN: cervical intraepithelial
neoplasia, AMH: anti-Müllerian hormone.
P values by aunpaired t test or bchi-square test.

Table 2. Comparison of surgical outcomes between the two study groups according to the type of surgery
Variable LAVH group (n = 71) AH group (n = 15) P value
Uterine weight (g) 305.41 ± 142.34 751. 43 ± 736.09 < 0.001a,*
Surgery time (min) 88.38 ± 22.94 95.33 ± 17.38 0.272a
∆ Hemoglobin (g/dL) 1.29 ± 0.80 1.15 ± 0.71 0.529a
Postoperative histology 0.205b
Myoma or adenomyosis 64 (90.1) 15 (100)
c
CIN 3 7 (9.9) 0
∆ AMH (ng/mL) 0.42 ± 0.76 0.01 ± 0.60 0.053a
Rate of decline of AMH levels (%) 14.62 ± 32.74 8.81 ± 19.35 0.510a
Data are presented as mean ± standard deviation or number (%). ∆ means the postoperative blood level changes compared to the preoperative ones.
LAVH: laparoscopy-assisted vaginal hysterectomy, AH: abdominal hysterectomy, CIN: cervical intraepithelial neoplasia, AMH: anti-Müllerian hormone.
P values by aunpaired t test or bchi-square test. cCoexistence of myoma or adenomyosis in 3/7 resected specimens. *P < 0.05.

In Table 2, the size of uterus of the patients who un- declined compared with baseline AMH levels (P <
derwent AH is larger compared with those who under- 0.001). The rate of decline of AMH levels after hyster-
went LAVH (751.43 ± 736.09 g vs. 305.41 ± 142.34 g, ectomy was 13.61% ± 30.81% (P < 0.001). In subgroup
respectively), but there were no significant differences analysis based on the type of surgery (Table 3, Fig. 1),
in terms of surgery time or postoperative change in day 3 postoperative serum AMH levels in the LAVH
hemoglobin level between the two groups. Mean post- group (2.26 ± 2.20 ng/mL) were significantly different
operative reductions of serum AMH levels in LAVH from preoperative levels (2.69 ± 2.46 ng/mL), and the
group (0.42 ± 0.76 ng/mL) were greater than those in rate of decline of AMH levels after hysterectomy was
AH group (0.01 ± 0.60 ng/mL), but this difference did 14.62% ± 32.74% (P < 0.001). However, serum AMH
not reach statistical significance (P = 0.053). level before surgery was not significantly different from
In Table 3, the baseline serum AMH level of all study the AMH levels at 3 days after operation in the AH
participants was 2.59 ± 2.33 ng/mL. Postoperative day group (2.12 ± 1.56 ng/mL and 2.11 ± 2.07 ng/mL, re-
3 serum AMH levels (2.24 ± 2.08 ng/mL) significantly spectively).

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Sungwook Chun and Yong Il Ji

Table 3. Changes of serum anti-Müllerian hormone (AMH) levels after 3.5

hysterectomy based on the type of surgery *
3.0
Variable Value P value *
All participants receiving hysterectomy (n = 86) 2.5

AMH (ng/mL)
Preoperative AMH (ng/mL) 2.59 ± 2.33
2.0
Postoperative AMH (ng/mL) 2.24 ± 2.08 < 0.001a,*
Rate of decline of AMH levels (%) 13.61 ± 30.81 < 0.001b,* 1.5
Participants receiving LAVH (n = 71)
1.0
Preoperative AMH (ng/mL) 2.69 ± 2.46
Postoperative AMH (ng/mL) 2.26 ± 2.20 < 0.001a,* 0.5
b, LAVH (pre) LAVH (post) AH (pre) AH (post)
Rate of decline of AMH levels (%) 14.62 ± 32.74 < 0.001 *
Participants receiving AH (n = 15) Fig. 1. Serum anti-Müllerian hormone (AMH) levels between the two
groups before and after hysterectomy. LAVH: laparoscopy-assisted
Preoperative AMH (ng/mL) 2.12 ± 1.56
vaginal hysterectomy, AH: abdominal hysterectomy, pre: preoperative,
Postoperative AMH (ng/mL) 2.11 ± 2.07 0.956a post: postoperative. *P < 0.05.
Rate of decline of AMH levels (%) 8.81 ± 19.35 0.099b
Data are presented as mean ± standard deviation. with ovarian conservation could accelerate ovarian fail-
LAVH: laparoscopy-assisted vaginal hysterectomy, AH: abdominal hysterec- ure [8-10]. Ahn et al. [10] reported that the mean age of
tomy. women who underwent hysterectomy (46.3 ± 3.0 years)
P values by apaired t test (compared to preoperative AMH levels) or bone-
sample t test. *P < 0.05. was significantly lower than that of those in the control
group (48.1 ± 3.2 years).
The reasons for the effect of a simple hysterectomy on
DISCUSSION the decrease of postoperative ovarian reserve even if
the both ovaries are preserved are unclear. One gener-
Hysterectomy is major surgical procedure which is the ally accepted hypothesis is that the decrease of ovarian
second most frequently conducted following cesarean reserve after hysterectomy may be attributed to the
section in the United States [1,2]. The first aim of the interruption of the ovarian branch of the uterine artery
present study was to evaluate whether ovarian reserve that leads to the disturbance of blood supply to the ova-
was immediately reduced after hysterectomy with bi- ries [3,11,12]. Atabekoğlu et al. [11] suggested that the
lateral ovarian preservation by assessing serum AMH decrease of ovarian reserve after hysterectomy may be
levels, and the result is that AMH levels significantly attributed to the acute hypoxia in the ovaries after the
decreased after postoperative day 3 when compared interruption of the uterine arteries during operation.
with preoperative ones in all the participants. The sec- However, this explanation is in contrast with the result
ond aim of this study was to assess whether the post- by Lee et al. [12] who revealed that hysterectomy did
operative change of ovarian reserve was different based not affect ovarian arterial blood flow indices (pulsatile
on the type of surgery, and we found that serum AMH and resistance indices) based on Doppler ultrasonog-
levels significantly decreased postoperatively compared raphy findings. In addition, this hypothesis hardly ex-
with baseline serum levels before surgery in the LAVH plains why the postoperative change of ovarian reserve
group, but not in the AH group. is different according to the type of hysterectomy in our
It is controversial whether hysterectomy with ovarian study.
preservation affects ovarian reserve [3]. The assessment The second hypothesis is that the electro-thermal en-
of the ovarian reserve using serial AMH level mea- ergy from the devices used during laparoscopic surgery,
surement is considered a useful tool for evaluating the such as bipolar forceps or LigaSure, can lead to delete-
ovarian function after hysterectomy [3,11], and several rious effects on the ovarian tissue and vessels, leading
studies have been conducted to ascertain whether the to additional loss of ovarian function. To the best of
postoperative AMH level decreases when compared our knowledge, only one study reported the compari-
with the preoperative level, but the results are conflict- son of changes of ovarian reserve after laparoscopic
ing [11-17]. Some authors reported that hysterectomy hysterectomy (LH) and non-laparoscopic hysterectomy

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 Ovarian Reserve Change after Hysterectomy according to Type of Surgery

(non-LH). Cho et al. [18] measured serum AMH levels erative decline of ovarian reserve after gynecologic sur-
preoperatively, and at 7 days, 2 months, and 6 months gery is difficult. There may be questions about whether
after LH (total LH or LAVH) and non-LH (vaginal hys- an AMH measurement 3-days postoperatively was too
terectomy or AH), and they found that the incidence early to assess the impact of surgery on the ovarian re-
of a significant decrease of serum AMH levels at post- serve. Most previous studies performed postoperative
operative 2 months was considerably higher in the LH serial AMH measurements at least 1 week after surgery
group compared with that in the non-LH group (43.9% [21]. Griesinger et al. [22], however, reported that the
vs. 20.0%). They suggested that electro-thermal devices length of time for serum AMH levels to decrease by
used for bleeding control during laparoscopic surgery the minimum detection limit after bilateral oophorec-
can lead to additional loss of ovarian function, and tomy is within 84 hours postoperatively. This finding
this result is comparable to ours. Two studies reported supports the suggestion of a previous study that 3 days
that the rate of decline of AMH levels in the bipolar after surgery could be an effective time point to assess
group was significantly higher than that in the suture early postoperative reduction of the ovarian reserve.
group after laparoscopic cystectomy for endometrioma Besides relatively small sample size with uneven
[19,20], which supports this hypothesis. In the present sample size between two groups and short-term study
study, postoperative decline of serum AMH level in design, this study had some serious limitations as fol-
LAVH group was greater than that in AH group which lows: First, the mean age of the patients in our study is
is partially consistent with the results of Cho et al. [18], 43 years old at which serum AMH levels has already
but regrettably, this difference of ours did not reach sta- reduced, and it may be an another drawback in the
tistical significance. In fact, most important drawback present study. Another limitation of our study was the
of our study was mostly attributable to the relatively inability to conduct an age-matching comparison be-
small sample size, and in particular, the difference in tween the two groups in a sub-group analysis because
sample sizes between the two groups is too large (71 of the small sample size and the relatively higher age of
vs. 15). If our study had had a larger and more even the target patients of our study. Furthermore, AMH is
sample size, this insignificant difference between the known to be recovered at 3 months postoperative after
two groups in our study would have reached statistical ovarian surgery [23], and for this reason, we might as
significance. well checked the serum AMH level at least one more
A prospective cohort study of 83 patients with symp- time around 3 months after the surgery. Finally, vari-
tomatic uterine fibroids who underwent LH with con- ables, such as unexpected events in the operative field,
servation of both ovaries reported that serum AMH which was difficult to compare semiquantitatively, may
levels were decreased significantly at 4 months after LH be additional critical confounding factors in our study.
[15], On the contrary, Abdelazim et al. [16] reported In summary, our results suggest that hysterectomy
that the preoperative AMH level (1.75 ± 4.61 ng/mL) has an effect on the decline of ovarian reserve immedi-
of the 220 studied women was not significantly differ- ately, and this result might be influenced by the type of
ent compared with the AMH level 6 and 12 months surgery. Electro-thermal energy from the laparoscopic
after AH (1.78 ± 2.45 ng/mL and 1.81 ± 2.19 ng/mL, surgical devices may lead to additional damage to the
respectively). The results from these two studies are ovarian reserve. Further prospective large-scale trials
in agreement with our results that serum AMH levels are needed to confirm these preliminary findings.
significantly decreased immediately after surgery in the
LAVH group, but not in the AH group. CONFLICT OF INTEREST
In our study, only AMH levels were assessed as an in-
dicator of ovarian reserve. Of course, AMH is known to No potential conflict of interest relevant to this article
be the most informative marker of ovarian reserve, and was reported.
serum AMH measurement is helpful for counseling
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