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Laparoscopic sleeve gastrectomy effects onoveractive bladder symptoms

Giovanni Palleschi, MD, PhD,a,b Antonio Luigi Pastore, MD, PhD,a,b,*Mario Rizzello, MD,c Giuseppe Cavallaro, MD, PhD,c

Gianfranco Silecchia, MD,c and Antonio Carbone, MDa,b

aDepartment of Sciences and Medico-Surgical Biotechnologies, Urology Unit, ICOT, Sapienza University of Rome,

Latina, ItalybUroresearch Association, Non Profit Association for Basic, Clinical and Surgical Research in Urology, Latina, ItalycCentre of Excellence for Bariatric and Metabolic Surgery, Department of Sciences and Medico-Surgical

Biotechnologies, ICOT, Sapienza University of Rome, Latina, Italy

a r t i c l e i n f o

Article history:

Received 7 January 2015

Received in revised form

7 February 2015

Accepted 13 March 2015

Available online 18 March 2015

Keywords:

Obesity

Overactive bladder

Sleeve gastrectomy

Body mass index

* Corresponding author. Via Ernesto MonaciE-mail address: antopast@hotmail.com (A

0022-4804/$ e see front matter ª 2015 Elsevhttp://dx.doi.org/10.1016/j.jss.2015.03.035

a b s t r a c t

Background: Morbidly obese patients may experience lower urinary tract symptoms. How-

ever, most studies focus only on urinary incontinence, with little regard to other symptoms

as those suggestive for overactive bladder (OAB) syndrome. Laparoscopic sleeve gastrec-

tomy (LSG) is commonly used to treat obesity; this procedure is effective, safe, and capable

of reducing the impact of comorbidities associated with severe increase in body weight.

Therefore, we investigated if LSG improves OAB symptoms in morbidly obese patients.

Methods: We prospectively recruited 120 morbidly obese patients (60 men and 60 women),

evaluated by history taking, comorbidity assessment, physical examination, urinalysis and

urine culture, renal and pelvic ultrasound, a 3-d voiding diary, and the OAB questionnaire

short form. Outcomes of these investigations were assessed 7 d before and 180 d after LSG

was performed. Controls were obese individuals (60 men and 60 women) from an LSG

waiting list.

Results: Symptoms of OAB were common in the morbidly obese cohort, affecting more

women than men. Compared with untreated patients, patients treated with LSG had

significantly reduced body mass index 180 d postoperatively; this outcome was associated

with improvement in OAB symptoms, whereas no change occurred in untreated controls.

Conclusions: OAB symptoms improve in morbidly obese patients successfully treated by

LSG.

ª 2015 Elsevier Inc. All rights reserved.

1. Background diabetes mellitus, cardiovascular and respiratory diseases,

Obesity is a pathology characterized by excessive fat accu-

mulation that presents a risk to health and is consistent with a

body mass index (BMI) �30 kg/m2 [1]. Obesity is associated

with increased incidence of a number of conditions, including

13, 00161 Rome, Italy. Te.L. Pastore).

ier Inc. All rights reserved

and nonalcoholic fatty liver disease, with an increased risk of

disability and a moderate increase in all-cause mortality [2].

Some evidence suggests that lower urinary tract symptoms

(LUTS) may develop in morbidly obese patients [3] and that

various urogenital complications are directly associated with

l.: þ39 3401138648; fax: þ39 0773 6513333.

.

j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 6 ( 2 0 1 5 ) 3 0 7e3 1 2308

obesity [4]. However, most studies focus on urinary inconti-

nence (UI) and pelvic floor disorders, whereas little informa-

tion is available on the overactive bladder (OAB) syndrome,

which is urgency with/without urinary urgency incontinence

(UUI), usually with frequency and nocturia [5]. Laparoscopic

sleeve gastrectomy (LSG) is now a common surgical procedure

for obesity, and within the last decade, several authors have

proposed that it is the definitive treatment for morbid obesity

basing on its efficacy and safety in large randomized trials [6].

Various disorders associated with obesity significantly

improve after BMI reduction achieved by LSG. Therefore, the

aim of the present study was to assess prevalence of OAB

symptoms in a morbidly obese population and to evaluate if

these symptoms improved after LSG.

2. Methods

We prospectively enrolled 120 patients (group A: 60 women

and 60 men) attending the Centre of Excellence for Bariatric

and Metabolic Surgery of the Department of Sciences and

Medico-Surgical Biotechnologies of Sapienza University of

Rome in this study between September 2011 and December

2012. These patients were from a cohort of 192 individuals

with preliminary evaluation based on history, physical ex-

amination (including a rectal and vaginal exploration,

respectively, in men and women), BMI assessment, blood

analysis, urinalysis and urine culture, renal and pelvic ul-

trasound, uroflowmetry with evaluation of postvoid residue,

and a neurologic and psychological evaluation. Inclusion

criteria were morbid obesity (BMI >40 kg/m2), age �18 and

�60 y, and eligibility for laparoscopic surgery. Exclusion

criteria were urine infection, previous gynecologic or uro-

logic surgery, previous or concomitant neoplastic conditions,

any pathologic finding on renal or pelvic ultrasonography,

Figure e The OABq SF. This questionnaire has been specifically

administered.

significant urinary bladder residue (�100 mL), pathologic

findings on uroflowmetry (peak flow <15 mL/s), stress uri-

nary incontinence (SUI), genital prolapse and previous ob-

stetric accidents in women, any previous surgical treatment

for obesity, neurogenic disorders, concomitant consumption

of drugs with anticholinergic activity or psychoactive agents

and any other treatment for LUTS, and serum creatinine

>1.5 mg/dL. Patients meeting the inclusion criteria and

recruited for the study filled in a 3-d voiding diary, which

included fluid intake count (OAB is characterized by at least

eight episodes of micturition per day, presence of urgency,

and a strong and sudden desire to void) and the OAB short-

form questionnaire (OABq SF), a specific investigational tool

developed to assess OAB severity (Figure) [7]. This protocol

was performed at 1 wk (baseline) and 180 d after LSG (con-

trol). Based on the same inclusion and exclusion criteria,

another 120 obese patients (60 women and 60 men) waiting

for bariatric surgery and scheduled to undergo surgery in

2014 were selected as a control population (group B). Pre-

liminary statistical data were used to compare sex, age, and

weight distributions in the two study populations; then, the

following parameters were compared before and after sur-

gery: number of micturitions per day, urgency episodes per

day, number of UUI episodes per day, mean-voided volume

for micturition, liquid intake count per day, and OABq SF

score. Statistical assessment was based on the c2 test and

odds ratios for categorical variables, and the Student t-test

for evaluating differences in continuous measurements.

Considering the strong association between obesity and

diabetes, a multiple linear regression model was used to

evaluate the correlation between OABq SF scores and glyco-

sylated hemoglobin (HbA1c) values in diabetics. All the study

participants signed a consent form, and the study was

approved by the local ethical committee and performed ac-

cording to the Declaration of Helsinki.

developed to diagnose OAB, is easy to fill, and is self-

j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 6 ( 2 0 1 5 ) 3 0 7e3 1 2 309

3. Results

3.1. Clinical findings

Table 1 shows the study data. No difference was found be-

tween the two groups in terms of patient age, BMI, and dis-

tribution of comorbidities and between men and women in

each group. In order of prevalence, comorbidities included

diabetes, dyslipidemia, obstructive sleep apnea syndrome

(OSAS), hypertension, and dysthyroidism. All diabetic patients

were prescribed oral therapy. OSAS diagnosis was based on

polysomnography findings, with determination of the apnea-

hypopnea index and the respiratory disturbance index, which

had already been determined during preoperative evaluation

for LSG. OSASwas diagnosed in 79 patients in group A (22 used

continuous positive air pressure therapy) and 72 patients in

group B (20 used continuous positive air pressure therapy).

3.2. OAB questionnaire and voiding diary outcomes

Patients were asked to report data on the OABq SF referring to

symptoms in the previous 4 wk and to fill the voiding diary

starting 3 d before the assessment. Based on the OABq SF

outcome and voiding diary examination, OAB was diagnosed

in 21 subjects (35%) in group A and 17 subjects (28%) in group

B; these patients were included in subsequent statistical

analysis. In both groups, symptoms were more prevalent in

women than in men (15 women and 6 men in group A and 12

women and 5 men in group B). No difference was found in

mean age and BMI in subpopulations with OAB between the

two groups. All patients with OAB also had diabetes and

dyslipidemia; 16 of 21 subjects in group A and 11 of 17 subjects

Table 1 e Demographic and clinical features two groupsenrolled.

Features Group A Group B

Males

Age: range, mean, and

SD

27e57 y,

42.4 � 8.24

31e55 y,

44 � 6.34

BMI: mean and SD 40 � 4.9 41 � 5.5

Diabetes 44 45

Dyslipidemia 40 44

OSAS 37 35

Hypertension 18 16

Dysthyroidism 13 14

Females

Age: range, mean, and

SD

59e74 y,

64.4 � 7.77

56e73 y,

63.6 � 3.3

BMI: mean and SD 41 � 2.8 40 � 2.7

Diabetes 41 40

Dyslipidemia 49 43

OSAS 42 37

Hypertension 22 20

Dysthyroidism 9 6

NS ¼ not significant; SD ¼ standard deviation.

The results show that the two cohorts do not present significant

difference about sex, age, BMI, and comorbidities distribution.

Diabetes, dyslipidemia, and OSAS were the most represented dis-

orders associated with obesity.

in group B also had OSAS. Differences in hypertension and

dysthyroidism were not significant. Eight women in group A

and 5 women in group B reported UUI episodes. No man re-

ported an UUI episode in both groups. The OABq SF

mean � standard deviation score was 18.69 � 8.9 in group A

and 16.4 � 1.5 in group B, showing a slight, nonsignificant

difference between the two groups. A slightly higher OABq SF

was found in women than in men in both groups and in those

with diabetes and OSAS. Voiding diaries confirmed the results

of the OABq SF, showing at least eight micturitions per day

associated with one or more urinary urgency episodes in all

these subjects; no statistical difference regarding daily fluid

intake and the other parameters assessed by the voiding diary

was observed between the two groups and between men and

women in each group; furthermore, none of the patients in

both groups reported >3 L of urinary voided volume/d, which

could have induced a suspicion of polyuria and consequently

confounded the diagnosis of OAB.

3.3. Surgical outcomes

All patients in group A underwent LSG. For all these patients,

LSG was the first bariatric surgical treatment. Mean operative

time was 64� 9.4min; mean blood loss, 45� 32mL; andmean

hospital stay, 3 � 1.8 d. No significant intraoperative or post-

operative complications were observed.

3.4. Comparison of preoperative and postoperative data

Table 2 compares preoperative data and data obtained at the

180-d follow-up. In group A, a significant decrease in BMI was

observed in all patients who underwent LSG, with no signifi-

cant difference between men and women. In the subgroup

with OAB diagnosis, normal blood glucose levels were

restored in all the patients, with a statistically significant

reduction in mean HbA1c. A concomitant reduction in the

number of subjects with OSAS was observed (from 21 in-

dividuals to 9). For lower urinary symptoms, the OABq SF

score significantly improved (showing a significant reduction

in total score) and a statistically significant improvement in

voiding diary parameters was observed, in particular, urgency

episodes and urinary frequency. UUI still occurred in one of

the eight women who reported this symptom at baseline. The

diary and OABq SF score outcomes showed that 11 of the 21

patients with OAB diagnosis at baseline did notmeet the same

diagnostic criteria at follow-up. A statistical subanalysis

showed a nonsignificant difference in OABq SF scores and

voiding diary improvement between OAB subjects with dia-

betes and OSAS with respect to the remainder of the cohort.

In group B, no significant change in BMI and comorbidities

was observed. In the subgroup of patients with OAB, no sig-

nificant change was seen in voiding diary parameters and

OABq SF scores. The number of patients with OAB diagnosis in

this group remained unchanged. Furthermore, a slight in-

crease in mean BMI was found in this population, and the

indication to perform LSGwas therefore confirmed in all these

subjects. As mentioned previously, all the patients in our

cohort who had obesity and OAB also had diabetes; therefore,

the correlation between OABq SF scores and HbA1c value was

investigated.

Table 2 e Comparison of baseline and control parametersin group A and B.

Parameters Preoperative Postoperative P

Group A

Mean, BMI, and, SD

Males 40.7 � 4.9 31 � 0.9 <0.001

Females 41.2 � 2.8 32 � 1.8 <0.001

Total fluid intake

per 24 h (mL)

1280 (�67.9) 1309 (�68.4) NS*

Total micturitions

per 24 h

9.6 (�1.2) 6.6 (�1.7) <0.001

Urgency episodes

per 24 h

3.5 (�1.1) 0.4 (�1.9) <0.001

UUI episodes per 24 h 1.2 (�0.7) 0 <0.001

Nocturnal

micturitions 24 h

2.3 (�1.2) 1.1 (�1.3) <0.001

Mean voided

volume (mL)

189 � 57 233 � 26 <0.01

OABq score 18.69 � 8.9 12.18 � 3.2 <0.0001

Group B

Mean BMI

Males 41.4 � 5.5 41.7 � 4.5 NS

Females 40.1 � 3.7 40.2 � 3.6 NS

Total fluid intake

per 24 h (mL)

1190 (�37.4) 1201 (�33.2) NS*

Total micturitions

per 24 h

9.2 (�1.4) 9.6 (�1.1) NS

Urgency episodes

per 24 h

3.3 (�0.9) 3.4 (�1.0) NS

UUI episodes per 24 h 1.4 (�0.8) 1.4 (�0.3) NS

Nocturnal

micturitions

per 24 h

2.3 (�1.3) 2.1 (�1.1) NS

Mean voided

volume (mL)

212 � 44 232 � 39 NS

OABq score 16.4 � 1.5 16.8 � 1.1 NS

NS ¼ not significant; SD ¼ standard deviation.

Data regard patients with OAB diagnosis.

P value was considered statistically significant when <0.005.

j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 6 ( 2 0 1 5 ) 3 0 7e3 1 2310

However, Pearson analysis showed no correlation between

the OABq SF scores and HbA1c measurements at baseline in

morbidly obese individuals either in group A (Pearson coeffi-

cient P ¼ 0.24; r ¼ 0.68; v2 ¼ 0.2) or in group B (Pearson coef-

ficient P ¼ 0.24; r ¼ 0.68; v2 ¼ 0.2).

4. Discussion

Obesity is a serious global health issue, and the latest National

Health and Nutrition Examination Survey data show a linear

increasing trend in the overall prevalence of obesity from

1999e2010 [8]. This pathologic condition results in increased

risk of all-cause mortality [9]; therefore, a global campaign

exists to fight obesity, especially in young individuals [10],

because restoration of normal BMI improves all comorbidities

and reduces the risk of mortality [11]. Some research suggests

that LUTS should also be considered to be a comorbidity

associated with obesity. Central obesity, asmeasured by waist

circumference, may predict LUTS severity [12], and severe

obesity is associated with increased risk of urinary disorders

[13]. Therefore, reducing obesity might be an important target

for the prevention of and intervention for LUTS [2,14].

Recently, Khullar et al. reported a post hoc analysis of a large

survey on LUTS performed in the United States, the United

Kingdom, and Sweden (the Epi-LUTS study); they showed that

obesity rates were highest among people with mixed UI (men

and women), SUI þ overflow incontinence (women), UUI, and

UUI plus overflow incontinence (men) [15]. These authors

concluded that BMI is associated with higher risk of UI, as

confirmed by other reports, even if most of the data reported

were for women [16e18]. In females, particularly, a quite

recent investigation performed on 1155 subjects byWhitcomb

et al. reported higher prevalence of pelvic organ prolapse, OAB,

SUI, and any pelvic floor disorder in morbidly compared with

obese women and higher prevalence of SUI in severely obese

compared with obese women [19]. In fact, UI does not repre-

sent all the paradigms of LUTS, and morbidly obese patients

frequently experience other urinary storage symptoms, such

as urinary frequency and urinary urgency, which are themost

common and bothersome. Morandi [4] reviewed the main

noncancer disorders strongly correlated with obesity,

including chronic kidney disease, kidney stones, and urinary

tract disorders, included urinary tract infections, voiding dis-

orders, and symptoms of bladder irritation. Despite the evi-

dence that bladder irritation is common in morbidly obese

patients, no studies have explored OAB syndrome or evalu-

ated if it improves after bariatric surgery. Therefore, we

decided to investigate this topic in our study. We found that

OAB syndrome is common in obese individuals. The exclusion

criteria were selected to minimize the influence of potential

urologic, neurologic, and iatrogenic causes of OAB. OABq SF

scores were consistent with data obtained by the 3-d voiding

diary and supported the reliability of the results at baseline

and follow-up, proving the correlation between obesity and

OAB. The specific mechanism underlying the effect of obesity

on OAB pathogenesis has not been yet described. Previous

studies indicate that poor lifestyle factors are causally linked

to diabetes and obesity and may contribute to the onset of

OAB. In particular, low physical activity appears to be an

important modifiable causal factor for OAB, operating directly

and indirectly via pathways involving obesity or diabetes [20].

This result has been strongly supported by the evidence of a

direct association between diabetes and OAB, which has been

reported in a recent investigation using the OABq SF and

voiding diary in type 2 diabetic individuals [21]. In an animal

model, insulin resistance contributes to detrusor overactivity,

which is a possible cause of OAB symptoms [22]. Other in-

vestigations showed that obesity and concurrent type 2 dia-

betes mellitus lower urinary tract fibrosis and are inextricably

and biologically linked to urinary voiding dysfunction [23].

However, the effect of irritation on obesity can be postulated

based on the assumption that fat in the pelvis reduces bladder

expansion and thus increases urinary frequency and de-

termines low mean urinary volumes for micturition, as

showed by voiding diaries in our study. Therefore, if all these

observations support the hypothesis of both indirect and

direct correlation between obesity and OAB, a significant

improvement in OAB symptoms should be expected after BMI

reduction provided by bariatric surgery, as already reported in

some studies for LUTS. In a prospective trial of more than 200

individuals, Kuruba et al. [24] reported that surgical reduction

j o u r n a l o f s u r g i c a l r e s e a r c h 1 9 6 ( 2 0 1 5 ) 3 0 7e3 1 2 311

of weight results in improvement or resolution of UI in 82% of

patients. This finding was confirmed in more recent in-

vestigations, which describe improvements in urinary and

fecal incontinence in obese subjects after bariatric surgery

[25]. Other reports evaluate the impact of bariatric surgery on

pelvic floor disorders, including symptoms of mixed UI and

storage bladder symptoms. In a cohort of 46 obese women

submitted to bariatric surgery, Whitcomb et al. [26] showed a

significant reduction in total mean distress scores, which was

attributed mainly to the significant decrease in urinary

symptoms. Ranashinghe et al. investigated the effects of

weight loss and time after laparoscopic gastric banding sur-

gery (LGB) on urinary and sexual function. Interestingly, their

study found significant improvement in women assessed

using the International Consultation on Incontinence Ques-

tionnaire short-form score (P¼ 0.0008) and quality of life (QOL;

P < 0.0001) scores; in women, each kilogram lost resulted in a

0.05 improvement in the Incontinence Questionnaire short

form score (P ¼ 0.03), whereas in men, no improvement in UI

occurred after bariatric surgery [27]. In men, post-LGB sexual

function improved on the International Index of Erectile

Function score but the erectile index (P ¼ 0.005) and orgasmic

function (P¼ 0.002) deteriorated when adjusted for time. More

men started using phosphodiesterase type 5 inhibitors after

LGB. Some studies showed that bariatric surgery improved

pelvic floor function [28] and QOL in morbidly obese women.

In a recent study, 44 female subjects undergoing bariatric

surgery were prospectively assessed using a questionnaire for

urinary impact, anorectal impact, and prolapse impact [29].

The results showed that the only questionnaire and the only

symptom that improved, respectively, resulted the pelvic

organ prolapse questionnaire and UI. Another study investi-

gated the hypothesis that bariatric surgery performed to

reduce weight in obese women would reduce the prevalence

and burden of pelvic floor disease and improve QOL [30]. In

this trial of 98 womenwith SUI, OAB, and anal incontinence at

baseline, 11/23 (48%), 8/11 (73%), and 4/20 (20%) women,

respectively, showed resolution of symptoms at 12 mo.

Scozzari et al. [31] recently showed that after bariatric surgery

was performed in 32 women, pelvic floor disease symptoms

related to UI improved slightly but anorectal function did not

change significantly and flatus incontinence increased.

All these data show a strong favorable impact of bariatric

surgery on LUTS, in agreement with our investigation, which

specifically confirmed this for OAB. Even though our study

adds to the literature, the generic association between LUTS

and obesity requires confirmation. Most available data are for

women but obese men also experience urinary disorders, as

evidenced by our results and the Epi-LUTS study. Obesity

markedly increases the risk of benign prostatic hyperplasia,

which is responsible for voiding and storage symptoms;

physical activity decreases the risk of benign prostatic hy-

perplasia [32]. The onset of storage symptoms secondary to

bladder outlet obstruction is common in both men and

women. Therefore, we specifically excluded patients with low

urinary flow indexes and significant postvoiding residue to

exclude individuals with a specific urologic disorder and those

who did not have OAB as a direct or indirect consequence of

obesity.

5. Conclusions

In morbidly obese patients, the onset of OAB symptoms may

have a complicated pathophysiology involving endocrine,

dysmetabolic, respiratory, and cardiovascular factors of vari-

able distribution but very often expressed contemporarily in

these patients. Therefore, as already shown for other comor-

bidities associated with obesity, the best method to overcome

OAB symptoms in morbidly obese individuals is to restore

normal BMI, thus reducing all contributing factors leading to

OAB onset. In our pilot investigation, in fact, OAB symptoms

resulted well represented in morbidly obese patients, with a

moderate prevalence in women, and the significant decrease

in BMI at the 6-mo follow-up after LSG results in amelioration

of OAB symptoms.

Acknowledgment

The authors acknowledge the patients and their families for

their willingness to collect questionnaires data.

Authors’ contributions: G.P., A.L.P., M.R., and G.C. contrib-

uted to the planning including the design and interpretation

of the data andwere responsible for the acquisition of the data

and the analysis. All authors contributed to the drafting,

revising, and final approval of the article.

Disclosure

The authors declare that they have no competing interests.

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