Impact of Obesity and Hyperglycemia on Pregnancy-specific Urinary Incontinence

Impacto da obesidade e hiperglicemia na incontinência urinária específica da gravidez

Abstract

Objective

The lack of data on the impact of hyperglycemia and obesity on the prevalence of pregnancy-specific urinary incontinence (PSUI) led us to conduct a cross-sectional study on the prevalence and characteristics of PSUI using validated questionnaires and clinical data.

Methods

This cross-sectional study included 539 women with a gestational age of 34 weeks who visited a tertiary university hospital between 2015 and 2018. The main outcome measures were the prevalence of PSUI, the International Consultation on Incontinence Questionnaire Short Form (ICIQ-SF), and the Incontinence Severity Index (ISI) questionnaires. The women were classified into four groups: normoglycemic lean, normoglycemic obese, hyperglycemic lean, and hyperglycemic obese. The differences between groups were tested using descriptive statistics. Associations were estimated using logistic regression analysis and presented as unadjusted and adjusted odds ratios.

Results

Prevalence rates of PSUI were no different between groups. However, significant difference in hyperglycemic groups worse scores for severe and very severe PSUI. When adjusted data for confound factors was compared with normoglycemic lean group, the hyperglycemic obese group had significantly higher odds for severe and very severe forms of UI using ICIQ-SF (aOR 3.157; 95% CI 1.308 to 7.263) and ISI (aOR 20.324; 95% CI 2.265 to 182.329) questionnaires and highest perceived impact of PSUI (aOR 4.449; 95% CI 1.591 to 12.442).

Conclusion

Our data indicate that obesity and hyperglycemia during pregnancy significantly increase the odds of severe forms and perceived impact of PSUI. Therefore, further effective preventive and curative treatments are greatly needed.

Keywords
urinary incontinence; pregnancy; diabetes mellitus; maternal obesity

Resumo

Objetivo

A falta de dados sobre o impacto da hiperglicemia e obesidade na prevalência de incontinência urinária específica da gravidez (IAPS) nos levou a realizar um estudo transversal sobre a prevalência e características da IAPS usando questionários validados e dados clínicos.

Métodos

Este estudo transversal incluiu 539 mulheres com idade gestacional de 34 semanas que visitaram um hospital universitário terciário entre 2015 e 2018. As principais medidas de desfecho foram a prevalência de PSUI, o formulário curto do International Consultation on Incontinence Questionnaire (ICIQ-SF) e os questionários do Incontinence Severity Index (ISI). As mulheres foram classificadas em quatro grupos: magras normoglicêmicas, obesas normoglicêmicas, magras hiperglicêmicas e obesas hiperglicêmicas. As diferenças entre os grupos foram testadas por meio de estatística descritiva. As associações foram estimadas usando análise de regressão logística e apresentadas como odds ratio não ajustadas e ajustadas.

Resultados

As taxas de prevalência de PSUI não foram diferentes entre os grupos. No entanto, houve diferença significativa nos grupos hiperglicêmicos com piores escores para PSUI grave e muito grave. Quando os dados ajustados para fatores de confusão foram comparados ao grupo magro normoglicêmico, o grupo obeso hiperglicêmico teve chances significativamente maiores de formas graves e muito graves de IU usando ICIQ-SF (aOR 3,157; IC 95% 1,308 a 7,263) e ISI (aOR 20,324; 95% CI 2,265 a 182,329) questionários e maior impacto percebido de PSUI (aOR 4,449; 95% CI 1,591 a 12,442).

Conclusão

Nossos dados indicam que a obesidade e a hiperglicemia durante a gravidez aumentam significativamente as chances de formas graves e o impacto percebido da PSUI. Portanto, tratamentos preventivos e curativos mais eficazes são extremamente necessários.

Palavras-chave
incontinencia urinaria; gravidez; diabetes mellitus; obesidade materna

Introduction

Urinary incontinence (UI) may be a very common experience during a woman’s lifetime,¹ with a robust influence on well-being and quality of life, as well as an immense economic burden for health services.² Estimates of the prevalence and incidence of UI depend on the definitions of the study type and population. Previous epidemiological data showed that the prevalence of UI in women older than 20 years was 23.4–26.4% in the United States.³ In Brazil, it is considered a common health problem, with an estimated prevalence rate of 27%.⁴ Therefore, UI is an important public health concern.

Pregnancy appears to be a major risk factor, particularly during late gestation.⁵ In general population, the risk of UI during pregnancy is 18–75%.⁶ The term pregnancy-specific UI (PSUI) is used to define any urinary leakage onset during pregnancy.⁷ The risk of UI increases as pregnancy progresses due to anatomical and hormonal changes.⁶,⁸ Despite certain risk factors being established for PSUI, some risk factors, such as gestational diabetes mellitus (GDM), are still under consideration. Although some perinatal morbidities related to GDM are associated with UI, GDM alone is considered an independent risk factor for all UI types on post-partum.⁹ Taken together, these studies provide compelling evidence for an association between GDM and post-partum UI. Likewise, women with a previous diagnosis of GDM have a well-known increased risk to develop type 2 diabetes mellitus (20–50%) by 10 years postpartum.¹⁰ Obesity (body mass index [BMI] > 30 kg/m²) and weight gain during pregnancy are some of the main modifiable risk factors for the development of postpartum diabetes.¹¹ In the United States, from 1999 to 2010, obesity increased from 28.4% to 34% in women aged 20–39 years.¹² Moreover, 15–20% of mothers have pre-pregnancy obesity¹³ and 20–40% experience excessive weight gain during pregnancy.¹⁴ Increased BMI has consistently been reported to play a role in the occurrence of clinical UI.¹⁵

Given that the prevalence of obesity has increased in recent decades, and it is one of the most common medical conditions in women of reproductive age,¹⁶ the premise that obesity and diabetes are linked and are considered a prominent risk factor for developing UI is concerning. Despite compelling epidemiologic data supporting the association of GDM and post-partum UI,⁹ as well as obesity and UI,¹⁷ little is known about how hyperglycemia and concurrent obesity might affect the severity of PSUI. Furthermore, current international clinical practice guidelines for UI management fail to present specific recommendations for pregnant women with comorbid conditions, including GDM and obesity, and the treatment of such patients remains a neglected aspect of care.¹⁸,¹⁹ Therefore, we hypothesized that GDM and obesity are associated with higher odds of PSUI severity.

The present study aimed to investigate the prevalence of PSUI in a population using questionnaires and clinical data to assess the possible associations between PSUI severity, GDM, and obesity.

Methods

This cross-sectional study focuses on the relationship between UI, obesity, and GDM. All pregnant women were recruited at the time of prenatal care follow-up at the University Hospital from the Perinatal Diabetes Research Centre (PDRC) of Botucatu Medical School/UNESP/Brazil between 2015 and 2018 and were screened for GDM.

We identified four groups of patients categorized as normoglycemic lean (NL), normoglycemic obese (NO), hyperglycemic lean (HL), and hyperglycemic obese (HO). The diagnosis of GDM was established between the 24th and 28th gestational weeks, using the 75-g oral glucose tolerance test (OGTT) according to the American Diabetes Association criteria²⁰ and glycemic profile.²¹,²² All women with positive screening results for GDM or altered glycemic profiles were classified as hyperglycemic. Glycemic control of women following a diagnosis of hyperglycemia followed the protocol in PDRC. The protocol includes a team of healthcare professionals that encourage adequate nutrition, exercise, and insulin administration.²¹ The cut-off for obesity was a BMI of > 30 kg/m² (calculated using the participant’s height and weight).²³ The inclusion criteria were restricted to women with singleton pregnancies who underwent an OGTT between 24 and 28 weeks of pregnancy with a new onset of urinary leakage during pregnancy. Pre-pregnancy UI, known type 1 or type 2 diabetes mellitus, preterm delivery (< 37 weeks of gestation), multiple pregnancies, known fetal anomaly, or any clinical condition that may have jeopardized the health status of the woman were considered as the exclusion criteria.

Data on baseline information (age, parity, pre-pregnancy and current BMI, weight gain during pregnancy, educational level, marital status, fasting glucose, and glycosylated hemoglobin) were collected during the interview at of 34 weeks of gestation and medical records assessment. The Brazilian version of the Incontinence Severity Index (ISI) was used to categorize incontinence severity.²⁴ The multiplicative score is based on two questions assessing the frequency and volume of incontinence.²⁵ Women were also asked to complete the Brazilian version of the International Consultation on Incontinence Questionnaire-Urinary Incontinence Short Form (ICIQ-UI SF).²⁶ The ICIQ-UI SF comprises three scored items and one non-scored item, making it possible to assess the prevalence, severity, interference in daily life, and type of UI.²⁶ The ICIQ-UI SF score ranges from 0 to 21. Scores on the perceived impact of those reporting UI are set from ‘0’ as not at all to ‘10’ as a great deal. One non-scored item of the ICIQ-UI SF includes eight answers and is a self-diagnostic item to understand the participant’s perception of the cause and type of leakage. A form completed immediately after birth was used to record the labor process, mode of delivery, and neonatal birth profile.

The primary outcome was the PSUI prevalence among the groups. UI was classified according to the International Continence Society guidelines for stress UI (SUI) (involuntary leakage on effort or exertion, sneezing, or coughing), urge UI (UUI) (involuntary leakage accompanied by or immediately preceded by urgency), and mixed UI (MUI) (involuntary leakage associated with urgency and exertion, effort, sneezing, or coughing).²⁷ Secondary outcomes were the prevalence of SUI, UUI, and MUI, as well as the frequency of UI, amount of leakage, the ISI score, the ICIQ-UI score, and perceived impact of UI.

SAS version 9.4 for Windows (Statistical Analysis System Institute Inc., USA) was used for statistical analyses. Clinical features are presented as frequencies and percentages or as means with standard deviations. Differences between groups were tested using chi-square or analysis of variance followed by the Tukey–Kramer analysis. A logistic regression model was used to assess the association between GDM and obesity and UI. Only clinical features with a p-value < 0.05 were included in the adjusted logistic regression analysis (age, gestational age, parity, previous newborn weight, hypertension, newborn weight, and classification).

This study was approved by the Research Ethics Committee of the institution (CAAE: 41570815.0.0000.5411). All patients were informed about the purpose of the study, and those who agreed to participate signed a consent form before recruitment.

Results

Among the 563 women eligible for recruitment, 539 (95.7%) agreed to participate in the present study. Among these patients, 172 participants were included in the NL group (31.91%), 113 in the NO group (20.97%), 109 in the HL group (20.22%), and 145 in the HO group (26.90%). Baseline characteristics differed between groups, including clinical features such as age, gestational age, parity, previous newborn weight, hypertension, newborn weight, and classification. The background variables of the study population are shown in Table 1.

Table 1
Clinical features of the study population

	Total population (n = 539)	Normoglycemic Lean (n = 172) 31.91%	Normoglycemic Obese (n = 113) 20.97%	Hiperglycemic Lean (n = 109) 20.22%	Hiperglycemic Obese (n = 145) 26.90%	p-value between groups
Age (years)	29.12 (6.44)	27.20 (6.15)	28.12 (6.47)	29.73 (7.15)a	31.68 (5.25)a,b
Gestational age (weeks)	36.85 (1.58)	37.01 (1.57)	37.30 (1.63)	36.54 (1.51)a	36.54 (1.52)a,b
Parity	1.11 (1.02)	1.02 (0.99)	0.97 (1.03)	1.06 (0.98)	1.37 (1.04) a,b,c
Previous newborn (g)	2237.27 (1601.06)	1950.31 (1590.17)	2221.50 (1590.23)	2188.87 (1655.11)	2627.24 (1518.14)a
Weight gain during pregnancy (kg)	10.34 (7.59)	13.15 (6.57)	9.16 (9.05)a	11.8 (6.52)b	6.74 (6.57)a,b,c
Prepregnancy BMI (kg/m2)	30.46 (7.46)	24.34 (3.27)	36.44 (5.12)a	25.49 (3.24)b	36.77 (5.93) a,c
Pregnancy BMI (kg/m2)	34.52 (7.21)	29.53 (3.97)	40.37 (7.01)a	30.18 (4.13)b	39.16 (5.70)a,c
OGTT (mg/dL)
Fasting	82.86 (16.42)	72.24 (7.65)	76.27 (7.59)	89.69 (17.06)a,b	94.74 (17.07)a,b,c
1 hour	134.77 (40.78)	107.50 (23.88)	115.58 (26.64)	159.72 (37.04)a,b	166.65 (36.28)a,b
2 hours	117.39 (56.78)	96.27 (20.10)	110.63 (98.77)a	136.59 (39.41)a,b	135.22 (38.69)a,b
Glycemic mean (mg/dL)	90.31 (13.54)	82.28 (8.46)	84.33 (7.98)	96.24 (10.36)a,b	99.43 (15.67)a,b
HbA1c	5.24 (0.55)	4.91 (0.42)	5.12 (0.47)a	5.33 (0.41)a,b	5.59 (0.59)a,b,c
Hypertension	161 (29.87%)	29 (16.86%)	56 (49.56%)	18 (16.51%)	47 (40%)	<.0001
Race
White	361 (66.98%)	127 (73.84%)	79 (69.91%)	67 (61.47%)	88 (60.69%)	0.0605
Non-white	178 (33.02%)	45 (26.16%)	34 (30.09%)	42 (38.53%)	57 (39.31%)
Smoker	53 (9.83%)	17 (9.88%)	9 (7.96%)	13 (11.93%)	14 (9.66%)	0.8038
Vaginal	202 (40.89%)	78 (53.42%)	44 (40.74%)	38 (36.89%)	42 (30.66%)	0.0011
C-section	292 (59.11%)	68 (46.58%)	64 (59.26%)	65 (63.11%)	95 (69.34%)
Newborn weight (g)	3367.28 (511.25)	3287.11 (493.22)	3350.09 (480.12)	3337.70 (506.14)	3496.01 (535.51)a
Newborn weight classification
SGA	31 (6.39%)	16 (11.19%)	5 (4.72%)	7 (6.86%)	3 (2.24%)	0.0058
AGA	403 (83.09%)	114 (79.72%)	94 (88.68%)	87 (85.29%)	108 (80.60%)
LGA	51 (10.52%)	13 (9.09%)	7 (6.60%)	8 (7.84%)	23 (17.16%)

• Abbreviations: AGA, appropriate for gestational age; BMI, Body Mass Index; HbA1c, Glycated Hemoglobin; LGA, large for gestational age; OGTT, Oral Glucose Tolerance Test; SGA, small for gestational age.
• ^a
  p < 0.05–indicate significant difference compared with normoglycemic lean group (Tukey-Kramer).
• ^b
  p < 0.05 - indicate significant difference compared with normoglycemic obese group (Tukey-Kramer).
• ^c
  p < 0.05 - indicate significant difference compared with hiperglycemic lean group (Tukey-Kramer).

The overall prevalence of PSUI was 70.87% (n = 382), with no difference in the prevalence or type of UI between groups (Table 2). However, the HO group had more frequent (p < 0.0001) and more abundant (p = 0.0009) higher scores for the perceived impact of UI (p < 0.0001), ICIQ-UI SF (p < 0.0001), and ISI (p < 0.0001) questionnaires (Table 3).

Table 2
Prevalence of Pregnancy-Specific Urinary Incontinence (PSUI), stress urinary incontinence (SUI), urge urinary incontinence (UUI) and mixed urinary incontinence (MUI)

		Total population (n = 539)	Normoglycemic Lean (n = 172)	Normoglycemic Obese (n = 113)	Hiperglycemic Lean (n = 109)	Hiperglycemic Obese (n = 145)	p-value between groups
PSUI	Yes	382 (70.87%)	115 (66.86%)	85 (75.22%)	73 (66.97%)	109 (75.17%)	0.2143
	No	157 (29.13%)	57 (33.14%)	28 (24.78%)	36 (33.03%)	36 (24.83%)
PSUI (n = 382)	UI	1 (0.26%)	0 (0%)	1 (100%)	0 (0%)	0 (0%)	0.1224
	SUI	152 (39.79%)	51 (44.35%)	26 (30.59%)	35 (47.95%)	40 (36.70%)
	MUI	201 (52.62%)	57 (49.57%)	50 (58.82%)	30 (41.10%)	64 (58.72%)
	UUI	28 (7.33%)	7 (6.09%)	8 (9.41%)	8 (10.96%)	5 (4.59%)

• PSUI: Pregnancy-Specific Urinary Incontinence; UI: Urinary incontinence; SUI: stress urinary incontinence; UUI: urge urinary incontinence; MUI: mixed urinary incontinence

Table 3
Frequency, duration, amount of leakage, scores for the perceived impact of those reporting UI, ICIQ UI-SF and ISI scores

			Total population (n = 539)	Normoglycemic Lean (n = 172) 31.91%	Normoglycemic Obese (n = 113) 20.97%	Hiperglycemic Lean (n = 109) 20.22%	Hiperglycemic Obese (n = 145) 26.90%	p-value between groups§
ICIQ UI-SF	Frequency of incontinence episodes	No leakage	157 (29.13%)	57 (33.14%)	28 (24.78%)	36 (33.03%)	36 (24.83%)	<0.0001
		≤Once/week	146 (27.09%)	63 (36.63%)	38 (33.63%)	22 (20.18%)	23 (15.86%)
		2–3 times/week	83 (15.40%)	25 (14.53%)	12 (10.62%)	20 (18.35%)	26 (17.93%)
		Once/day	60 (11.13%)	13 (7.56%)	17 (15.04%)	8 (7.34%)	22 (15.17%)
		>Once/day	78 (14.47%)	11 (6.40%)	12 (10.62%)	22 (20.18%)	33 (22.76%)
		All the time	15 (2.78%)	3 (1.74%)	6 (5.31%)	1 (0.92%)	5 (3.45%)
	Amount of leakage	None	157 (29.13%)	57 (33.14%)	28 (24.78%)	36 (33.03%)	36 (24.83%)	0.0009
		Small	217 (40.26%)	78 (45.35%)	56 (49.55%)	41 (37.61%)	42 (28.97%)
		Moderate	121 (22.45%)	31 (18.02%)	20 (17.70%)	22 (20.18%)	48 (33.10%)
		Severe	44 (8.16%)	6 (3.49%)	9 (7.96%)	10 (9.17%)	19 (13.10%)
		Score perceived impact of those reporting UI (n = 382)	4.16 (3.72)	5.12 (3.01)	5.12 (3.17)	5.26 (3.61)	6.69 (3.11)* # ‡
		ICIQ UI-SF score (n = 539)	7.76 (6.41)	6.49 (5.78)	7.47 (5.93)	7.27 (6.51)	9.64 (6.97) a b c
	Perceived impact of those reporting UI (n = 382)	Not at all	39 (10.21%)	11 (9.57%)	9 (10.59%)	13 (17.81%)	6 (5.50%)	<0.0001
		Mildly	76 (19.9%)	26 (22.61%)	21 (24.71%)	13 (17.81%)	16 (14.68%)
		Moderately	97 (25.39%)	40 (34.78%)	27 (31.76%)	14 (19.18%)	16 (14.68%)
		Severely	112 (29.32%)	22 (19.13%)	15 (17.65%)	26 (35.62%)	49 (44.95%)
		To a great extent	58 (15.18%)	16 (13.91%)	13 (15.29%)	7 (9.59%)	22 (20.18%)
	ICIQ UI-SF (n = 539)	None	157 (29.13%)	57 (33.14%)	28 (24.78%)	36 (33.03%)	36 (24.83%)	<0.0001
		Slight	61 (11.32%)	20 (11.63%)	15 (13.27%)	15 (13.76%)	11 (7.59%)
		Moderate	167 (30.98%)	65 (37.79%)	45 (39.82%)	27 (24.77%)	30 (20.69%)
		Severe	132 (24.49%)	26 (15.12%)	19 (16.81%)	30 (27.52%)	57 (39.31%)
		Very Severe	22 (4.08%)	4 (2.33%)	6 (5.31%)	1 (0.92%)	11 (7.59%)
	ISI (n = 382)	Slight	123 (32.20%)	53 (46.09%)	33 (38.82%)	22 (30.14%)	15 (13.76%)	<0.0001
		Moderate	135 (35.34%)	42 (36.52%)	33 (38.82%)	25 (34.25%)	35 (32.11%)
		Severe	86 (22.51%)	15 (13.04%)	11 (12.94%)	19 (26.03%)	41 (37.61%)
		Very Severe	38 (9.95%)	5 (4.35%)	8 (9.41%)	7 (9.59%)	18 (16.51%)

• Abbreviations: ICIQ-SF, International Consultation on Incontinence Questionnaire-Urinary Incontinence-Short Form; ISI, Incontinence Severity Index; UI, Urinary incontinence.
• ^a
  p < 0.05–indicate significant difference compared with normoglycemic lean group (Tukey-Kramer).
• ^b
  p < 0.05 - indicate significant difference compared with normoglycemic obese group (Tukey-Kramer).
• ^c
  p < 0.05 - indicate significant difference compared with hiperglycemic lean group (Tukey-Kramer).
• ^*
  p < 0.05–indicate significant difference compared with normoglycemic lean group (Poisson).
• ^#
  p < 0.05 - indicate significant difference compared with normoglycemic obese group (Poisson).
• ^‡
  p < 0.05 - indicate significant difference compared with hiperglycemic lean group (Poisson).
• ^§
  Chi-square test.

Table 4 shows the logistic regression analysis with unadjusted and adjusted UI. Surprisingly, when adjusted for age, gestational age, parity, previous newborn weight, hypertension, newborn weight, and classification, the hyperglycemic group had significantly higher odds of UI severity than the other groups in the study. Furthermore, these groups presented a higher perceived impact of UI, ISI, and ICIQ-UI SF severe scores.

Table 4
Unadjusted and adjusted odds ratio in the four groups

		Normoglycemic Lean (n = 172)	Normoglycemic Obese (n = 113)	Hiperglycemic Lean (n = 109)	Hiperglycemic Obese (n = 145)
Unadjusted						p-value between groups
			OR with 95% CI	OR with 95% CI	OR with 95% CI
	PSUI	1	1.505 (0.884 - 2.562)	1.005 (0.604 - 1.674)	1.501 (0.917 - 2.456)	0.2164
PSUI	SUI	1	0.563 (0.312 - 1.016)	1.156 (0.642 - 2.082)	0.727 (0.426 - 1.243)	0.1056
	MUI	1	1.496 (0.847 - 2.643)	0.710 (0.393 - 1.284)	1.447 (0.853 - 2.454)	0.0586
	UUI	1	1.624 (0.565 - 4.669)	1.899 (0.658 - 5.481)	0.742 (0.228 - 2.411)	0.3427
Perceived impact of those reporting UI	Not at all	1	0.745 (0.453 - 1.225)	1.249 (0.769 - 2.030)	0.624 (0.389 - 0.999)	0.0419
	Mildly	1	1.123 (0.581 - 2.170)	0.742 (0.353 - 1.557)	0.589 (0.296 - 1.171)	0.2871
	Moderately	1	0.873 (0.481 - 1.585)	0.445 (0.221 - 0.894)	0.323 (0.168 - 0.621)	0.0021
	Severely	1	0.906 (0.438 - 1.872)	2.338 (1.200 - 4.558)	3.452 (1.897 - 6.282)	<0.0001
	To a great extent	1	1.117 (0.506 - 2.467)	0.656 (0.256 - 1.682)	1.565 (0.773 - 3.168)	0.2690
ICIQ UI-SF	None	1	0.665 (0.390 - 1.132)	0.995 (0.597 - 1.657)	0.666 (0.407 - 1.091)	0.0419
	Slight	1	1.163 (0.568 - 2.380)	1.213 (0.596 - 2.484)	0.624 (0.288 - 1.349)	0.3856
	Moderate	1	1.089 (0.670 - 1.772)	0.542 (0.318 - 0.924)	0.429 (0.259 - 0.713)	0.0008
	Severe	1	1.135 (0.595 - 2.165)	2.132 (1.179 - 3.855)	3.637 (2.132 - 6.204)	<0.0001
	Very Severe	1	2.355 (0.649 - 8.540)	0.389 (0.043 - 3.526)	3.448 (1.074 - 11.072)	0.0580
ISI	Slight	1	0.742 (0.420 - 1.313)	0.505 (0.271 - 0.938)	0.187 (0.097 - 0.360)	<0.0001
	Moderate	1	1.103 (0.619 - 1.967)	0.905 (0.490 - 1.674)	0.822 (0.473 - 1.429)	0.7878
	Severe	1	0.991 (0.430 - 2.282)	2.346 (1.104 - 4.983)	4.020 (2.063 - 7.831)	<0.0001
	Very Severe	1	2.285 (0.720 - 7.249)	2.332 (0.711 - 7.647)	4.350 (1.555 - 12.171)	0.0372
adjusted
	PSUI	1	0.760 (0.297 - 1.949)	2.439 (1.016 - 5.855)	0.631 (0.256 - 1.557)	0.0238
PSUI	SUI	1	0.567 (0.220 - 1.462)	2.012 (0.664 - 6.099)	0.637 (0.261 - 1.551)	0.1220
	MUI	1	1.241 (0.498 - 3.095)	0.490 (0.158 - 1.513)	1.820 (0.766 - 4.328)	0.1138
	UUI	1	2.372 (0.500 - 11.257)	0.927 (0.135 - 6.352)	0.420 (0.063 - 2.784)	0.3238
Perceived impact of those reporting UI	Not at all	1	0.687 (0.281 - 1.680)	2.066 (0.874 - 4.885)	0.511 (0.214 - 1.216)	0.2222
	Mildly	1	2.221 (0.770 - 6.407)	0.822 (0.212 - 3.182)	0.805 (0.270 - 2.400)	0.2564
	Moderately	1	1.156 (0.445 - 3.001)	0.301 (0.087 - 1.039)	0.300 (0.111 - 0.809)	0.0271
	Severely	1	0.468 (0.126 - 1.737)	3.810 (1.134 - 12.801)	4.449 (1.591 - 12.442)	0.0005
	To a great extent	1	0.920 (0.239 - 3.537)	0.962 (0.195 - 4.747)	1.198 (0.361 - 3.977)	0.9752
ICIQ UI-SF	None	1	0.760 (0.297 - 1.949)	2.439 (0.516 - 5.855)	0.631 (0.256 - 1.557)	0.2381
	Slight	1	0.677 (0.181 - 2.539)	0.600 (0.145 - 2.474)	0.631 (0.180 - 2.217)	0.8412
	Moderate	1	2.081 (0.903 - 4.793)	0.204 (0.071 - 0.584)	0.415 (0.178 - 0.964)	0.0001
	Severe	1	0.438 (0.141 - 1.357)	2.244 (0.885 - 5.691)	3.157 (1.308 - 7.623)	0.0012
	Very Severe	1	3.852 (0.357 - 41.511)	3.389 (0.443 - 33.526)	6.496 (0.662 - 63.742)	0.4536
ISI	Slight	1	0.759 (0.297 - 1.939)	0.214 (0.059 - 0.774)	0.194 (0.072 - 0.527)	0.0042
	Moderate	1	1.739 (0.683 - 4.427)	1.106 (0.377 - 3.242)	0.587 (0.234 - 1.472)	0.1660
	Severe	1	0.208 (0.037 - 1.188)	2.297 (0.617 - 8.547)	3.130 (1.070 - 9.153)	0.0059
	Very Severe	1	6.092 (0.603 - 61.538)	11.709 (1.027 - 133.489)	20.324 (2.265 - 182.392)	0.0381

• Abbreviations: ICIQ-SF, International Consultation on Incontinence Questionnaire-Urinary Incontinence-Short Form; ISI, Incontinence Severity Index; MUI, mixed urinary incontinence; PSUI, Pregnancy-Specific Urinary Incontinence; SUI, stress urinary incontinence; UI, Urinary incontinence; UUI, urge urinary incontinence.

Discussion

To the best of our knowledge, this is the first study to assess the influence of obesity and hyperglycemia on the odds of PSUI severity. This cross-sectional study assessed the prevalence, frequency, amount, perceived impact, and severity of PSUI in women as of 34 weeks of gestation. Overall, a high prevalence (70.87%) of PSUI among the 539 participants. We found the highest odds of PSUI severity and the perceived impact of UI in women with hyperglycemia. Even after adjustment for various confounders, including age, gestational age, parity, previous newborn weight, hypertension, newborn weight and classification, women with hyperglycemia without obesity presented the highest odds of PSUI (adjusted odds ratio [aOR]: 2.43; 95% confidence interval [CI]: 1.01–5.85). We observed a substantial increase in the odds of extremely severe PSUI in the HL (aOR: 11.70; 95% CI: 1.02–133.48) and HO groups (aOR: 20.32; 95% CI: 2.26–182.39). Our logistic regression model found that hyperglycemia alone and hyperglycemia linked to obesity were also associated with severe perceived impact of UI in daily life (aOR: 3.81; 95% CI: 1.13–12.80; aOR: 4.44; 95% CI: 1.59–12.44). The persistence, progression and severity of pelvic floor dysfunction can have a significant impact on women’s quality of life.²⁸

With respect to the baseline characteristics of the present study, this cohort represented the underlying population characteristics of women with hyperglycemia during pregnancy. Advancing maternal age has been recognized as a major risk factor for the development of hyperglycemia during pregnancy.²⁹ The other risk factors greater parity, increased BMI, and hypertension.³⁰,³¹ Our data indicate these risk factors in the present cohort of the hyperglycemic groups. Such risk factors are also associated with an increased risk of developing UI.⁶,³² In our study, although women in the HO group presented lower weight gain during pregnancy, which may be related to the fact that they received the treatment at PDRC, the symptoms related to UI appeared to be more severe than those in the other groups.

According to Daly et al.,³³ 21.7% of the population studied presented women with new-onset leakage who were continent in the 12 months before pregnancy. Brown et al.,³⁴ found that the most common PSUI is SUI, characterized by unintentional loss of urine during physical movement or activity (e.g., sneezing, coughing, running, or heavy lifting). The pathophysiology of PSUI is multifactorial and yet to be understood. It has been implicated that hormonal and mechanical changes may play an important role.³⁵ In our sample, there was no difference in the prevalence of the UI types between the groups. Studies showed that irrespective of the type, UI has detrimental effects on the quality of life in ∼54.3% of all pregnant women³⁶ and the quality of life of pregnant women with incontinence worsens with increasing gestational age to term.³⁷ Our sample presented higher prevalence of PSUI rates (70.87%) when compared the general literature. However, this corresponds with a similar study with smaller sample size, in the same gestational period (i.e., 34–38 weeks of gestation) the prevalence rate was 60.5%.³⁸ Further research is needed to explore the differences in prevalence of PSUI in multicentric and multi-ethnic groups.

Our findings show that women with a BMI of ≥ 30 kg/m² are significantly more likely to report less frequent incontinence episodes and amount of leakage, moderately perceived impact of UI, and slight to moderate UI severity. A large longitudinal study that enrolled 10,098 women who were followed up as of 28 weeks of gestation found that high prenatal BMI increased the risk of SUI in late pregnancy (OR: 1.037; 95% CI: 1.020–1.054).³⁹ Overweight and obesity are considered major modifiable risk factors for UI in young and middle-aged women.⁴⁰ Previous studies have shown that middle-aged women with obesity are 3.1 times more likely to have severe UI than women with BMI in the normal range.⁴¹ These differences might be related to the different types of inquiries used to address UI symptoms and study designs. Anatomical changes in patients with obesity assessed by ultrasonography showed that bladder neck descent was more evident in women with obesity than in women with normal weight.⁴² A high BMI increases intra-abdominal pressure, resulting in an imbalance between vesical pressure and urethral closure, triggering urine leakage.¹⁵,⁴³

The first study to report the prevalence of UI in women with GDM was conducted by Kim et al.⁴⁴ They recruited 228 women with GDM; 49% reported weekly or more episodes of incontinence during pregnancy and 50% after delivery.⁴⁴ Another cross-sectional study found that GDM was an independent risk factor (OR: 2.26; 95% CI: 1.116–4.579) for PSUI, and PSUI was a risk factor 2 years post cesarean section UI (OR: 4.992; 95% CI: 1.383–18.023).⁴⁵ A large study⁹ recruited 6653 women who were followed up for 2 years postpartum to investigate the association between GDM and postpartum UI. They demonstrated that women with GDM were more likely to report SUI (OR: 1.97; 95% CI: 1.56–2.51), UUI (OR: 3.11; 95% CI: 2.18–4.43), and MUI (OR, 2.73; 95% CI: 1.70–4.40).⁹ Furthermore, another study showed that the occurrence of PSUI, the severity of UI, and the negative impact of UI on the quality of life are increased in women with hyperglycemia during pregnancy.³⁸ Recent studies⁴⁶,⁴⁷ conducted in animal models and pregnant women have aimed to identify and quantify the morphological changes in the rectus abdominis muscles due to hyperglycemia during pregnancy. Changes in the fiber type, fiber area, and collagen content have been reported and may be related to diabetic myopathy.

The strengths of this study include the use of validated questionnaires that enable the identification of the type, frequency, severity, and perceived impact of UI. The International Consultation on Incontinence recognized that ICIQ questionnaires are grade A (high-quality) measurement instruments for assessing UI.⁴⁸ Another strength of our study is the use of a database with the glycemic values of the participants and the established diagnostic criteria for GDM and obesity. An important limitation is the limited number of participants that could have powered our results and the lack of an objective measure of UI assessment, such as bladder diaries, pad test, and/or urodynamic test, to compare with our subjective measures.

Conclusion

The results of the present study show that hyperglycemia during pregnancy is an independent risk factor for PSUI. The logistic regression models showed that when compared with the normoglycemic lean women, women who are obese and have hyperglycemia during pregnancy are more likely to experience severe and very severe PSUI with important perceived impact on daily life. The findings from our study provide information on PSUI in volunteers at the third trimester of pregnancy screened for hyperglycemia, and such findings are directly relevant to clinical practice. Such risk factors are preventable, manageable, and even curable, and healthcare professionals should perform evidence-based treatment.

References

• ¹
  Irwin DE, Kopp ZS, Agatep B, Milsom I, Abrams P. Worldwide prevalence estimates of lower urinary tract symptoms, overactive bladder, urinary incontinence and bladder outlet obstruction. BJU Int. 2011;108(07):1132-1138. Doi: 10.1111/j.1464-410X.2010.09993.x [published Online First: 2011/01/15]
  » https://doi.org/10.1111/j.1464-410X.2010.09993.x
• ²
  Ekelund P, Grimby A, Milsom I. Urinary incontinence. Social and financial costs high. BMJ. 1993;306:1344. Doi: 10.1136/bmj.306.6888.1344 (6888): [published Online First: 1993/05/15]
  » https://doi.org/10.1136/bmj.306.6888.1344(6888)
• ³
  Markland AD, Richter HE, Fwu CW, Eggers P, Kusek JW. Prevalence and trends of urinary incontinence in adults in the United States, 2001 to 2008. J Urol. 2011;186(02):589-593. Doi: 10.1016/j. juro.2011.03.114 [published Online First: 2011/06/21]
  » https://doi.org/10.1016/j.juro.2011.03.114
• ⁴
  Amaro JL, Macharelli CA, Yamamoto H, Kawano PR, Padovani CV, Agostinho AD. Prevalence and risk factors for urinary and fecal incontinence in Brazilian women. Int Braz J Urol. 2009;35(05):592-597, discussion 598. Doi: 10.1590/s1677-55382009000500011 [published Online First: 2009/10/29]
  » https://doi.org/10.1590/s1677-55382009000500011
• ⁵
  Liang CC, Chang SD, Lin SJ, Lin YJ. Lower urinary tract symptoms in primiparous women before and during pregnancy. Arch Gynecol Obstet. 2012;285(05):1205-1210. Doi: 10.1007/s00404-011-2124-2 [published Online First: 2011/11/02]
  » https://doi.org/10.1007/s00404-011-2124-2
• ⁶
  Sangsawang B, Sangsawang N. Stress urinary incontinence in pregnant women: a review of prevalence, pathophysiology, and treatment. Int Urogynecol J Pelvic Floor Dysfunct. 2013;24(06): 901-912. Doi: 10.1007/s00192-013-2061-7 [published Online First: 2013/02/26]
  » https://doi.org/10.1007/s00192-013-2061-7
• ⁷
  Hvidman L, Hvidman L, Foldspang A, Mommsen S, Bugge Nielsen J. Correlates of urinary incontinence in pregnancy. Int Urogynecol J Pelvic Floor Dysfunct. 2002;13(05):278-283. Doi: 10.1007/s001920200061 [published Online First: 2002/10/02]
  » https://doi.org/10.1007/s001920200061
• ⁸
  Sangsawang B. Risk factors for the development of stress urinary incontinence during pregnancy in primigravidae: a review of the literature. Eur J Obstet Gynecol Reprod Biol. 2014;178:27-34. Doi: 10.1016/j.ejogrb.2014.04.010 [published Online First: 2014/05/03]
  » https://doi.org/10.1016/j.ejogrb.2014.04.010
• ⁹
  Chuang CM, Lin IF, Horng HC, Hsiao YH, Shyu IL, Chou P. The impact of gestational diabetes mellitus on postpartum urinary incontinence: a longitudinal cohort study on singleton pregnancies. BJOG. 2012;119(11):1334-1343. Doi: 10.1111/j.1471-0528.2012.03468.x [published Online First: 2012/08/21]
  » https://doi.org/10.1111/j.1471-0528.2012.03468.x
• ¹⁰
  Bellamy L, Casas JP, Hingorani AD, Williams D. Type 2 diabetes mellitus after gestational diabetes: a systematic review and meta-analysis. Lancet. 2009;373:1773-1779. Doi: 10.1016/S0140-6736 (09)60731-5 (9677): [published Online First: 2009/05/26]
  » https://doi.org/10.1016/S0140-6736(09)60731-5(9677)
• ¹¹
  Yun S, Kabeer NH, Zhu BP, Brownson RC. Modifiable risk factors for developing diabetes among women with previous gestational diabetes. Prev Chronic Dis. 2007;4(01):A07[published Online First: 2006/12/19]
• ¹²
  Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. 2010;303(03): 235-241. Doi: 10.1001/jama.2009.2014 [published Online First: 2010/01/15]
  » https://doi.org/10.1001/jama.2009.2014
• ¹³
  Heslehurst N, Ells LJ, Simpson H, Batterham A, Wilkinson J, Summerbell CD. Trends in maternal obesity incidence rates, demographic predictors, and health inequalities in 36,821 women over a 15-year period. BJOG. 2007;114(02):187-194. Doi: 10.1111/j.1471-0528.2006.01180.x [published Online First: 2007/02/20]
  » https://doi.org/10.1111/j.1471-0528.2006.01180.x
• ¹⁴
  Thangaratinam S, Rogozińska E, Jolly K, et al. Interventions to reduce or prevent obesity in pregnant women: a systematic review. Health Technol Assess. 2012;16(31):iii-iv, 1-191. Doi: 10.3310/hta16310 [published Online First: 2012/07/21]
  » https://doi.org/10.3310/hta16310
• ¹⁵
  Waetjen LE, Liao S, Johnson WO, et al. Factors associated with prevalent and incident urinary incontinence in a cohort of midlife women: a longitudinal analysis of data: study of women’s health across the nation. Am J Epidemiol. 2007;165(03):309-318. Doi: 10.1093/aje/kwk018 [published Online First: 2006/11/30]
  » https://doi.org/10.1093/aje/kwk018
• ¹⁶
  Catalano PM, Shankar K. Obesity and pregnancy: mechanisms of short term and long term adverse consequences for mother and child. BMJ. 2017;356:j1. Doi: 10.1136/bmj.j1 [published Online First: 20170208]
  » https://doi.org/10.1136/bmj.j1
• ¹⁷
  Doumouchtsis SK, Loganathan J, Pergialiotis V. The role of obesity on urinary incontinence and anal incontinence in women: a review. BJOG. 2022;129(01):162-170. Doi: 10.1111/1471-0528.16848 [published Online First: 20210914]
  » https://doi.org/10.1111/1471-0528.16848
• ¹⁸
  Nambiar AK, Arlandis S, Bø K, et al. European Association of Urology Guidelines on the Diagnosis and Management of Female Non-neurogenic Lower Urinary Tract Symptoms. Part 1: Diagnostics, Overactive Bladder, Stress Urinary Incontinence, and Mixed Urinary Incontinence. Eur Urol. 2022;82(01):49-59. Doi: 10.1016/j.eur-uro.2022.01.045 [published Online First: 2022/02/27]
  » https://doi.org/10.1016/j.eururo.2022.01.045
• ¹⁹
  Abrams P, Cardozo L, Wagg A, et al. 6th International Consultation on Incontinence 2017.
• ²⁰
  American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2014;37:S81-S90. Doi: 10.2337/dc14-S081 (Suppl 1): [published Online First: 2013/12/21]
  » https://doi.org/10.2337/dc14-S081
• ²¹
  Rudge MVC, Barbosa AMP, Sobrevia L, et al; Perinatal Diabetes Research Group. Altered maternal metabolism during mild gestational hyperglycemia as a predictor of adverse perinatal outcomes: A comprehensive analysis. Biochim Biophys Acta Mol Basis Dis. 2020;1866(02):165478. Doi: 10.1016/j.bbadis.2019.05.014 [published Online First: 2019/06/04]
  » https://doi.org/10.1016/j.bbadis.2019.05.014
• ²²
  Rudge MV, Calderon IM, Ramos MD, Abbade JF, Rugolo LM. Perinatal outcome of pregnancies complicated by diabetes and by maternal daily hyperglycemia not related to diabetes. A retrospective 10-year analysis. Gynecol Obstet Invest. 2000;50 (02):108-112. Doi: 10.1159/000010293 [published Online First: 2000/08/31]
  » https://doi.org/10.1159/000010293
• ²³
  WHO Consultation on Obesity. 1999: Geneva SWHO. Obesity: preventing and managing the global epidemic: report of a WHO consultation. World Health Organization 2000
• ²⁴
  Pereira VS, Santos JY, Correia GN, Driusso P. [Translation and validation into Portuguese of a questionnaire to evaluate the severity of urinary incontinence]. Rev Bras Ginecol Obstet. 2011; 33(04):182-187. Doi: 10.1590/s0100-72032011000400006 [published Online First: 2011/08/17]
  » https://doi.org/10.1590/s0100-72032011000400006
• ²⁵
  Sandvik H, Hunskaar S, Seim A, Hermstad R, Vanvik A, Bratt H. Validation ofa severity index in female urinary incontinence and its implementation in an epidemiological survey. J Epidemiol Community Health. 1993;47(06):497-499. Doi: 10.1136/jech.47.6.497 [published Online First: 1993/12/01]
  » https://doi.org/10.1136/jech.47.6.497
• ²⁶
  Tamanini JT, Dambros M, D’Ancona CA, Palma PC, Rodrigues Netto N Jr. [Validation of the “International Consultation on Incontinence Questionnaire - Short Form” (ICIQ-SF) for Portuguese]. Rev Saude Publica. 2004;38(03):438-444. Doi: 10.1590/s0034-89102004000300015 [published Online First: 2004/07/10]
  » https://doi.org/10.1590/s0034-89102004000300015
• ²⁷
  Haylen BT, de Ridder D, Freeman RM, et al; International Urogy-necological Association; International Continence Society. An International Urogynecological Association (IUGA)/International Continence Society (ICS) joint report on the terminology for female pelvic floor dysfunction. Neurourol Urodyn. 2010;29 (01):4-20. Doi: 10.1002/nau.20798 [published Online First: 2009/11/27]
  » https://doi.org/10.1002/nau.20798
• ²⁸
  Liang CC, Chao M, Chang SD, Chiu SY. Impact of prepregnancy body mass index on pregnancy outcomes, incidence of urinary incontinence and quality of life during pregnancy - An observational cohort study. Biomed J. 2020;43(06):476-483. Doi: 10.1016/j.bj.2019.11.001 [published Online First: 20201124]
  » https://doi.org/10.1016/j.bj.2019.11.001
• ²⁹
  Lao TT, Ho LF, Chan BC, Leung WC. Maternal age and prevalence of gestational diabetes mellitus. Diabetes Care. 2006;29(04): 948-949. Doi: 10.2337/diacare.29.04.06.dc05-2568 [published Online First: 2006/03/29]
  » https://doi.org/10.2337/diacare.29.04.06.dc05-2568
• ³⁰
  Casagrande SS, Linder B, Cowie CC. Prevalence of gestational diabetes and subsequent Type 2 diabetes among U.S. women. Diabetes Res Clin Pract. 2018;141:200-208. Doi: 10.1016/j.dia- bres.2018.05.010 [published Online First: 2018/05/18]
  » https://doi.org/10.1016/j.diabres.2018.05.010
• ³¹
  Sibai BM, Ross MG. Hypertension in gestational diabetes mellitus: pathophysiology and long-term consequences. J Matern Fetal Neonatal Med. 2010;23(03):229-233. Doi: 10.3109/1476705090355 0899 [published Online First: 2010/02/04]
  » https://doi.org/10.3109/14767050903550899
• ³²
  Dinç A Prevalence of Urinary Incontinence During Pregnancy and Associated Risk Factors. Low Urin Tract Symptoms. 2018;10(03): 303-307. Doi: 10.1111/luts.12182 [published Online First: 2017/07/05]
  » https://doi.org/10.1111/luts.12182
• ³³
  Daly D, Clarke M, Begley C. Urinary incontinence in nulliparous women before and during pregnancy: prevalence, incidence, type, and risk factors. Int Urogynecol J Pelvic Floor Dysfunct. 2018;29(03):353-362. Doi: 10.1007/s00192-018-3554-1 [published Online First: 2018/01/25]
  » https://doi.org/10.1007/s00192-018-3554-1
• ³⁴
  Brown SJ, Donath S, MacArthur C, McDonald EA, Krastev AH. Urinary incontinence in nulliparous women before and during pregnancy: prevalence, incidence, and associated risk factors. Int Urogynecol J Pelvic Floor Dysfunct. 2010;21(02):193-202. Doi: 10.1007/s00192-009-1011-x [published Online First: 2009/10/17]
  » https://doi.org/10.1007/s00192-009-1011-x
• ³⁵
  Viktrup L. The risk of lower urinary tract symptoms five years after the first delivery. Neurourol Urodyn. 2002;21(01):2-29. Doi: 10.1002/nau.2198 [published Online First: 2002/02/09]
  » https://doi.org/10.1002/nau.2198
• ³⁶
  Dolan LM, Walsh D, Hamilton S, Marshall K, Thompson K, Ashe RG. A study of quality of life in primigravidae with urinary incontinence. Int Urogynecol J Pelvic Floor Dysfunct. 2004;15(03): 160-164. Doi: 10.1007/s00192-004-1128-x [published Online First: 2004/05/29]
  » https://doi.org/10.1007/s00192-004-1128-x
• ³⁷
  van de Pol G, van Brummen HJ, Bruinse HW, Heintz AP, van der Vaart CH. Is there an association between depressive and urinary symptoms during and after pregnancy? Int Urogynecol J Pelvic Floor Dysfunct. 2007;18(12):1409-1415. Doi: 10.1007/s00192-007-0371-3 [published Online First: 2007/04/04]
  » https://doi.org/10.1007/s00192-007-0371-3
• ³⁸
  Piculo F, Marini G, Vesentini G, et al. Pregnancy-specific urinary incontinence in women with gestational hyperglycaemia worsens the occurrence and severity of urinary incontinence and quality of life over the first year post partum. Eur J Obstet Gynecol Reprod Biol. 2020;252:336-343. Doi: 10.1016/j.ejogrb.2020.06.036 [published Online First: 2020/07/14]
  » https://doi.org/10.1016/j.ejogrb.2020.06.036
• ³⁹
  Zhu L, Li L, Lang JH, Xu T. Prevalence and risk factors for peri- and postpartum urinary incontinence in primiparous women in China: a prospective longitudinal study. Int Urogynecol J Pelvic Floor Dysfunct. 2012;23(05):563-572. Doi: 10.1007/s00192-011-1640-8 [published Online First: 2012/01/27]
  » https://doi.org/10.1007/s00192-011-1640-8
• ⁴⁰
  Lamerton TJ, Torquati L, Brown WJ. Overweight and obesity as major, modifiable risk factors for urinary incontinence in young to mid-aged women: a systematic review and meta-analysis. Obes Rev. 2018;19(12):1735-1745. Doi: 10.1111/obr.12756 [published Online First: 2018/09/20]
  » https://doi.org/10.1111/obr.12756
• ⁴¹
  Danforth KN, Townsend MK, Lifford K, Curhan GC, Resnick NM, Grodstein F. Risk factors for urinary incontinence among middleaged women. Am J Obstet Gynecol. 2006;194(02):339-345. Doi: 10.1016/j.ajog.2005.07.051 [published Online First: 2006/02/07]
  » https://doi.org/10.1016/j.ajog.2005.07.051
• ⁴²
  Eltatawy HH, Eltatawy TM, Soliman MG, et al. The link between female obesity and urinary stress incontinence. Uro Today Int J. 2011;4(05):x
• ⁴³
  Noblett KL, Jensen JK, Ostergard DR. The relationship of body mass index to intra-abdominal pressure as measured by multichannel cystometry. Int Urogynecol J Pelvic Floor Dysfunct. 1997;8(06): 323-326. Doi: 10.1007/BF02765589 [published Online First: 1997/01/01]
  » https://doi.org/10.1007/BF02765589
• ⁴⁴
  Kim C, McEwen LN, Sarma AV, Piette JD, Herman WH. Stress urinary incontinence in women with a history of gestational diabetes mellitus. J Womens Health (Larchmt). 2008;17(05):783-792. Doi: 10.1089/jwh.2007.0616 [published Online First: 2008/06/10]
  » https://doi.org/10.1089/jwh.2007.0616
• ⁴⁵
  Barbosa AM, Dias A, Marini G, Calderon IM, Witkin S, Rudge MV. Urinary incontinence and vaginal squeeze pressure two years post-cesarean delivery in primiparous women with previous gestational diabetes mellitus. Clinics (São Paulo). 2011;66(08): 1341-1346. Doi: 10.1590/s1807-59322011000800006 [published Online First: 2011/09/15]
  » https://doi.org/10.1590/s1807-59322011000800006
• ⁴⁶
  Vesentini G, Barbosa AMP, Damasceno DC, et al; DIAMATER Study Group. Alterations in the structural characteristics of rectus abdominis muscles caused by diabetes and pregnancy: A comparative study of the rat model and women. PLoS One. 2020;15 (04):e0231096. Doi: 10.1371/journal.pone.0231096 [published Online First: 2020/04/04]
  » https://doi.org/10.1371/journal.pone.0231096
• ⁴⁷
  Vesentini G, Barbosa AMP, Floriano JF, et al; Diamater Study Group. Deleterious effects of gestational diabetes mellitus on the characteristics of the rectus abdominis muscle associated with pregnancy-specific urinary incontinence. Diabetes Res Clin Pract. 2020;166:108315. Doi: 10.1016/j.diabres.2020.108315 [published Online First: 2020/07/18]
  » https://doi.org/10.1016/j.diabres.2020.108315
• ⁴⁸
  Diaz D, Robinson D, Bosch R, et al. Patient-reported outcome assessment. In: Abrams P, Cardozo L, Wagg A, et al., eds. 6th International Consultation on Incontinence: ICI–ICS. International Continence Society, Bristol UK 2017:541-98.

Publication Dates

• Publication in this collection
  04 Aug 2023
• Date of issue
  2023

History

• Received
  15 Sept 2022
• Accepted
  17 Apr 2023