Received: 8 May 2019 | Accepted: 10 June 2019

DOI: 10.1002/nau.24086

ORIGINAL CLINICAL ARTICLE

Association of diabetic retinopathy stage with the severity

of female urinary incontinence

Veysel Cankurtaran MD1 | Serdar Ozates MD2 | Serkan Ozler MD3 |

4
Emre Dirican MD

1
Department of Ophthalmology, Medical
School of Mustafa Kemal University,
Antakya, Hatay, Turkey
2
Department of Ophthalmology, Kars
Harakani State Hospital, Kars, Turkey
3
Department of Urology, Medical School
of Mustafa Kemal University, Antakya,
Hatay, Turkey
4
Department of Biostatistics, Medical
School of Mustafa Kemal University,
Antakya, Hatay, Turkey
Correspondence
Serdar Ozates, Yenişehir Mahallesi, İsmail
Aytemiz Blv. No. 55, 36200 Merkez, Kars,
Turkey.
Email: serdarozates@gmail.com
Abstract
Purpose: To assess the relation between diabetic retinopathy (DR) severity and
urinary incontinence (UI) in patients with diabetes mellitus (DM).
Materials and methods: This prospective and observational study included
153 subjects. Patients were divided into three subgroups, according to severity of
DR, as: No‐DR, nonproliferative DR (NPDR), and proliferative DR (PDR); 40
age‐matched healthy subjects formed the control group. Turkish version of the
Urogenital Stress Inventory 6 (UDI‐6) and Incontinence Impact Questionnaire
(IIQ‐7) were used to assess the UI symptoms and their effect on quality of life.
The UDI‐6 and IIQ‐7 scores were the primary outcomes of the study.
Results: No significant difference was observed between groups regarding age,
maternal parity, body mass index, type of delivery, menopausal status, and
smoking. The mean UDI‐6 urgency UI questions score was significantly higher
in the PDR group and significantly higher in the NPDR group than in the
control group. The mean UDI‐6 stress UI questions score was similar between
groups. The mean UDI‐6 voiding difficulty questions score was significantly
higher in the PDR group and no significant difference was observed between
other groups. The mean IIQ‐7 score was significantly lower in the PDR group. A
moderate and positive correlation was found between glycated hemoglobin level
and the UDI‐6 urgency UI and voiding difficulty questions and total scores. A
weak and positive correlation was found between the duration of DM and the
all UDI‐6 scores.
Conclusion: The present study showed that UI symptoms and their effect on
QOL were more severe in patients with PDR.

KEYWORDS
diabetic retinopathy, quality of life, urinary incontinence

1 | INTRODUCTION obesity, neurologic disorder, and chronic diseases such

Urinary incontinence (UI) is defined as the complaint of
involuntary leakage of urine.1 UI is a common disorder
and female UI prevalence increases with age, constipa-
tion, pelvic surgery, number of children delivered,
Neurourology and Urodynamics. 2019;38:1883-1888.
as diabetes mellitus (DM).2-4 UI also restricts social
functionality and disrupts psychological well‐being,
causing decrease in quality of life (QOL).2,4,5
DM is a worldwide systemic disorder that cause
multisystemic damages and increases mortality and
wileyonlinelibrary.com/journal/nau © 2019 Wiley Periodicals, Inc. | 1883
1884 | CANKURTARAN
morbidity.6 Increasing evidence has shown that DM is an
independent risk factor for female UI.3,7,8 Similar
pathophysiological processes were involved in both UI
and diabetic retinopathy (DR) in patients with DM.3,7 In
the literature, several studies have investigated the
relation between microvascular complications of DM
and female UI and its psychological aspects; however, no
study has investigated the relation between the severity of
DR and female UI.3,7,8 We hypothesise that the severity of
DR is associated with the severity of UI in women. The
present study sought to investigate the relation between
the severity of DR and the severity of female UI.
2 | MATERIALS AND MET HODS
This prospective and observational study was conducted at
the ophthalmology department of a tertiary referral hospital
in accordance with the ethical standards of the Declaration
of Helsinki. The study protocol was approved by the
institutional board of our hospital’s ethics committee. All
included patients granted written informed consent before
inclusion to the study.
Patients with type 2 DM and age‐matched healthy
subjects were included in the study. Patients with history
of cardiovascular diseases, unregulated hypertension,
history of perineal or vaginal surgery, history of traumatic
delivery, treatment for UI, history of anticholinergic drug
use, and systemic diseases that affect the central or
peripheral nervous system and genitourinary system,
except DM, were excluded.
A complete physical examination was performed, and all
the findings and previous medical history were noted for
each subject. Maternal parity, delivery type, menopausal
status, history of smoking, and education status were noted.
UI defined according to standardization of terminology in
lower urinary tract function.1,9 All patients were examined
and UI was diagnosed by a urologist. UI was diagnosed
based on the medical history, three‐day voiding diary,
physical examination including perineum examination and
cough‐stress test, and incontinence questionnaire. Patients
with UI symptoms associated with cough or sneezing,
positive cough‐stress test, and small‐volume urine leakage
in voiding diary diagnosed as stress UI. Patients with
urgency symptoms, nocturia, negative cough‐stress test, and
variable‐volume urine loss diagnosed as urgency UI. The
Urogenital Stress Inventory 6 (UDI‐6) and Incontinence
Impact Questionnaire (IIQ‐7) scores were the primary
outcomes of the study. The UDI‐6 and IIQ‐7 evaluated the
severity of UI symptoms and impact of UI on quality of life,
respectively.10 Symptom distress and the impact on daily
life of UI were assessed based on the Turkish version of the
UDI‐6 and IIQ‐7 scores.11 The first and second questions of
ET AL.
the UDI‐6 evaluate the urgency UI symptoms, the third and
fourth questions evaluate the stress UI symptoms, and the
fifth and sixth questions evaluate the voiding difficulty
symptoms.11 All subjects completed the Turkish version of
the UDI‐6 and IIQ‐7 without any assistance. Cronbach’s α
reliability coefficient of the Turkish version of the UDI‐6
and IIQ‐7 were .87 and .74, respectively.11 Test‐retest
reliability of the Turkish version of the UDI‐6 and IIQ‐7
were 0.99 for both scales.11 Responses to each question of
the UDI‐6 and IIQ‐7 were assigned a value that ranged
between 0 and 3.11 Total scores of the UDI‐6 and IIQ‐7 were
transformed to a range between 0 and 100.11 Higher scores
of UDI‐6 and IIQ‐7 indicated more severe UI symptoms and
decreased QOL, respectively. Type 2 DM diagnosis was
confirmed by the Endocrinology Department of our
hospital. Glycated hemoglobin (HbA1c) level and duration
of DM was noted. Body mass index (BMI) was calculated as
body weight (in kilograms) divided by the square of the
person’s height (in centimeters). Duration of DM and
HbA1c level were the secondary outcomes of the study.
Ophthalmological examination of all patients was per-
formed by the same clinician. All patients underwent a
complete ophthalmological examination, including cor-
rected distance visual acuity testing with Snellen chart,
noncontact tonometry, and slit‐lamp biomicroscopy of
anterior segment and fundus. DR stage was classified based
on the Early Treatment of Diabetic Retinopathy Study
criteria using the findings of fundus examination, fundus
florescein angiography, and optical coherence tomogra-
phy.12 Patients with type 2 DM were divided into three
subgroups based on the severity of DR. Patients with DM
and no DR comprised the No‐DR group; patients with
nonproliferative DR (NPDR) comprised the NPDR group;
and patients with proliferative DR (PDR) comprised the
PDR group. Age‐matched healthy subjects comprised the
control group.
A priori statistical power analysis using G*Power
software (version 3.0.10; Franz Faul, Universität Kiel,
Germany) revealed that a sample size of 32 participants
in each group would be sufficient to attain a power of
90% with an effect size of 0.340 and an α of .05.
Statistical Package for the Social Science (SPSS Version
22.0; IBM Corp, Armonk, NY) software were used to
analyze the study outcomes. The normal distribution
assumption of the data was tested by the Shapiro‐Wilk
test. Differences in categorical data between groups
were tested using the χ 2 test. Differences in the
outcomes between the groups were tested with one‐
way analysis of variance and the Kruskal‐Wallis test.
Post‐hoc analysis was performed for subgroup analysis.
The Spearman rank‐order correlation was used for
correlation analysis. A level of P < .05 was assumed
statistically significant for all tests.
CANKURTARAN ET AL. | 1885

the NPDR group, and 37 were included in the PDR

FIGURE 1 Enrollment flow‐chart of the study
3 | RESULTS
Figure 1 shows enrollment flow‐chart of the present
study. Of the 153 subjects enrolled, 40 were included in
the control group and 113 were included in the study
group. Of the 113 patients with DM in the study group, 35
were included in the No‐DR group, 41 were included in
group. Table 1 presents the demographic data and
clinical characteristics of the groups. No significant
difference was observed between groups regarding age,
maternal parity, type of delivery, BMI, menopausal
status, educational status, and smoking.
Table 2 shows the mean values and standard
deviations for the primary outcomes and comparison
between the groups. Table 3 presents the subgroup
analysis of mean UDI‐6 urgency UI questions score. The
mean UDI‐6 urgency UI questions score was significantly
higher in the PDR group than in the other groups and
significantly higher in the NPDR group than in the
control group. No significant difference was observed
between other groups regarding mean UDI‐6 urgency UI
questions score. The mean UDI‐6 stress UI questions
score was similar between groups. Table 3 shows the
subgroup analysis of mean UDI‐6 voiding difficulty
questions score. The mean UDI‐6 voiding difficulty
questions score was significantly higher in the PDR
group than in the other groups and no significant
difference was observed between other groups. Table 3
shows the subgroup analysis of mean UDI‐6 total score.
The mean UDI‐6 total score was significantly higher in
the PDR group than in the other groups and significantly
higher in the NPDR group than in the control group. No

T A B L E 1 Demographic data and clinical characteristics of the groups

Control group No‐DR group NPDR group PDR group

(n = 40) (n = 35) (n = 41) (n = 37) P value
Age (min‐max), y 56.9 ± 8.8 (41‐72) 57.8±8.2 (42‐71) 58.4±6.6 (40‐71) 57.9±6.8 (42‐70) .841*
Parity (min‐max), n 3.3 ± 1.6 (1‐7) 3.7 ± 1.9 (1‐8) 3.9 ± 2.5 (1‐11) 4.2 ± 1.9 (1‐10) .179**
Body mass index (min‐max) 30.1 ± 4.2 (23.1‐46.8) 31.3 ± 4.7 (21.7‐42.9) 30.5 ± 4.8 (21.4‐52.1) 30.8 ± 5.1 (22.2‐40.9) .551**
HbA1c (min‐max), % 5.2±0.2 (5.0‐5.6) 7.5±1.5 (5.5‐11.1) 8.8±1.8 (5.6‐14.0) 9.2±1.8 (5.6‐13.1) .001*
Duration of DM (min‐max), y ⋯ 10.1 ± 5.0 (3‐20) 15.0 ± 4.6 (5‐25) 18.8 ± 5.4 (9‐33) .001*
Smokers/Nonsmokers (n/n) 10/30 6/29 7/34 9/28 .722***
Type of delivery, n/n .990****
Vaginal/Cesarean 36/4 32/3 37/4 34/3
Menopausal status, n/n 34/6 30/5 36/5 33/4 .946***
Education level, n .937****
Nonliterate 4 3 4 4
Primary education 13 13 14 15
High school 17 13 20 14
University 6 6 3 3
Note: Bold text indicates statistical significance.
Abbreviations: DM, diabetes mellitus; DR, diabetic retinopathy; HbA1c, glycated hemoglobin; NPDR, nonproliferative diabetic retinopathy; PDR, proliferative
diabetic retinopathy.
*
One‐way analysis of variance.
**
The Kruskal‐Wallis test.
***
ThePearson χ 2 test.
****
Likelihood ratio.
1886 | CANKURTARAN ET AL.

T A B L E 2 Outcomes of the urogenital stress inventory and incontinence impact questionnaire

Control group No‐DR group NPDR group PDR group

(n = 40) (n = 35) (n = 41) (n = 37) P value*
UDI‐6 score
Urgency UI questions 16.7 ± 20.7 32.4 ± 28.6 37.4 ± 32.4 64.9 ± 33.3 .001
Stress UI questions 16.7 ± 18.5 15.2 ± 16.8 15.9 ± 17.0 31.9 ± 32.9 .105
Voiding difficulty 7.1 ± 14.1 5.7 ± 12.7 8.1 ± 14.5 24.3 ± 22.4 .001
questions
Total 12.5 ± 13.7 18.0 ± 14.8 20.6 ± 16.7 40.1 ± 21.3 .001
IIQ‐7 score 6.6 ± 13.7 8.0 ± 10.1 10.8 ± 16.3 28.7 ± 26.8 .001
Note: Bold text indicates statistical significance.
Abbreviations: DR, diabetic retinopathy; IIQ‐7, Incontinence Impact Questionnaire; NPDR, nonproliferative diabetic retinopathy, PDR, proliferative diabetic
retinopathy; UDI‐6, Urogenital Stress Inventory; UI, Urinary incontinence.
*
The Kruskal‐Wallis test.

T A B L E 3 Subgroup analysis of Urogenital Stress Inventory outcomes

No‐DR group NPDR group PDR group

Urgency UI questions 0.017 0.002 0.001 Control group
⋯ 0.607 0.001 No‐DR group
⋯ ⋯ 0.001 NPDR group
Voiding difficulty questions 0.747 0.600 0.001 Control group
⋯ 0.392 0.001 No‐DR group
⋯ ⋯ 0.001 NPDR group
Total score 0.061 0.007 0.001 Control group
⋯ 0.56 0.001 No‐DR group
⋯ ⋯ 0.001 NPDR group
Note: Bold text indicates statistical significance.
Abbreviations: DR, diabetic retinopathy, NPDR, nonproliferative diabetic retinopathy, PDR, proliferative diabetic retinopathy; UI, Urinary incontinence.

significant difference was observed between other groups
regarding mean UDI‐6 total score. The mean IIQ‐7 score
was significantly higher in the PDR group than in the
other groups (P < .001) and no significant difference was
observed between other groups (P > .05 for all).
The mean values and standard deviations for the
secondary outcomes are presented in Table 1. The
mean duration of DM was significantly different in
each study group and the highest in the PDR group and
the lowest in the No‐DR group (P < .001 for all). The
mean HbA1c level did not differ between the PDR and
NPDR groups (P = .916), was significantly higher in the
NPDR group than No‐DR group, was significantly
higher in the No‐DR group than in the control group
(P < .001 for all). Table 4 presents correlation analysis
between the UDI‐6 scores and HbA1c levels and DM
duration. A moderate and positive correlation was
found between HbA1c level and the UDI‐6 urgency UI
questions, voiding difficulty questions, and total scores.
A weak and positive correlation was found between the
duration of DM and the all UDI‐6 scores.
4 | DISCUSSION
Female UI remains a frequent disorder that disrupts the
patient’s well‐being. Female UI has several confounding
factors, such as middle‐age, obesity, race, parity, vaginal
delivery, pelvic or perineal surgery, smoking, respiratory
diseases, menopause, and systemic diseases.13-15 Previous
reports have noted DM as a risk factor for female UI.3,7
Jackson et al8 reported that DR was independently
associated with severe female UI and suggested that the
presence of DR may indicate the severity of female UI. In
the present study, we tested the hypothesis that the
severity of DR is associated with the severity of female UI
and found that female UI symptoms were more severe
and QOL was worse in patients with PDR.
CANKURTARAN ET AL.
T A B L E 4 Correlation analysis between the Urogenital Stress Inventory scores and glycated hemoglobin levels and diabetes mellitus
duration
Urgency UI questions
HbA1C, %
Correlation coefficient 0.40
P value* .01
Duration of DM, y
Correlation coefficient 0.21
P value* .03
Note: Bold text indicates statistical significance.
Abbreviations: DR, diabetic retinopathy; DM, diabetes mellitus; HbA1c, glycated hemoglobin; NPDR, nonproliferative diabetic retinopathy, PDR, proliferative
diabetic retinopathy; UI, urinary incontinence.
*
Spearman rank correlations analysis
Urgency UI symptoms were more severe in patients
with any retinal microvascular changes than control
subjects and the severity of urgency UI symptoms
increase as the DR progresses to more advanced stages.
The effect of DM on female UI is attributed to
microvascular complications.16 Brown et al3 reported
increased risk of female UI in patient with microvascular
complications and categorized UI as a microvascular
complication. Consistently, Danforth et al17 suggested
that microvascular changes in bladder and pelvic floor
muscles increased the risk of urgency UI. Yamaguchi
et al18 noted that diabetic cerebral vascular changes are
also associated with detrusor overactivity, which is an
underlying factor of urgency UI. Daneshgari et al19
suggested that diabetic bladder dysfunction was asso-
ciated with the progression of DM. Consistently, our
study results indicated increasing urgency UI symptoms
as DR progresses and, to our knowledge, progressing DR
may be a direct indicator of the damage in structures
involved in UI. DR progression is also associated with
uncontrolled DM and higher HbA1c levels were asso-
ciated with increased urgency UI symptoms in our study.
Diuresis related to hyperglycemia increases the risk of
urgency UI and triggers the initial pathologic changes in
bladder.17,19
In our study, stress UI symptoms did not differ
between groups and, in the literature, conflicting results
have been reported in this regard. Brown et al3 and
Lawrence et al20 reported that stress UI was more
frequent among patients with DM. Consistent with our
results, Danforth et al17 and McGrother et al21 noted no
association between DM and stress UI. DM is associated
with obesity and higher BMI was an important con-
founding factor for stress UI.21 To our knowledge, effect
of BMI should be controlled while evaluating the effect of
DM and DR on stress UI to perform reliable and
repeatable observations.
| 1887
Stress UI questions Voiding difficulty questions Total score
0.61 0.19 0.36
.45 .02 .01
0.25 0.18 0.28
.008 .006 .03
In the present study, voiding difficulty symptoms
were more severe in patients with PDR. Consistently,
Yu et al22 reported that voiding difficulty was more
frequent in patients with DM than in those without
DM. DM impairs detrusor innervation and contrac-
tility, and impaired detrusor functions cause voiding
difficulty and increased residual urine in bladder.23
Previous studies have shown that UI did not become
symptomatic until the advanced stages of DM as this
was also shown by our study.22,23
Female UI causes significant physical restriction and
has psychological and economic consequences as well.24
Recent evidence has revealed a significant association
between female UI and QOL.25,26 Our study showed that
female UI had a negative effect on QOL, and its effect on
QOL was significant in patients with PDR. Our findings
also indicated that DM‐associated UI may have an
insidious course and did not affect the QOL until
advanced retinal microvascular complications are appar-
ent. Most of the patients with female UI do not seek
treatment, or hesitate to visit a urologist, and do not
mention UI unless especially questioned.27 Ophthalmol-
ogists do not perform a urological examination in their
routine; however, our study results may encourage
ophthalmologists to inquire about UI in patients with
DR, which will ease identifying the patients with UI, help
patients to reach treatment for UI, and improve their
QOL.
There are several limitations to the present study.
We evaluated the severity of UI symptoms by a
screening test. Severity of UI symptoms should be
evaluated with more objective methods, such as pad
testing, in further studies. We also did not categorized
patients in the NPDR group according to the retinal
findings. Further studies with retinal finding‐based
categorizing of NPDR may provide more data regarding
the association of DR and female UI.
1888 | CANKURTARAN ET AL.

5 | C ON C LU S I O N S 13. Danforth KN, Townsend MK, Lifford K, Curhan GC, Resnick

NM, Grodstein F. Risk factors for urinary incontinence among
In conclusion, the present study showed that UI symptoms middle‐aged women. Am J Obstet Gynecol. 2006;194:339‐345.
14. Zhu L, Lang J, Liu C, Han S, Huang J, Li X. The
and their effect on QOL were more severe in patients with
epidemiological study of women with urinary incontinence
PDR. These results indicate the importance of retinal
and risk factors for stress urinary incontinence in China.
microvascular changes over envisaging the severity of UI. Menopause. 2009;16:831‐836.
15. Luber KM. The definition, prevalence, and risk factors for
stress urinary incontinence. Rev Urol. 2004;6(suppl 3):3‐9.
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Serdar Ozates http://orcid.org/0000-0002-0365-8786 diabetes on female voiding behavior. J Urol. 2004;172:989‐992.
17. Danforth KN, Townsend MK, Curhan GC, Resnick NM,
Grodstein F. Type 2 diabetes mellitus and risk of stress, urge
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