ORIGINAL PAPERS

orIginal papers
Adv Clin Exp Med 2013, 22, 4, 489–494
ISSN 1899–5276
© Copyright by Wroclaw Medical University
Hasan S. Sağlam1, A, C. Serkan Gökkaya2, B, Remzi Salar2, B, C, Ali Memiş2, E,
Öztuğ Adsan1, F
The Effects of Age, Metabolic Syndrome,
Nocturnal Polyuria and Sleep Disorders on Nocturia
Wpływ wieku, zespołu metabolicznego,
nocnego wielomoczu i zaburzeń snu na moczenie nocne
Sakarya University, Medical Faculty, Department of Urology, Sakarya, Turkey
Ankara Numune Education and Training Hospital, Department of Urology, Ankara, Turkey
1
2
A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation;
D – writing the article; E – critical revision of the article; F – final approval of article; G – other
Abstract
Background. Nocturia, which is especially frequent among older men, adversely affects the individual’s quality of
life. It is regarded as one of the most bothersome lower urinary tract symptoms (LUTS).
Objectives. The aim of the study was to investigate factors contributing to the frequency of nocturia.
Material and Methods. Men ≥ 40 years with LUTS were enrolled in this study. After medical histories were taken and
physical examinations conducted, biochemical tests and measures for LUTS were carried out. Anthropometric measurements were performed and Epworth scores (ES) were examined. Patients were divided into two groups with respect to
nocturia: the first group having no nocturia or one incident of nocturia per night, and the second group with two or more
nightly incidents of nocturia. The data were analyzed statistically; p < 0.05 was considered significant.
Results. A total of 118 consecutive patients (56 ± 10 years) were enrolled in the study. The first group consisted
of 31 participants, while the second group contained 87 patients. The groups differed significantly with respect to
age, body height, body weight, waist circumference and body mass index (BMI). ES, prostatic volumes, maximum
flow rates (Qmax) and international prostate symptom scores (IPSS) were significantly different. Fasting blood
glucose levels were similar for both groups. Homeostasis model assessment (HOMA) scores showed borderline
significance. Insulin levels were different, while insulin resistance (IR) was similar between the groups. Nocturnal
polyuria was associated with nocturia, systolic blood pressure and IPSS.
Conclusions. Age, nocturnal polyuria, metabolic syndrome and sleep disturbances have been shown to be contributing factors in the frequency of nocturia and LUTS. Therefore, steps taken to alleviate factors that can be altered
– such as hypertension, weight gain, sleep disturbances and IPSS – may improve the individual’s quality of life (Adv
Clin Exp Med 2013, 22, 4, 489–494).
Key words: benign prostatic hyperplasia, hypertension, insulin resistance, lower urinary tract symptoms, nocturia.
Streszczenie
Wprowadzenie. Nykturia, która występuje zwłaszcza wśród starszych mężczyzn, negatywnie wpływa na jakość życia
jednostki. Jest uznana za jeden z najbardziej uciążliwych objawów ze strony dolnych dróg moczowych (LUTS).
Cel pracy. Zbadanie czynników przyczyniających się do zwiększenia częstotliwości nykturii.
Materiał i metody. Mężczyzn w wieku ≥ 40 lat z LUTS zakwalifikowano do udziału w badaniu. Zebrano wywiad
medyczny i przeprowadzone badania fizyczne, następnie przeprowadzono testy biochemiczne i oceniono
LUTS. Wykonano pomiary antropometryczne i przyznano pacjentom punktację w skali Epworth (ES). Pacjentów
podzielono na 2 grupy w zależności od występowania nykturii: w pierwszej grupie nykturia nie występowała lub
wystąpił 1 incydent nykturii na dobę, a w drugiej grupie występowało ≥ 2 incydentów nykturii. Dane analizowano
statystycznie, p < 0,05 uznano za znaczące.
Wyniki. Łącznie 118 kolejnych chorych (56 ± 10 lat) uczestniczyło w badaniu. Pierwsza grupa składała się
z 31 uczestników, a druga grupa zawierała 87 pacjentów. Grupy różniły się istotnie pod względem wieku, wzro-
490
H. S. Sağlam et al.
stu, masy ciała, obwodu talii i wskaźnika masy ciała (BMI). ES, objętość prostaty, maksymalne natężenie przepływu (Qmax) i wyniki międzynarodowej skali punktowej objawów towarzyszących chorobom gruczołu krokowego
(IPSS) różniły się istotnie. Stężenie glukozy we krwi na czczo były podobne w obu grupach. Wyniki modelu oceny
homeostazy (HOMA) miały wątpliwe znaczenie. Stężenie insuliny było różne, a odporność na insulinę (IR) była
podobna w obu grupach. Nocny wielomocz był związany z nykturią, ciśnieniem skurczowym krwi i IPSS.
Wnioski. Wykazano, że wiek, nocny wielomocz, zespół metaboliczny i zaburzenia snu są czynnikami przyczyniającymi się do zwiększenia częstotliwości nykturii i LUTS. Dlatego działania podjęte w celu wpływu na czynniki
modyfikowalne – takie jak: nadciśnienie, przyrost masy ciała, zaburzenia snu i IPSS – mogą poprawić jakość życia
jednostki (Adv Clin Exp Med 2013, 22, 4, 489–494).
Słowa kluczowe: łagodny przerost gruczołu krokowego, nadciśnienie tętnicze, insulinooporność, objawy ze strony
dolnych dróg moczowych, moczenie nocne.
Nocturia, which is a symptom that adversely affects the quality of life, is especially frequent
in older men [1]. It is regarded as one of the most
bothersome lower urinary tract symptoms (LUTS),
which include frequency, urgency, nocturia, difficulty initiating urination, a sense of incomplete
bladder emptying, decreased force of the stream
and interruption of the stream [2].
It has been suggested that the most common
causes of LUTS are benign prostatic hyperplasia
(BPH) causing urethral obstruction, and conditions increasing the volume of urine, such as the
use of diuretics; but other conditions are also considered to contribute to LUTS: heart failure, diabetes mellitus (DM), sleep apnea syndrome, problems that reduce functional capacity, as well as
some nutrients [2–4].
Nocturia is problematic not only because it
awakens the patient to void, but also because it is
a significant cause of falls and fractures, fatigue,
depression, obesity, coronary heart disease and
sudden death, especially for elderly men who have
difficulty walking [5].
The aim of this study was to investigate the
roles of age, metabolic syndrome, nocturnal polyuria and sleep disorders in patients with lower urinary symptoms.
Material and Methods
This study has been conducted in accordance
with good clinical practice as defined by the Helsinki Declaration of the World Medical Association
(Seul 2008). After approval was obtained from the
local ethics committee, the participants were enrolled in the study, providing written consent. The
patients were consecutive male patients ≥ 40 years
old with LUTS. Those with a history of urogenital
trauma, urethral catheterization or urethritis were
excluded from the study, as were those with overactive bladder, neurogenic deficit, low bladder capacity or urinary tract infection. In addition, those
with kidney failure, polyuria due to external causes
and those taking drugs causing diuresis were also
excluded. Comorbidities and the drugs patients
were taking were asked about and recorded. The
patients were asked to measure their blood pressure daily for a week and record the findings. Patients were also asked to record voiding, fluid intake and sleep patterns for three days. The mean
values from these blood pressure and voiding diary records were calculated and used in this study.
Nighttime urine output of more than 33% of the
total daily urine volume was considered to be nocturnal polyuria.
The patients’ body height, body weight, waist
circumference and hip circumference were measured. BMI was calculated as the body weight in
kilograms divided by the square of the height in
meters (kg/m2). Prostatic volume was measured by
transrectal ultrasonography. Urine flow rate and
suprapubic residual urine volume were measured
and recorded. In addition to prostate specific antigen (PSA) and routine biochemical tests, lipid profiles, fasting insulin level and urine spot natrium
levels were determined. The patients’ international
prostate symptom scores (IPSSs) were examined.
BPH was considered when an individual’s prostatic volume was ≥ 25 cc and IPSS was ≥ 8.
Insulin resistance (IR) was assessed via the
homeostatic model assessment (HOMA) method by calculating the fasting insulin level (µIU/ml)
× fasting blood sugar (mmol/L)/22.5; a HOMA
score ≥ 2.5 was considered IR. Epworth scores
(ES) were used to measure sleep disturbances. An
ES ≤10 was considered normal; an ES between
11–17 and ≥ 18 were considered to be moderate
and serious sleep disturbances, respectively.
The patients were divided into two groups according to nocturia frequency, with the first group
having one or no incidents of nocturia per night,
and the second having two or more nightly incidents of nocturia. The values obtained from the
patients were compared using the Student’s T test,
Mann-Whitney U test and Spearman’s rho test. For
Spearman correlations, rs values between 0.10–0.24
were considered very weak, 0.25–0.49 were designated weak to moderate, 0.50–0.74 were strong
and 0.75–1.00 very strong.
491
Factors Contributing to Nocturia
P < 0.05 was considered significant. The statistical analysis was carried out using SPSS 20.0 software (SPSS Inc., Chicago, USA).
Results
A total of 118 patients with a mean age of
56 ± 9 years were enrolled in the study. The first
group consisted of 31 participants, while the second group included 87 patients. The groups
were different in respect to age (52 ± 9 years vs.
57 ± 9 years, P = 0.025). Body height, body weight
and waist circumference measures were also significantly different (P = 0.048, 0.003 and 0.045 respectively – see Table 1).
BMIs were significantly different for the two
groups (P = 0.030). The two groups’ systolic and
diastolic blood pressure were similar (P>0.05).
The ESs of the groups were different (P = 0.005).
Prostatic volumes, maximum flow rates (Qmax)
and IPSS scores were significantly different
(P = 0.044, 0.003 and 0.001 respectively). Postvoiding residual urine volumes were similar in
the two groups.
Fasting blood glucose levels were similar in
the two groups, and HOMA scores were borderline significant (P = 0.051). Insulin levels were different (P = 0.042), while IR was similar in the two
groups. No difference was observed between the
groups with respect to lipid profile, PSA and urine
spot natrium levels.
In all patients, a moderate and significant
(rs = 0.46, P = 0.001) association between age and
prostate volume was observed. A weak but significant (rs = 0.323, P = 0.004) association between
age and ES was detected. In the first group, three
cases (10%) of nocturnal polyuria were found,
while 39 cases (45%) were found in the second
group (P = 0.001). Nocturnal polyuria was associated strongly with nocturia (rs = 0.510, P = 0.001),
weakly with systolic blood pressure (rs = 0.380,
Table 1. Basic demographic features of the patients
Tabela 1. Podstawowe cechy demograficzne pacjentów
Demographic features
(Cechy demograficzne)
Nocturia
≤ 1
(n = 31)
Nocturia
≥ 2
(n = 87)
p
Age (years)
52 ± 9
57 ± 9
0.025
Height (cm)
173 ± 10
170 ± 6
0.048
Waist circumference
(cm)
100 ±12
105 ± 12
0.045
Weight (kg)
79 ±16
91 ±14
0.003
Table 2. The patients’ basic results
Tabela 2. Podstawowe wyniki pacjentów
Basic parameters
(Podstawowe
wskaźniki)
Nocturia
≤ 1
(n = 31)
Nocturia
≥ 2
(n = 87)
p
Qmax (ml/s)
20 ±4
14 ± 8
0.003
IPSS
5 ± 9
17 ± 9
0.000
Epworth score
7 ± 6
11 ± 6
0.005
Prostate volume
(cm3)
23 ± 16
28 ± 16
0.440
BMI (kg/m2)
28 ± 4
30 ± 4
0.030
Fasting insulin
(µIU/ml)
7.2 ± 8
1.2 ± 8
0.043
Fasting blood
sugar (mg/dl)
105 ± 39
110 ± 39
0.510
HOMA score
1.9 ± 3.08
2.7 ± 3.08
0.498
Systolic BP
(mmHg)
120 ± 19
135 ± 19
0.137
24-urine volume
(ml)
1590 ± 151
1657 ± 151
0.001
Nocturnal urine
volume (ml)
460 ± 73
545 ±73
0.001
Nocturnal
polyuria (n)
3 (%10)
39 (% 44)
0.001
Qmax – maximum flow rate.
BMI – Body mass index.
HOMA – homeostatic model assessment.
IPSS – International prostate symptom score.
BP – Blood pressure.
Qmax – maksymalne natężenie przepływu.
BMI – wskaźnik masy ciała.
HOMA – model oceny homeostazy.
IPSS – objawy towarzyszące chorobom gruczołu krokowego.
BP – ciśnienie krwi.
P = 0.006) and strongly with IPSS (rs = 0.505,
P = 0.001) as indicated in Table 2.
Discussion
Nocturia, a multifactorial symptom, is one of
the irritative lower urinary system symptoms and
one of the most disturbing [4, 5]. In patients over
50 years of age, BPH has been suggested as the
most frequent etiologic factor. The majority of patients with LUTS have BPH, and the majority of
patients with BPH have LUTS. Therefore these two
terms are often used interchangeably [2, 6].
While it has multiple definitions, metabolic
syndrome generally denotes a number of factors
492
including obesity, dyslipidemia, hypertension and
IR; among the consequences of these factors are insulin and glucose metabolic disturbances [2, 6–12].
Different authors have different views about the
number of the aforementioned factors that are required for a diagnosis of metabolic syndrome [11].
The present study has found an association
between nocturia and large waist circumference,
which represents central obesity. Other studies
suggest that obesity may cause a rise in LUTS by
increasing insulin levels, which activates the sympathetic nervous system [13, 14].
In addition, the patients’ heights and weights
were both found to be associated with the frequency of nocturia, and BMIs obtained from these data
were significantly different between the two groups
in the study. Rohrman did not observe any association between BMI and LUTS, but stated that increases in waist circumference might positively
influence LUTS via sympathetic nervous system
activation through increased insulin levels [15].
In the present study, no significant association
was observed between nocturia and hypertension.
Systolic and diastolic blood pressure measures
were similar in the two groups. Neither additional drug administration nor disease (e.g., diabetes
mellitus) had a significant bearing on nocturia.
Kim reported that hypertension is a risk factor for
vascular diseases, and men with risk factors for vascular diseases were more likely to have LUTS than
men without vascular risk factors [13]. Rohrman
found higher odds (odds ratio 1.76) for LUTS in
men with a history of hypertension [16]. It has
been stated that factors activating the sympathetic nervous system increase LUTS; in this context,
many factors, including DM, IR and hypertension,
have been suggested as causing LUTS in the same
way [13, 14, 17]. In this study, it was observed that
hypertension was weakly associated with nocturnal polyuria but did not affect nocturnal frequency. While some authors have reported significant
positive associations between hypertension and
LUTS, others have proposed that no association
existed between hypertension and LUTS [18–20].
It has been suggested that in BPH patients with
DM, prostatic volumes are larger, and sometimes
these two diseases might be superimposed due to
diabetic cystopathy, so that differentiating between
the two might be impossible for diagnostic purposes [7, 8]. However, the authors of the present study
did not find any significant positive association between BPH and DM in terms of prostatic volume.
In this study, a significant association was observed between high fasting insulin levels and nocturia, but the HOMA score was borderline. IR
was similar in both groups. Hammarsten has suggested that an elevated fasting insulin level was
H. S. Sağlam et al.
a consequence of IR, which is assumed in metabolic
syndrome, and with lipid metabolism disturbances
it is considered a risk factor for BPH. Therefore, he
proposed that high fasting insulin levels along with
other factors of metabolic syndrome might have an
effect on prostatic volume [21]. The current study
showed only an association between prostatic volume and age, but no association with other factors,
including insulin level or insulin metabolism.
It has also been stated that when BMI and
waist circumference indicate obesity, which is suggested as a cause of larger prostatic volume, these
were often taken as risk factors for prostatic surgery [2, 6, 17]. Lee et al. stated that a waist circumference indicating central obesity might influence
prostatic volume, whereas a BMI representing
overall obesity might not [22]. On the other hand,
Kim et al. stated that obesity was not associated
with LUTS [14]. In this study, BMI, waist circumference, DM and lipid profile were not found to
correlate with prostatic volume.
Nocturia has been reported to cause some
problems, including an increased risk of nighttime falls, fatigue due to awakening during the
night, decreased work efficiency and even traffic
accidents [9]. In the current study, patients with
one or no incidents of nocturia had significantly
fewer sleep disturbances than patients with two or
more. Nevertheless, as stated by Yoo et al., the degree of sleep disturbance might be more than what
the study determined, because some people mask
or omit their sleep problems [9].
The International Continence Society has defined nocturia as the individual waking in the
night with the desire to void [23]. Two types of
nocturia have been identified: true nocturia and
pseudonocturia. In true nocturia, a need for micturation awakens the patient, while in pseudonocturia, the patient awakens due to other causes and
then goes to void [9]. It has been reported that one
of the most important causes of true nocturia is
obstructive sleep apnea, a condition in which intra-thoracic negative pressure leads to partial or
full airway obstruction. In this condition, respiration efforts cause the heart to receive an erroneous overload signal. The consequence of these
events is an increase in atrial natriuretic factor and
in nocturnal urine output, which is called nocturnal polyuria if it is ≥ 33% of the daily urine volume [24–26]. High levels of urine production have
been found to be one of the major cause of nocturia, and a reduction in anti-diuretic hormone secretion seems to be the most important factor in
nocturnal polyuria. The two conditions – nocturia and sleep disturbance – seem to be connected reciprocally [26]. In the current study, a strong
and significant association was observed between
Factors Contributing to Nocturia
nocturnal polyuria and nocturnal frequency. Similarly, an association between nocturnal polyuria
and IPSS was noted, and this association was considered in relation to nocturnal frequency. In the
current study, nocturnal polyuria did not inevitably cause an increase in nocturnal frequency in all
patients; in some patients with nocturnal polyuria,
nocturnal frequency did not increase, as Furtado
concluded [24].
Although weak, an association between ES
and nocturnal polyuria has been established; it has
therefore been suggested that sleep disturbances
might influence nocturnal frequency due to nocturnal polyuria. Kaynak et al. concluded in their
study that a nocturnal voiding frequency of more
than three times is common in severe obstructive
sleep apnea syndrome (OSAS), and that clinicians
should have a high degree of suspicion of severe
493
OSAS in subjects who complain of more than
three nightly incidents of nocturia [27]. Although
nocturia is defined as a complaint that the individual wakes up one or more times to void, it has been
suggested that it has more impact in terms of daily consequences when it occurs two or more times
per night [1, 5, 23, 24]. In this study it has also been
shown that the patients perceive nocturia as more
inconvenient when the nocturnal voiding frequency is two or more times.
In conclusion, age, nocturnal polyuria, metabolic syndrome and sleep disturbances have been
determined to be important factors in the frequency of nocturia and consequently in LUTS. Therefore, steps taken to alleviate factors that can be altered – such as hypertension, weight gain, sleep
disturbances and IPSS – may improve the individual’s quality of life.
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Address for correspondence:
Hasan S. Sağlam
Kemalpaşa mah, 132 sokak
Seyirtepe sitesi, no 3
Serdivan
Sakarya, 54100
Turkey
Tel.: +90 532 417 88 41
E-mail: [email protected]
Conflict of interest: None declared
Received: 18.07.2011
Revised: 27.09.2012
Accepted: 12.08.2013