European Journal of Internal Medicine 24 (2013) 273277

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European Journal of Internal Medicine

journal homepage: www.elsevier.com/locate/ejim

Original article

Comparison of demographic and clinical characteristics of patients with early vs.

adult vs. late onset ulcerative colitis
smail Hakk Kalkan a,, lk Dali b, Erkin zta a, Bilge Tun a, Aysel lker a
a
b

Gastroenterology Department, Turkiye Yuksek Ihtisas Hospital, Ankara, Turkey

Gastroenterology Department, Bolu Abant zzet BAYSAL University, Turkey

a r t i c l e

i n f o

Article history:
Received 21 October 2012
Received in revised form 12 December 2012
Accepted 13 December 2012
Available online 12 January 2013
Keywords:
Ulcerative colitis
Late-onset
Early-onset
Clinical course
Colectomy

a b s t r a c t
Background & aims: There is limited data comparing inuence of age on the presentation, clinical course, and
therapeutic response of patients with ulcerative colitis. We aimed to compare the demographic and clinical
characteristics of patients diagnosed with UC in older age vs. adulthood vs. early age.
Methods: Five-hundred sixty one patients with UC seen at our center from 1995 to 2011 were categorized into
early onset (EO), adult onset (AO) and late onset (LO) due to age at date of initial diagnosis. Patients diagnosed
younger than age 17 were dened as EO, while those diagnosed between 17 and 60 were dened as AO and older
than age 60 as LO. All patients were analyzed for demographic and clinical characteristics.
Results: There was a male predominancy among LO patients (50% vs. 57.7% vs. 78.6%, p =0.004). Patients with
EO UC were more likely to be non-smokers (pb 0.001), and had higher family history of UC (p=0.02). Patients
with EO UC had more steroid use (p=0.03), total colectomy (p=0.04), presence of chronic active disease (p=
0.04) rates when compared with AO and LO groups. Patients in EO group had higher overall probability of surgery in 1, 5 and 10 years, when compared with patients in LO group (p=0.02), but it wasn't different between
EO and AO groups (p=0.09).
Conclusions: Our study showed that clinical course of UC was more aggressive in younger ages. Also the difference between the demographic characteristics suggests that different age groups have different risk factors for
the disease development.
2012 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.

1. Introduction
Ulcerative colitis (UC) is an inammatory disease of colon and rectum that has a bimodal peak of incidence. It is most commonly found
in teenagers and young adults with a peak incidence between 20 and
29 years of age. A second peak incidence has been reported in the 60
to 70 age group. Approximately 15% of cases manifest after the age of
65 years [14]. The incidence of late onset UC is expected to increase
due to the aging of population; therefore, an attention to the epidemiologic and clinical features specic to this cohort is essential for optimizing medical management.
There are conicting data regarding the clinical course and epidemiologic/clinical characteristics for UC with respect to age at disease.
Most studies have demonstrated a comparable clinical course among
patients with UC who are diagnosed at an older age and younger age
[57]. Due to earlier reports; the older patients tend to have UC with a
more aggressive clinical course [8,9]. In contrast, more recent studies
have found no differences in clinical course between older and younger patients presenting with an initial UC are. Some have even
Corresponding author at: Attar Sokak 21/14, Gaziosmanpaa/ankaya 06700, Ankara,
Turkey. Tel.: +90 505 270 40 85.
E-mail address: drismailster@gmail.com (.H. Kalkan).

demonstrated that older patients may have a more benign clinical

course [10,11].
In this study, we aimed to compare the demographic characteristics of patients diagnosed with UC in early age vs. adulthood vs.
older age in the term of the continuity of the disease. We also examined the association of age at diagnosis between disease phenotype,
clinical course of UC and requirement of surgery.
2. Material and methods
2.1. Study population
All patients with an established diagnosis of UC and regularly
followed-up were identied using medical records maintained consecutively in the Inammatory Bowel Disease outpatient clinic in
our center over a 15-year period from 1995 to 2011. The date of initial
UC diagnosis was conrmed by review of initial diagnostic endoscopic data, histopathologic, clinical and radiographic ndings. Patients
were categorized into early onset (EO), adult onset (AO) and late
onset (LO) due to age at date of initial diagnosis. Patients diagnosed
younger than age 17 were dened as EO, while those diagnosed between 17 and 60 were dened as AO and older than age 60 as LO.
All patients were analyzed for age, gender, family history, smoking

0953-6205/$ see front matter 2012 European Federation of Internal Medicine. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.ejim.2012.12.014

.H. Kalkan et al. / European Journal of Internal Medicine 24 (2013) 273277

274

Table 1
Comparison of epidemiologic and demographic characteristics of patients in EO, AO and LO groups.
EO (n = 58, 10.3%)

AO (n = 447, 79.7%)

LO(n = 56, 10.0%)

p value

Age (mean SD) (years)

Age at diagnosis (mean SD) (years)
Follow-up time (mean SD) (years)
Gender (male, %)
Presence of family history (n, %)

25.5 6.0
15.3 1.4
10.1 6.1
29 (50.0)
9 (15.5)

46.0 10.9
37.3 9.6
8.7 6.5
258 (57.7)
34 (7.6)

72.9 6.5
65.2 5.1
7.7 4.6
44 (78.6)
1 (1.8)

b0.001a
b0.001a
0.1
0.004a
0.02a

Smoking habitus
Ex-smoker (n, %)
Smoker (n, %)
Non-smoker

1 (1.7)
4 (6.9)
23 (91.4)

106 (23.7)
62 (13.9)
279 (62.4)

22 (39.3)
2 (3.6)
32 (57.1)

b0.001a

EO: Early-Onset Group, AO: Adult-Onset Group, LO: Late-Onset Group.

a
Statistically signicant.

habitus, duration of disease, localization of disease, clinical course,

medical treatment, corticosteroid (CS) resistancy and dependency,
further extension in localization of the disease, requirement of total
colectomy and mortality.
2.2. Clinical course
To detect the presence of chronic continious symptoms the clinical
course guideline about UC which has been published by European
Crohn's and Colitis Organization (ECCO) in 2008 was used [12].
According to this guideline, the presence of chronic active disease
(CAD) was described to patients who have persistent symptoms of
active UC without a period of remission.

variables were provided as percentages. Comparisons of continuous

variables were made using the One-Way ANOVA depending on normality of distribution. Categorical variables were compared by the
Pearson's or Fisher's exact Chi-square tests. Kaplan-Meier survival
(KMS) curves was built for the overall probability of surgery after
1, 5, and 10-years, ever steroids exposure and further extension in disease when the patients were divided into 3 groups according to age at
diagnosis; EO, AO and LO. Standardized Mortality Ratios (SMRs) has
been calculated for each study group by the division of age specic observed death rates to age specic expected death rates. Age specic
expected death rates has been maintained by the data of general population which has been presented by the Turkish Statistics Institute. A
SMR greater than 1.0 has been accepted as an indicator of increased
mortality risk.

2.3. Steroid dependency and resistance to steroid

3. Results
The guideline about UC which has been published by European
Crohn's and Colitis Organization (ECCO) in 2008 was used to dene
the steroid-dependent and steroid-resistant patients. According to
this; patients who were either unable to reduce steroids below the
equivalent of prednisolone 10 mg/day within 3 months of starting steroids, without recurrent active disease; or who had a relapse within
3 months of stopping steroids were considered as steroid-dependent
while the patients who had active disease despite prednisolone up to
0.75 mg/kg/day over a period of 4 weeks were considered as steroidresistant patients [12].

3.1. Study population

The complete records of a total of 561 patients (230 (41.0%) female
and 331(59.0%) male) fullling inclusion criteria at our hospital during
the study period could be retrieved, with a mean follow-up period of
8.8 6.3 years. Fifty-eight (10.3%) patients were in EO group, 447
(79.7%) patients were in AO group and 56 (10.0%) were in LO group.

2.4. Statistical analysis

Statistical analyses were performed using SPSS version 18 (SPSS,
Chicago, IL). Descriptive statistics; frequencies, means and standard
deviations; were calculated in each case. Values for continuous variables were given as mean standard deviation while categorical
Table 2
Comparison of groups due to disease phenotype and clinical course.
EO, (n = 58)

AO, (n = 447)

LO, (n = 56)

p value

Localization of disease
Distal (n, %)
Left-sided (n, %)
Extensive (n, %)

13 (22.4)
19 (32.8)
26 (44.8)

157 (35.1)
147 (32.9)
143 (32.0)

15 (26.8)
26 (46.4)
15 (26.8)

0.06

Presence of chronic
Active disease (n, %)
Steroid use (n, %)
Steroid dependency (n, %)
Steroid resistance (n, %)
Total colectomy (IPAA)

11 (19.0)
22 (37.9)
5 (21.7)
4 (17.4)
10 (17.2)

38 (8.5)
127 (28.4)
15 (12.2)
21 (17.1)
37 (8.3)

4
9
2
2
3

0.04a
0.03a
0.4
0.9
0.04a

(7.1)
(16.1)
(20.0)
(20.0)
(5.4)

EO: Early-Onset Group, AO: Adult-Onset Group, LO: Late-Onset Group, IPAA: Ileal-Pouch
Anal Anastomosis.
a
Statistically signicant.

Fig. 1. Comparison of further extension of localization free survival rates among

patients in EO, AO and LO groups.

.H. Kalkan et al. / European Journal of Internal Medicine 24 (2013) 273277

Fig. 2. Comparison of probability of ever steroids exposure among patients in EO, AO

and LO groups.

275

Fig. 3. Comparison of total colectomy free survival rates among patients in EO, AO and
LO groups.

while it was 12.2% (15/127) in AO group and 20.0% (2/20) in LO

group (p= 0.4). (Table 2).

3.2. Demographic characteristics

The gender distribution was different in study groups, with a higher
proportion of males among LO patients (50.0% vs. 57.7% vs.78.6%,
p = 0.004). No statistically signicant difference in follow-up time was
present between groups (p= 0.1). Patients with EO UC were more
likely to be non-smokers (91.4% vs. 62.4 vs. 57.1%, p b 0.001), and had
a family history of UC compared to AO and LO patients (13.9% vs. 6.9%
vs. 3.6%, p = 0.02) (Table 1).
3.3. Disease phenotype and clinical course
Distribution of disease location didn't differ between groups
(Left-sided disease; 32.8 vs. 32.9 vs. 46.4%, p = 0.06). The presence
of CAD was signicantly higher in EO group. Eleven (19.0%) of patients in EO group, 38 (8.5%) patients in AO group and 4 (7.1%) of patients in LO group had chronic continuous symptoms (p = 0.04)
(Table 2). A KMS curve was built to compare further extension free
survival rates, there was no statistical difference between groups
(p = 0.7) (Fig. 1).

3.5. Surgery
Total colectomy, (Ileal-Pouch Anal Anastomosis) IPAA was performed for 10 (17.2%) patients in EO group, 37 (8.3%) patients in AO
group, and 3 (5.4%) patients in LO group (p=0.04). Indications for
each group are shown in Table 3. When overall probability of surgery
after 1, 5, and 10-years was calculated, there wasn't a statistical difference between groups (p=0.05) (Fig. 3, Table 4), but when the EO
group was compared separately with AO and LO groups, there was a statistically signicant difference between EO and LO groups (p=0.02),
while it wasn't different between EO and AO groups (0.09). Also there
wasn't a difference between AO and LO groups (p=0.6).
3.6. Mortality
The calculation of SMRs for each age group revealed that, there was
an increase risk of mortality in EO (SMR = 40.0) and AO (SMR= 5.1)
groups. But in LO group, there was not an increase in mortality risk
due to UC (SMR=0.5) (Table 5).

3.4. Steroid therapy

4. Discussion
A total of 22 (37.9%) in EO group, 127 (28.4%) in AO group, and 9
(16.1%) in LO group had taken steroids at least once (p= 0.03). A KMS
which was built to compare probability of ever steroids exposure
showed that there was statistically difference between groups (p=
0.009) (Fig. 2). Among patients who had taken steroids at least once,
4 (17.4%) patients in EO group, 21 (17.1%) patients in AO group and 2
(20.0%) patients in LO group were considered as steroid-resistant
(p= 0.9). Steroid dependency rate was 21.7% (5/22) in EO group
Table 3
Comparison of indications of IPAA between study groups.

No response to medical
treatment/side effect of drug (n, %)
Emergent complication (n, %)
Dysplasia (n, %)

In the present study, a retrospective cohort analysis was used to

compare early vs. adult vs. late onset ulcerative colitis patients including
assessment of demographic characteristics of patients, extent of the disease, clinical course, treatment and outcomes in patients diagnosed
with UC between 1995 and 2011.
Due to some previous reports regarding the elderly population
with UC, the incidence of ulcerative colitis in older men exceeds

Table 4
Comparison of total colectomy free survival rates of groups.

EO
(n = 58)

AO
(n = 447)

LO
(n = 56)

8 (80.0)

27 (73.0)

2 (66.7)

1 (10.0)
1 (10.0)

8 (21.6)
2 (5.4)

1 (33.3)

p value

0.7

EO: Early-Onset Group, AO: Adult-Onset Group, LO: Late-Onset Group, IPAA: IlealPouch Anal Anastomosis.

Colectomy free survival

rates

EO
AO
LO

1 Year

5 year

10 year

93.1
98.2
99.3

83.5
95.6
98.0

83.5
91.2
93.1

Estimated colectomy free

survival time (95% CI)

23.2 (18.927.6)
29.7 (28.331.1)
16.0 (15.017.1)

Log-rank

p value

5.99

0.05

EO: Early-onset, AO: Adult-onset, LO: Late-onset, CI: Condence Interval.

.H. Kalkan et al. / European Journal of Internal Medicine 24 (2013) 273277

276

Table 5
Mortality rates in study groups and standardized mortality ratios for each age group.

b17 years
1860 years
>60 years

Mortality rates in
study groups
(number of exitus/
number of total
patients)

Mortality rates in
general population
(number of exitus/
number of total
population)a

SMR (CI, 95%)

1/58
4/447
1/56

5602/12.920.188
71.690/41.462.909
265665/8.057.202

40.0 (26.60260.426)
5.1 (2.7878.385)
0.5 (1.3222.472)

SMR: Standardized Mortality Ratio.

a
Population statistics and projections, Database of Turkish Statistics Institute.

that in older women. In the literature it has been reported that the
male/female ratio in elderly could be greater than 2 [13,14]. In our
study, in concordance with literature, there was a signicant male
predominancy (M/F:3.6, p = 0.004) in LO group. There are few data
that compare prominent risk factors for UC in early-onset and lateonset UC. According to the study of Ha et al., family history of UC was
more prevalent in the early onset cohort and former smoking status
was signicantly more common in the late onset cohort [15]. It has
been previously suggested that genetic factors may predominate the development of early-onset UC [16], while accumulation of environmental
exposure like tobacco over time and age-related changes in the immune
system and intestinal barrier function may promote the development of
late-onset UC [17]. In support of these reports we have found that, family
history of UC was signicantly higher in EO group while smoking status
was signicantly more common in LO group.
It has been suggested that ulcerative colitis tends to be less extensive when it develops later in life. Several reports conrm that there is
an extensive increase in the percentage of proctitis or left-sided colitis
in elderly patients with UC. Lakatos et al. found that left-sided colitis
was predominant in elderly patients with UC when compared with
young adults, also they found that further extension in disease location didn't signicantly differ between elderly patients and adults
[13,18]. In a multicenter study, 12.3% of patients over age 60 had
pancolitis, compared with 26.5% of those under the age of 60 [19].
In contrast with these results, Triantallidis et al. [20] found no signicant differences in the extent of the disease between younger and
older patients. In accordance with the literature, we found that leftsided colitis was predominant in LO group, while extensive disease
was predominant in EO group, but, there was not a signicant difference between groups, in terms of extension of the disease. Also, in
concordance with the literature [13], further extension in disease location was not signicantly different between groups.
Previous studies examining the clinical course of UC in elderly
patients have yielded conicting results. Late-onset UC has been
found to be more aggressive with fewer colectomies in some reports
[15,18,21], whereas other studies conrmed that disease course and
prognosis (including surgery rates) were not different between young
patients and patients diagnosed above the age of 40 years [22]. In a
population-based study from Aberdeen, Scotland, patients aged over
70 had severe initial episodes, compared with younger patients [23].
In a comprehensive review, excess of severe rst episodes and increased mortality rates in older patients has been described [16]. In contrast, the data of Lee et al. [22] showed a more severe disease course of
UC at younger ages. In their retrospective study on 455 patients with
UC, the patients were divided into two groups (older than 40 years at
diagnosis and younger than 40 years at diagnosis). They found that disease severity, frequency of pancolitis and steroid use were higher in the
young patients. Similarly, in study of Lacatos et al. [13], more adult patients required systemic steroids during follow-up compared to the elderly population, and age at diagnosis was independently associated
with the need for systemic steroid therapy in logistic regression analysis. In contrast, D'Jesus et al. found that, the patients who have been
diagnosed UC when aged more than 60 years old had more frequent

corticosteroid dependency-resistance and requirement for immunosuppressive treatment [24]. In our study, although we have found
higher systemic steroid requirement in EO group, steroid dependency
and steroid resistance rates were comparable between three groups.
The presence of CAD and total colectomy rates in term of clinical course
were higher in EO group when compared with AO and LO groups. Although comparison of groups was comparable according to overall
probability of surgery in 1, 5 and 10 years, when groups was compared
separately, it was higher in EO group when compared with LO group
(p= 0.02). But there wasn't a signicant difference between EO and
AO groups (p= 0.09). In contrast to previous reports [16], increased
mortality risk has not been detected in LO group in our study. Although
standardized mortality ratios were greater than 1 in EO and AO groups,
it should be kept on mind that there were very low absolute mortality
numbers in both groups.
Previous reports showed that, the presence of UC-associated dysplasia and cancer was comparable between younger age patients and
older age patients [13,20]. In our study, UC-associated dysplasia and
cancer was diagnosed in 1 (1.7%) in EO group, 2 (0.4%) in AO group,
while it wasn't detected in any patient in LO group. Due to the low absolute number of dysplasia/cancer cases, the head-to-head comparison of groups couldn't be performed.
There are certain limitations to this study. First of all although, only
regularly followed-up patients were included, its retrospective feature
is the major limitation of this study. Also, this is a single tertiary referral
center-based study. While referral centers tend to see sicker patients,
tertiary hospitals in our country has outpatient clinics and patients
can directly admit to these referral centers. The majority of patients
with UC are initially diagnosed in tertiary referral centers, and we
think that this fact reduces the possibility of selection bias in our study.
5. Conclusion
In our study we demonstrated that the indicators of clinical course
(presence of CAD, total colectomy, steroid use) were observed in higher
rates in EO group. We also demonstrated that tobacco use and male
gender were higher in LO group, while family history was higher in
EO group. All these ndings suggest that age-related factors differentially inuence the development, presentation and course of disease. We
believe that, prospective, large-size studies are essential to conrm
the demographic and clinical behavioral differences due to onset age
of UC to improve age-specic management and treatment.
Learning points
Approximately 15% of cases with UC manifest after the age of
65 years and the incidence of late onset UC is expected to increase
due to the aging of population.
Previous reports present conicting and limited data concerning
the relationship of the onset age with the presentation and clinical
characteristics of ulcerative colitis.
Our results showed that the clinical course of UC was more aggressive in younger ages. Also the demographic characteristics were different between groups suggesting that different age groups have
different risk factors for the disease development.
Conict of interests
Guarantor of the article: smail Hakk KALKAN
Financial support: None
Potential competing interests: None
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