Effects of Ficus carica paste on constipation induced by a high-protein feed and movement restriction in beagles

Abstract

Constipation is one of the most common functional digestive complaints worldwide. We investigated the laxative effects of figs (Ficus carica L) in a beagle model of constipation induced by high protein diet and movement restriction. The experiments were consecutively conducted over 9 weeks divided into 3 periods of 3 weeks each. All 15 beagles were subjected to a non-treatment (control) period, a constipation induction period, and a fig paste treatment period. We administered fig paste (12 g/kg daily, by gavage) for 3 weeks following a 3-week period of constipation induction in dogs. Segmental colonic transit time (CTT) was measured by counting radiopaque markers (Kolomark) using a radiograph performed every 6 h after feeding Kolomark capsules, until capsules were no longer observed. Fig paste significantly increased fecal quantity in constipated dogs, and segmental CTT was also reduced following fig paste administration. There were no significant differences in feed intake, water intake, body weight, or blood test results, between the constipation and fig paste administration periods. Our results demonstrate that fig is an effective treatment for constipation in beagles. Specifically, stool weight increased and segmental CTT decreased. Fig pastes may be useful as a complementary medicine in humans suffering from chronic constipation.

Full text

275
Effects of Ficus carica paste on constipation induced by
a high-protein feed and movement restriction in beagles
Hong-Geun Oh1, Hak-Yong Lee1, Min-Young Seo1, Young-Rye Kang1, Jung-Hoon Kim1, Jung-Woo Park1,
Ok-Jin Kim2*, Hyang-Im Back3,4, Sun-Young Kim3,4, Mi-Ra Oh3,4, Soo-Hyun Park3,4, Min-Gul Kim3,4,
Ji-Young Jeon3,4, Min-Ho Hwang3,4, Sook-Jeong Shin3,4, Soo-Wan Chae3,4,5*
1Huvet Co., Ltd, Iksan, Korea
2Center for Animal Resources Development, Wonkwang University, Iksan, Korea
3Clinical Trial Center for Functional Foods, and Chonbuk National University Hospital, Jeonju, Korea
4Clinical Trial Center, Chonbuk National University Hospital, Jeonju, Korea
5Department of Pharmacology, Chonbuk National University Medical School, Jeonju, Korea
Constipation is one of the most common functional digestive complaints worldwide. We investigated the
laxative effects of figs (Ficus carica L) in a beagle model of constipation induced by high protein diet and
movement restriction. The experiments were consecutively conducted over 9 weeks divided into 3
periods of 3 weeks each. All 15 beagles were subjected to a non-treatment (control) period, a
constipation induction period, and a fig paste treatment period. We administered fig paste (12 g/kg daily,
by gavage) for 3 weeks following a 3-week period of constipation induction in dogs. Segmental colonic
transit time (CTT) was measured by counting radiopaque markers (Kolomark) using a radiograph
performed every 6 h after feeding Kolomark capsules, until capsules were no longer observed. Fig paste
significantly increased fecal quantity in constipated dogs, and segmental CTT was also reduced following
fig paste administration. There were no significant differences in feed intake, water intake, body weight,
or blood test results, between the constipation and fig paste administration periods. Our results
demonstrate that fig is an effective treatment for constipation in beagles. Specifically, stool weight
increased and segmental CTT decreased. Fig pastes may be useful as a complementary medicine in
humans suffering from chronic constipation.
Key words: Constipation, fig paste, segmental colonic transit time, Kolomark, beagle dog
Received 26 September 2011; Revised version received 22 October 2011; Accepted 26 October 2011
Constipation is prevalent in modern societies and is a
common gastrointestinal symptom in c linical practice, affecting
5 to 20% of the general population [1]. Constipation is typically
defined as stool frequency of less than 3 bowel movements
per week [2]. Constipation is thought to be partially caused
by psychosocial and behavioral factors, such as decreased
mobility, inadequate caloric intake, and anorectal sensation
changes. Furthermore, it has a multifactorial etiology, including
co-morbid illness and medication side effects, including those
induced by narcotic analgesics, anticonvulsants, anti-
depressants, and anticancer drugs [3-5]. In addition, repeated
use of a purgative medicine can cause chronic constipation,
diarrhea, enteritis, and colorectal dysfunction, and is a risk
factor for colorectal neoplasm [6,7].
Although constipation is a symptom, rather than a disease,
it may be the cause of severe secondary diseases resulting
from enteral fermentation, inducing toxic gas, and therefore
requires active prevention and proper treatment [8]. The most
Lab Anim Res 2011: 27(4), 275-281
http://dx.doi.org/10.5625/lar.2011.27.4.275
*Corresponding authors: Soo-Wan Chae, Department of Pharmacology, School of Medicine, Chonbuk National University, 567
Baekjaedaero, Jeonju, Jeonbuk 561-712, Korea
Tel: +82-63-250-2348; Fax: +82-63-250-2349; E-mail: soowan@jbnu.ac.kr
Okjin Kim, Center for Animal Resources Development, Wonkwang University, 460 Iksandaero, Iksan, Jeonbuk 570-749, Korea
Tel: +82-63-850-6668; Fax: +82-63-850-7308; E-mail: kimoj@wku.ac.kr
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/
by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

276 Hong-Geun Oh et al.
Lab Anim Res | December, 2011 | Vol. 27, No. 4
common functional food remedy for constipation is dietary
fiber. There are various studies on the treatment of constipation
using natural substances [9.10].
The common fig (Ficus carica L) is a deciduous broadleaf
shrub belonging to the Moraceae family and is widely known
as one of the first edible fruits cultivated by humans in areas
with subtropical climate [11]. The fig originates from Carica
in Asia Minor and the primary fig producers now are America
and the Mediterranean [12]. Figs are high in natural and
simple sugars, minerals, water, and fiber. They contain
substantial levels of potassium, calcium, magnesium, iron,
copper, manganese, and sodium, while they are low in fat
[13,14]. They are a good source of flavonoids and polyphenols
as well as being rich in the phytosterols lanosterol and
stigmasterol [12]. Several reports have shown that the leaf,
stem, and woody tissue contain antioxidants and antibiotics
[15,16].
The purpose of the present study was to evaluate the laxative
effect of figs by measuring stool weight and colonic transit
time (CTT) after fig paste administration for 3 weeks in beagles
with constipation induced by a high protein diet and exercise
restriction.
Materials and Methods
Materials
Figs were supplied by the Black Raspberry Research Institute
(Gochang, Korea) and made into a paste at the Research
Center for Industrial Development of BioFood Materials
(Chonbuk University, Jeonju, Korea).
Animals
Fifteen healthy beagle dogs (4 years old; Marshall Beijing,
Beijing, China) with a weight range of 10-13 kg were purchased
from Orient Co (Seongnam, Korea). All animals were subjec ted
to a physical examination and were quarantined. The animals
were housed individually in clean cages (H100×W120×L120
cm) placed in a well-ventilated house with a controlled
temperature (25oC), 12/12-h light/dark cycle, and illumination
of 200 lux. All experiments complied with ethical standards
and were approved by the Animal Ethics Committee at
Wonkwang University (Iksan, Korea).
Constipation model
We created a canine model of constipation with 15 beagles
who were individually housed in general cage (H100×W120×
L120 cm). In order to induce a constipation condition, the
dogs were restrained in a small cage (H38×W60×L50 cm)
for 1 week and moved to indoor kennels.
The experiment was performed in the same 15 dogs and
separated to three time sections which were control period,
constipation period (constipation induction in the small cage),
and +fig paste period (fig paste administration), for 3 weeks
each. In control period, dogs were given feed containing
23% of proteins at the rate of 3% of weight and 100 mL/
kg of water. Being changed to over 40% of high proteins
(Feline feed, Purina Korea, Seoul, Korea) in constipation and
+fig paste periods, feed was cut down to 2% of weight to
inhibit the movement of digestive duct. Water also reduced
to 80 mL/kg. Dogs during constipation and +fig paste periods
were individually housed in small cage to restrict movement.
Dogs during +fig paste period were administered 12 g/kg
of fig paste.
Measurement of body weight, fecal weight, and
feed and water intakes
We measured body weights and stool weights each week
during the experimental periods. Feed and water intakes were
measured for each 24-h period.
Blood biochemical analysis
We analyzed serum chemical parameters for the assessment
of fig paste’s safety in the experimental beagles. Venous blood
was collected at the last day of each experimental period.
The whole blood was centrifuged at 2,000 g for 20 min at
4oC to obtain serum. Blood lipids including total cholesterol
(TC), high-density lipoproteins (HDL) and triglycerides (TG)
were analyzed using commercial kits (Sigma Diagnostics, St.
Louis, MO, USA). Serum aspartate aminotransferase (AST)
and alanine aminotransferase (ALT) as hepatotoxicity
parameters were measured using automated techniques at
the Department of Diagnostic Analysis, Wonkwang University
Hospital (Iksan, Korea).
Measurement of segmental CTT
Based on preliminary tests, in which normal CTT was less
than 6 h, 1 capsule of Kolomark (20 Ring; Konsyl Pharma-
ceuticals, Easton, MD, USA) containing 20 radiopaque rings,
was ingested at 09:00, and simple abdominal radiographs
were taken with PET 325 (Medinet, Gwangju, Korea) were
taken in the ventro-dorsal position at 6-h intervals until the
Kolomark was egested. The localization of markers on
abdominal films relied on identifying bony structures as
suggested by Arhan et al. [17]. Markers located to the right
of the vertebral spinous processes above a line from the seventh
lumbar vertebra to the right pelvic outlet were assigned to
the right colon, markers to the left of the vertebral spinous
processes and above an imaginary line from the seventh lumbar

Effects of Ficus carica paste on constipation 277
Lab Anim Res | December, 2011 | Vol. 27, No. 4
vertebra to the anterior superior iliac crest were assigned to
the left colon, and markers inferior to a line from the pelvic
brim on the right and superior iliac crest on the left were
judged to be in the rectosigmoid colon and rectum. CTT
was calculated by monitoring the Kolomark ring movement
in the entire or segmental colon [17].
Statistical analysis
Results are given as mean ±standard error (SE). Differences
were tested for significance by one-way ANOVA (Duncan’s
multiple-range test). Differences were considered significant
at error probabilities smaller than 0.05.
Results
Feed and water intakes and body weights
Feed intake was 318±13, 212±16, and 235±12 g during
the control, constipation, and +fig paste periods, respectively
(Table 1). This showed a significant tendency to decrease
feed intake between the constipation and +fig paste periods
compared with the control period, although the difference
in feed intake was not statistically significant between
constipation and +fig paste periods. There were no changes
in water intake or body weight among the 3 periods (Table
1 and Figure 1).
Fecal weights
To examine the laxative effect of fig paste on constipation,
the wet weight of stools was measured and compared. Figure
2 shows that fecal weight significantly decreased during the
constipation period compared with control period, while it
was significantly increased by fig administration (Figure 2,
P<0.05). However, after 24 h of drying, there was no d ifference
in water content (data not shown).
Blood biochemistry
Serum concentrations of blood lipids and hepatotoxicity
parameters such as TC, HDL, TG, AST, and ALT were not
significantly different among the 3 experimental periods (Table
2). The results of all experimental period were within the
normal range, and no abnormal symptoms were observed.
Segmental CTT
We observed the movement of Kolomark rings to assess
intestinal activity using time-dependant radiography (Figure
3). Kolomark rings migrated from the right colon to the
rectosigmoid colon over a period of time. The transit time
of Kolomark rings in the gastrointestinal tract was shortest
over constipation period and was shorter during the +fig
paste period than during constipation period. There was no
remarkable findings on the abdominal radiography. We
counted Kolomark rings using radiography (Figure 4, P<0.05).
The numbers of Kolomark rings in the right colon were higher
during +fig paste period than during constipation period after
6 h, but the numbers of Kolomark rings in the right, left,
rectosigmoid and total colons were fewer during +fig paste
period than during constipation period after 18 h (Table 3,
P<0.05). There were no Kolomark rings in the right colon
during the control period after 12 h, and all rings had been
Table 1. Effects of fig paste in change of feed and water intakes
(n=15)
Period Feed intake (g) Water intake (mL)
Control 318±13a879±103
Constipation 212±16b762±58
+fig paste 235±12b894±43
Column values with different superscripts are significantly
different (P<0.05).
Figure 2. Effects of fig paste on fecal weight in each
experimental period (n=15). Bars with different letters from the
control are significantly different (P<0.05).
Figure 1. Effects of fig paste on change in body weight in each
beagle experimental period (n=15).

278 Hong-Geun Oh et al.
Lab Anim Res | December, 2011 | Vol. 27, No. 4
egested after 18 h. The CTT of +fig paste period was 18
h, which was shorter than 30 h during constipation period.
The final Kolomark ring was egested after 48 h during
constipation period (data not shown). The CTT in the right
colon, left colon, rectosigmoid colon, and total colon during
control period was significantly faster than during constipation
and +fig paste periods. Whereas the CTT in the left colon
and total colon during +fig paste period was significantly
shorter than during constipation period, there were no
statistically significant differences in the CTT in the right and
rectosigmoid colons between constipation and +fig paste
periods.
Discussion
The Rome criteria define chronic constipation on the basis
of the presence of 2 or more of a list of 5 symptoms related
to the ability to defecate over a period of 3 months or more,
such as a frequency of 2 or less bowel movements per week,
stools of hard mass over 25%, uncomfortable feeling after
evacuation, fecal weight below 35 g, and excessive abdominal
press at defecation [18]. Chronic constipation can be caused
by peripheral neuropathy (Chagas disease or Hirschsprung’s
disease), obstructive disease (colon cancer, hernia, or intestinal
stricture), endocrine disease (hypothyroidism, diabetes mellitus,
or hypokalemia), drugs (morphine, anticholinergic compounds,
or calcium) and idiopathic factors [19].
Recently, the use of herbal remedies as constipation
treatments has become a common practice in many countries.
This study clearly demonstrates that fig extract or paste has
a laxative activity. Figs contain numerous components:
vitamins, minerals, cellulose, and amino acids [20,21]. They
are reported to have antioxidant effects, as well as beneficial
effects on cardiovascular, respiratory, and inflammatory
diseases [22,23].
Figs contain cellulose, and beneficial effects of cellulose
have been reported for cardiac disease, hype rtension, diabetes,
obesity, gastrointestinal disease, hyperlipidemia, and immune
function [24-30]. Lee and Hwang [31] reported that cellulose
increases fecal excretion by increasing water content and bulk,
and elevating viscosity, and that both water-soluble and
insoluble cellulose increases fecal egestion [32]. Fecal water
content and volume are increased by eating fiber that does
not decompose and is not digested by coliform bacilli [33,34].
Fig paste administration significantly decreased the feed intake
both during constipation and +fig paste periods compared
with control period. Our results show a tendency to increase
during +fig paste period compared with constipation period,
but this difference was not statistically significant. There were
no changes in water intake and body weight (Table 1 and
Figure 1). All serum chemistry results were also in the normal
range following fig administration, indicating that fig paste
Table 2. Effects of fig paste on blood biochemical parameters (n=15)
Period TC (mg/dL) HDL (mg/dL) TG (mg/dL) AST (mg/dL) ALT (mg/dL)
Control 157.07±6.00 123.87±4.33 32.93±3.24 38.67±1.38 72.40±15.80
Constipation 158.13±7.82 124.67±6.06 39.00±5.76 32.27±1.83 89.60±27.96
+fig paste 164.60±7.63 128.60±5.89 53.07±5.45 36.07±3.81 82.27±25.48
TC: total cholesterol, HDL: high-density lipoproteins, TG: triglycerides, AST: aspartate aminotransferase, ALT: alanine
aminotransaminase.
Figure 3. Effects of fig paste on radiographic measurement o
f
Kolomark transit in each experimental period (n=15). Rt.: right,
Lt.: left, Rs.: rectosigmoid.

Effects of Ficus carica paste on constipation 279
Lab Anim Res | December, 2011 | Vol. 27, No. 4
is safe to use (Table 2). The weight of stools significantly
decreased during constipation period compared with control
period, which was increased by fig paste administration,
although the water content of stools was not increased by
fig paste (Figure 2).
CTT is the basic test used to assess movement disorder
in the diagnosis of chronic constipation and irritable bowel
syndrome [35]. It involves the use of radiography to count
the number of markers remaining after a certain time period
following administration of a gelatin capsule that contains
20 radiopaque markers; segmental CTT is also reported by
Arhan et al. [17] and Metcalf et al. [36].
In the present study, considering that CTT in dogs is faster
than in humans, we took abdominal radiographs every 6
h until there was no remaining Kolomark in the body (Figure
3) and measured CTT by counting the number of Kolomark
rings in the intestinal tract (Table 3 and Figure 4). CTT was
shortest during the control period, of all 3 periods. CTT in
the left colon was faster during +fig paste period than during
constipation period, whereas in the right colon and rectosigmoid
colon, there was no difference between constipation period
and +fig paste period. In our study, we confirmed that total
CTT was fastest during control period followed by +fig paste
period, and this result indicates that CTT was decreased by
fig administration. Soluble cellulose accelerates peristaltic
activity by maintaining higher acidity, because fermented
cellulose results in acid production by coliform bacilli in rats
[37]. Furthermore, Gordon [38] reported that cellulose shortens
large intestine transit time, so that fecal e xcretion time decreases
accordingly. Similar to our results, Spiller et al. [39] reported
that intestinal transit time was diminished following
administration of food-mixed cellulose and 5% guar gum,
compared with rats given normal food [39]. Moreover, Jenkins
et al. [40] reported that cellulose increases fecal egestion and
reduces intestinal transit time, as well as reducing fecal sojourn
time within intestines [40-42]. The shortened CTT indicates
that fig paste stimulates intestinal peristalsis and accelerates
fecal movement. Recently, intestinal ileum peristalsis was
reported to be enhanced in rats by treatment with a low
concentration of fig extract, but reduced by a high
concentration [43]. Similarly, Baldassano et al. [44] reported
that intestinal ileum peristalsis declined in a dose-dependent
manner in the isolated mouse intestinal ileum after treatment
with 10-320 mg/mL fig extract. Although these results differ
from ours, this might be due to different experimental
conditions with regard to animal species, type of figs used,
Table 3. Effects of fig paste on radiographic measurement of Kolomark transit for each experimental period (n=15)
Time Treatment Right colon Left colon Rectosigmoid colon Total colon
6 h
Control 2.00±1.03a5.50±1.80a3.20±1.55a10.70±2.32a
Constipation 8.53±1.86b10.93±1.82b0.40±0.40b19.87±0.50b
+fig paste 14.80±1.83c4.07±1.60a0.13±0.09b19.00±1.00b
12 h
Control 0.00±0.00a2.50±1.18a5.90±1.59a8.40±1.70a
Constipation 3.87±1.78b14.00±1.74b1.67±0.87b19.53±0.35b
+fig paste 2.27±1.18b10.60±2.07b4.47±1.78a17.33±0.67b
18 h
Control 0.00±0.00a0.00±0.00a0.00±0.00a0.00±0.00a
Constipation 0.67±0.37b15.33±1.60b3.40±1.56b19.40±0.48b
+fig paste 0.00±0.00a6.67±2.09c7.40±1.93b14.07±2.12c
24 h
Control 0.00±0.00a0.00±0.00a0.00±0.00a0.00±0.00a
Constipation 0.53±0.32b11.40±2.25b4.47±1.88b16.40±1.95b
+fig paste 0.00±0.00a2.47±1.48c9.40±2.36b11.87±2.46b
30 h
Control 0.00±0.00 0.00±0.00a0.00±0.00a0.00±0.00a
Constipation 0.00±0.00 5.40±2.1b8.53±2.29b13.93±2.32b
+fig paste 0.00±0.00 0.20±0.20c2.60±1.68c2.80±1.81c
Data are numbers of markers present. Column values with different superscripts are significantly different (P<0.05).
Figure 4. Effects of fig paste on change in segmental CTT fo
r
each experimental period (n=15). Bars with different letters
from the control are significantly different (P<0.05). Rt.: right,
Lt.: left, Rs.: rectosigmoid.

280 Hong-Geun Oh et al.
Lab Anim Res | December, 2011 | Vol. 27, No. 4
and dosage.
In conclusion, feeding fi g paste increased fecal weight, which
had been decreased by diet-induced constipation, and
shortened CTT. The results of serum chemistry showed that
oral administration of fig paste is safe, and we did not observe
any abnormal symptoms in experimental animals. Therefore,
fig paste may be suitable for human patients suffering from
constipation, particularly where it is due to diet. In addition,
our findings on the use of beagles as a constipation model
could be useful in other constipation studies.
Acknowledgments
This work was supported by the Yeong-Am Figs of Food
Cluster project of the Ministry for Food, Agriculture, Forestry
and Fisheries, Republic of Korea (Grant: 2008-001).
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