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Cryptogenic pyogenic liver abscess as the


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doi:10.1111/j.1440-1746.2011.06851.x

GASTROENTEROLOGY jgh_6851 248..255

Cryptogenic pyogenic liver abscess as the herald of colon


cancer
Soung Won Jeong,* Jae Young Jang,* Tae Hee Lee,* Hyun Gun Kim,* Sung Wook Hong,*
Seung Hoon Park,* Sang Gyune Kim,* Young Koog Cheon,* Young Seok Kim,* Young Deok Cho,*
Jin-Oh Kim,* Boo Sung Kim,* Eun Jung Lee and Tae Hyong Kim
*Institute for Digestive Research and Digestive Disease Center, and Department of Internal Medicine, Soonchunhyang University Hospital,
Seoul, Korea

Key words Abstract


colon cancer, colonoscopy, diabetes mellitus,
Klebsiella pneumoniae, pyogenic liver
Background and Aim: Colonic mucosal defects might be a route for bacterial invasion
abscess. into the portal system, with subsequent hematogenous spread to the liver. We retrospec-
tively investigated the results of colonoscopy and the clinical characteristics of patients
Accepted for publication 28 June 2011. with pyogenic liver abscess of colonic origin.
Methods: A total of 230 consecutive patients with pyogenic liver abscess were reviewed
Correspondence between 2003 and 2010. The 230 patients were categorized into three groups (pancreato-
Associate Professor Jae Young Jang, Institute biliary [n = 135], cryptogenic [n = 81], and others [n = 14]). Of the 81 cryptogenic patients,
for Digestive Research and Digestive Disease 37 (45.7%) underwent colonoscopy. Colonic lesions with mucosal defects were considered
Center, Division of Gastroenterology, colonic causes of abscess.
Department of Internal Medicine, Results: In the 37 colonoscopic investigations, colon cancer was found in six patients
Soonchunhyang University Hospital, Yong San (16.2%), laterally-spreading tumor (LST) in two patients (5.4%), multiple colon ulcers in
Gu, Han Nam Dong, Daesakwan Gil 22, one patient (2.7%), colon polyps in 17 patients (45.9%), and diverticula in four patients
Seoul, Korea. Email: jyjang@hosp.sch.ac.kr (10.8%). Nine (11%) of 81 cryptogenic abscesses were therefore reclassified as being of
colonic origin (colon cancer = 6, LST = 2, ulcer = 1). Three cases were stage III colon
cancer, and the others were stage I. Two LST were high-grade dysplasia. The percentage of
patients with Klebsiella pneumoniae (K. pneumoniae) and diabetes mellitus (DM) of
colonic origin was 66.7%, which was significantly higher than the 8.6% for other causes
(P < 0.001).
Conclusions: Of the 37 patients with cryptogenic pyogenic liver abscess who underwent
colonoscopy, nine (24.3%) were diagnosed with a colonic cause. Colonoscopy should be
considered for the detection of hidden colonic malignant lesions in patients with crypto-
genic pyogenic liver abscess, especially for patients with K. pneumoniae and DM.

with asymptomatic diverticulitis,3,4 inflammatory bowel disease,57


Introduction
tubulovillous adenoma,8,9 colon cancer,1019 and even colon
The liver is the organ most vulnerable to the development of polypectomy20 have been reported. It has been believed that
abscesses. Abcesses might arise from the hematogenous spread of mucosal defects present within colonic lesions or a compromised
bacteria or from contiguous sites of infection within the peritoneal mucosal barrier separating enteric bacteria from the circulation
cavity. Pyogenic liver abscess is usually related to hepatobiliary allows a route for bacteria invasion into the portal system, with
tract disease or intra-abdominal infections, including cholecystitis, subsequent hematogenous spread to the liver. Moreover, if the
suppurative cholangitis, suppurative pylephlebitis, appendicitis, colonic origin is colon cancer, prompt detection and treatment will
diverticulitis, and peritonitis.1,2 In the past, appendicitis with be essential. However, there have been few data about colono-
rupture and subsequent spread of infection was the most common scopic investigation in patients with cryptogenic pyogenic liver
source for a liver abscess. Currently, associated disease of the abscess, and there is no colonoscopic recommendation or consen-
biliary tract is most common. sus for these patients. Therefore, we retrospectively investigated
Recently, there have been many case reports of pyogenic liver the results of colonoscopy and the clinical characteristics of
abscess associated with various colonic diseases. The association patients with cryptogenic pyogenic liver abscess.

248 Journal of Gastroenterology and Hepatology 27 (2012) 248255


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
SW Jeong et al. Colon cancer in cryptogenic liver abscess

Methods start of antibiotic therapy. The abscess contents were aspirated


under abdominal ultraosonography guidance for diagnosis and
Patients microorganism culture. Cultures were isolated for aerobic and
anaerobic organisms. Organisms found from the abscess or in
Between May 2003 and May 2010, the records of 230 patients blood were assumed to be the etiologic organisms.
diagnosed with pyogenic liver abscess at the Soonchunhyang Uni-
versity Seoul Hospital in South Korea were reviewed. The cause of
pyogenic liver abscess was ascribed to the precipitating disease Association with DM
that was most likely to account for the abscess. Computed tomog- The presence of DM was evaluated in each patient, and was
raphy (CT) scan and routine laboratory tests were performed on all defined by the 1997 criteria:21 history of DM, or symptoms of
abscess patients. Biliary tract disease was documented by ultra- DM and casual blood glucose concentrations 200 mg/dL, or
sound, CT with contrast, magnetic resonance cholangiopancre- fasting plasma glucose 126 mg/dL, or 2 h plasma glucose
atography, or endoscopic retrograde cholangiopancreatography. 200 mg/dL during an oral glucose tolerance test.
When no primary cause of infection is found, the cause of abscess
was considered as cryptogenic by the physician in charge. Asso-
ciated conditions believed to contribute to abscess formation, such Statistical analysis
as diabetes mellitus (DM) or immunocompromise, were recorded. Fishers exact test was used to assess the association between
This study was approved by the institutional review boards of the etiology of abscess and the presence or absence of Klebsiella
Soonchunhyang University Hospital, Seoul, Korea. pneumoniae (K. pneumoniae) and DM. Data are presented as the
mean standard deviation. A P-value < 0.05 was considered sta-
Diagnosis tistically significant. All statistical analyses were performed using
the SPSS software package (version 17.0; SPSS, Chicago, IL,
Pyogenic liver abscess was diagnosed if the abscess was confirmed USA).
by imaging as well as by either documentation of an organism
from the abscess site or resolution of symptoms and signs after
antibiotic treatment. Patients with amebic infection with Entam- Results
oeba histolytica in pus or in the abscess wall, and patients found to
be ameba antibody immunoglobulin G positive by ELISA were Patients
excluded. The mean age of the 230 patients was 60.7 12.8 years. Of these,
120 (52.2%) were men, and 110 (47.8%) were women. The 230
Colonoscopic investigation patients with pyogenic liver abscess were classified according to
the cause of abscess: pancreatobiliary disease (n = 135), cryptoge-
The results of the colonoscopic investigation were reviewed from nic (n = 81), and others (n = 14; metastatic liver cancer, 7; appen-
the medical records between 2003 and 2010. Colonoscopy was dicitis, 5; prostate abscess, 1; postoperation colon cancer, 1). Of
performed based on the patients gastrointestinal symptoms or a the 81 cryptogenic patients, one patient with HIV infection and
search of an occult colonic etiology, unless the patients refused or one post-kidney transplantation patient were included.
could not tolerate a colonoscopy. Routine colonoscopic investiga-
tions were performed after the resolution of pyogenic liver
abscess, generally within 6 weeks of diagnosis. Colonoscopic investigation
Colonic lesions were categorized according to the colono- Colonoscopic investigation was performed in 37 (45.7%) of 81
scopic findings and histology. To identify a colonic cause of patients whose abscesses were of cryptogenic origin. Of these 37
cryptogenic pyogenic liver abscess, colonic lesions that had patients, 15 underwent colonoscopy for symptoms including
mucosal defects were investigated. When mucosal defects or altered bowel habits, hematochezia, and anemia, whereas 22
diverticulitis was noted in the colonoscopic findings, they were patients underwent colonoscopy purely to find the cause of the
determined to be the cause of pyogenic liver abscess. However, abscess. The median time to colonoscopy after the diagnosis of
colonic lesions that did not have mucosal defects, or diverticula abscess was 21 days (range: 1183). Colon cancer was noted in
without diverticulitis, were excluded as the cause of liver six patients (16.2%), laterally-spreading tumor (LST) with high-
abscess. The location of colonic lesions and the characteristics of grade dysplasia was noted in two (5.4%), multiple colon ulcers
the liver abscesses were also evaluated when colonic lesions was noted in one (2.7%), colon polyps were noted in 17 (45.9%),
were identified as the cause of the liver abscess. Colon cancer and diverticula were noted in four patients (10.8%). Of these,
was diagnosed with histology and assessed with stage. To iden- two patients had colon polyps and diverticula together. Nine
tify liver metastasis in colon cancer patients after abscess reso- patients (24.3%) showed normal colonoscopic findings. Both
lution, patients were monitored by abdominal enhanced CT scan mucosal defects and friability were noted in six patients with
after the treatment of colon cancer. colon cancer, two patients with LST, and one patient with mul-
tiple colonic ulcers. Seventeen cases of colon epithelial lesions
(small polyps without mucosal defects and four cases of diver-
Pathogens
ticula without diverticulitis) were not considered causative eti-
The microbiological results of blood and abscess cavity cultures ologies of abscess. Figure 1 shows the outcome of colonoscopic
were assessed. All samples for the cultures were taken before the investigation. Twenty-eight patients who underwent colonoscopy,

Journal of Gastroenterology and Hepatology 27 (2012) 248255 249


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
Colon cancer in cryptogenic liver abscess SW Jeong et al.

Figure 1 Algorithm of pyogenic liver abscess after colonoscopic investigation. LST, laterally-spreading tumor.

Figure 2 Distribution of causes in all patients according to colonoscopy. Distribution of causes in all patients before (a) and after (b) adding the results
of the colonoscopy. Others; metastatic liver cancer, appendicitis, prostate abscess, colon cancer, post operation state.

and 44 who did not, were classified as having cryptogenic colonoscopy lowers the rate of cryptogenic etiology among all
abscess, leading to reclassification of the initial 81 patients as patients with pyogenic abscess.
follows: cryptogenic, 72 (88.9%), and colonic, 9 (11.1%; colon In summary, our cohort of 230 pyogenic liver abscesses was
cancer, 6, 7.4%; LST with high-grade dysplasia, 2, 2.5%; colon classified as follows: pancreatobiliary (58.7%), cryptogenic origin
ulcers, 1, 1.2%). Figure 2 shows the distribution of causes in (31.3%), colonic (3.9%), metastatic liver cancer (3%), appendicitis
all 230 patients according to colonoscopy. It shows how (2.2%), others (0.8%) (Table 1).

250 Journal of Gastroenterology and Hepatology 27 (2012) 248255


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
SW Jeong et al. Colon cancer in cryptogenic liver abscess

Clinical characteristics of patients with T2N0M0). Pathologies for two patients with LST showed high-
abscesses of colonic origin grade dysplasia. Regarding the location, one was in the hepatic
flexure, and the other was in the transverse colon. Figure 3 shows
In nine cases with abscesses of colonic origin, there were six cases
LST and associated pyogenic liver abscess.
of colon cancer, two LST, and one case with multiple colonic
One patient, who was HIV positive, had multiple ulcers
ulcers. Among the six colon cancers, three were adenocarcinoma
throughout the entire colon. The median time to colonoscopy after
of the well-differentiated type, and three were of the moderately-
diagnosis of abscess was 23 days (range: 1153), the mean size of
differentiated type. With respect to the location of colon cancers,
liver abscesses was 6.1 4.2 cm, and the treatment for the liver
two were from the ascending colon, two were from the descending
abscesses in all the patients with colonic pathologies was percu-
colon, one was from the sigmoid colon, and one was from the
taneous catheter drainage and intravenous antibiotics therapy. All
hepatic flexure. Three patients were stage III (T3N1M0, T3N1M0,
patients recovered from liver abscess after treatment.
T2N1M0), and three patients were stage I (T1N0M0, T1N0M0,
The characteristics of all colonic lesions are shown in Table 2.
Of the six patients with colon cancers, three patients with stage
Table 1 Possible causes of pyogenic liver abscess III cancer had surgery with adjuvant chemotherapy. Of the other
three patients with stage I cancer, one patient with T2 had surgery
Cause Patients and adjuvant chemotherapy, one patient with a large T1 tumor had
n % surgery, and the other patient with a T1 tumor had endoscopic
mucosal resection (EMR). Two LST were removed completely by
Pancreatobiliary 135 58.7 EMR. The mean follow-up period was 38.7 32.3 months. There
Biliary stone 56 24.3
was no tumor recurrence or hepatic metastasis in these patients
Cholangiocarcinoma 51 22.2
during follow up.
Choledochoduodenostomy 10 4.3
Metastatic bile duct cancer 9 3.9
Pancreatic cancer 3 1.3
Pathogens
Benign bile duct stricture 3 1.3
Gallbladder empyema 2 0.9 Bacterial cultures from abscess pus or blood were performed in
Bile duct fistula 1 0.4 230 patients, with a positive culture rate of 64.8% (149/230).
Cryptogenic 72 31.3 Cultures were sterile in 81 (35.2%) patients, and multiple organ-
Colonic 9 3.9 isms were found in 12.1% (18/149) of positive cultures. Sixteen
Colon cancer 6 2.6 species of bacteria were cultured. K. pneumoniae was the most
LST with high-grade dysplasia 2 0.9 frequently isolated aerobe (42.9%, 73/170) (Fig. 4). For pancre-
Colon ulcer 1 0.4 atobiliary abscess patients (n = 135), the positive culture rate was
Metastatic liver cancer 7 3.0 66.7% (90/135). Multiorganisms were cultured from 15 patients.
Appendicitis 5 2.2 K. pneumoniae was the most frequently isolated aerobe (23%,
Prostate abscess 1 0.4
31/135), and Escherichia coli was the second most common
Colon cancer, post operation state 1 0.4
(21.5%, 29/135). For cryptogenic abscess (n = 72) cultures, the
LST, lateral spreading tumor. positive culture rate was 59.7% (43/72). One patient has a positive

Figure 3 Pyogenic liver abscess derived from huge laterally-spreading tumor. (a) Huge laterally-spreading tumor with mucosal defects and
easy-touch bleeding in colonoscopy, (b) Multiseptated pyogenic liver abscess in right lobe.

Journal of Gastroenterology and Hepatology 27 (2012) 248255 251


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
Colon cancer in cryptogenic liver abscess SW Jeong et al.

Diabetes
mellitus
Stenotrophomonas

Yes
Yes
Yes

Yes

Yes
Yes
Yes
No

No
Serratia
Morganella

Sixteen species of bacteria cultured


Acinetobacter

Klebsiella pneumoniae
Klebsiella pneumoniae
Klebsiella pneumoniae

Klebsiella pneumoniae
Klebsiella pneumoniae
Klebsiella pneumoniae
Klebsiella pneumoniae
Anaerobes
Citrobacter
Streptococcus

No growth Pseudomonas

No growth
Pathogen

Enterobacter
Enterococcus
Staphylococcus
Escherichia
Klebsiella
Liver abscess

Both/multiple

Both/multiple
Both/multiple
Right/single

Right/single

Right/single
Right/single
Left/single

Left/single

Pathogens recovered per case (%)

Figure 4 Number of pathogens recovered per case in patients with


pyogenic liver abscesses.
Hepatic flexure

Hepatic flexure
Entire colon
Descending

Transverse
Ascending
Ascending

culture for Escherichia and Enterococcus. K. pneumoniae was the


Location

Sigmoid
Sigmoid

most frequently isolated aerobe (41.7%, 30/72). For abscess due to


colonic origin (n = 9), the positive culture rate was 77.8% (7/9).
No patient had a culture for more than one organism. K. pneumo-
niae was the most frequently isolated aerobe (77.8%, 7/9).
Size (cm)

Association with DM and K. pneumoniae


1.8
3.4
2.1
5.0
4.0
2.3
2.9
2.5
2.1

The overall percentage of DM was 23% (53/230). The DM per-


centage was 20% (27/135) in the pancreatobiliary-origin category,
High grade dysplasia
High grade dysplasia

22.2% (16/72) in the cryptogenic-origin category, 77.8% (7/9) in


the colonic-origin category, 28.6% (2/7) in the metastatic liver
cancer category, and 0% (0/5) in the appendicitis category.
T2N1M0(III)
T3N1M0(III)
T3N1M0(III)
T1N0M0(I)
T2N0M0(I)

T1N0M0(I)

In patients with DM, the percentage of K. pneumoniae was


Stage

None

47.2% (25/53), and in patients without DM, the percentage of


K. pneumoniae was 27.1% (48/177) (P = 0.006).
The percentage of patients with both K. pneumoniae and DM in
colonic-origin abscesses was 66.7% (6/9), and those in the groups
Moderately differentiated
Moderately differentiated
Moderately differentiated

with cryptogenic and all other causes were 12.5% (9/72) and 8.6%
(19/221), respectively (P < 0.001 for both) (Fig. 5).
Acute inflammation
Well differentiated

Well differentiated
Well differentiated
Tubular adenoma
Tubular adenoma

Overall mortality
Histology

The hospital mortality for all 230 patients was 4.3% (10/230). Ten
patients died of sepsis and underlying disease. Nine of 10 patients
Characteristics of colonic lesions

had underlying cancer. Five patients had cholangiocarcinoma, two


patients had advanced gastric cancer, and one patient had pancre-
Diagnosis

atic cancer. One patient without underlying cancer died of septic


Cancer
Cancer
Cancer
Cancer
Cancer
Cancer

Ulcers

shock and femoral artery thrombosis. There was no death from


LST, laterally spreading tumor.
LST
LST

abscess without an accompanying underlying disease.

Discussion
(years)
Age

61
66
46
44
46
48
63
70
44

The aim of the present study was to examine the results of colonos-
copy and clinical characteristics of colonic origin in cryptogenic
pyogenic liver abscess. In this study, a colonoscopic investigation
Table 2

Female

Female
Female

Female

in patients with cryptogenic pyogenic liver abscess revealed a high


Male
Male

Male

Male

Male
Sex

percentage of advanced colonic lesions. Moreover, in the 45.7% of

252 Journal of Gastroenterology and Hepatology 27 (2012) 248255


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
SW Jeong et al. Colon cancer in cryptogenic liver abscess

P<0.001 strength of the immune barrier in the host, the difference in patho-
gens, and other as yet unknown complex factors that might regu-
P<0.001 late the invasion of bacteremia into the portal blood flow. In this
process, DM might weaken the immunologic system in affected
100%
patients.
33.3 K. pneumoniae has been reported to be the most common patho-
80% gen in Asia2733 and emerging pathogen in Western countries.34 In
No. patients (%)

our study, K. pneumoniae was the most common pathogen. Kleb-


60% siella is a colonizer in the human gastrointestinal tract and is rarely
87.5 91.4
associated with disease in the normal host. However, abscesses
40% containing only Klebsiella are much more likely to be cryptoge-
66.7 nic,31,34 and still, a considerable percentage of pyogenic liver
20% abscess are deemed cryptogenic (4099%).3538 In the present
study, K. pneumoniae was found to be highly associated with the
12.5 8.6
0% cryptogenic categories, including DM, compared to all other
causes. Interestingly, the percentage of K. pneumoniae in
Colonic cause Cryptogenic Other causes
abscesses of colonic origin was higher than that of cryptogenic
Figure 5 Percentage of patients with both Klebsiella pneumoniae and origin and in all other causes. Colonic mucosal defects might be
diabetes mellitus (DM) in colonic, cryptogenic and other causes. , Both the route of K. pneumoniae transmission. Also, the prevalence
Klebsiella pneumoniae and DM; , others. rates of K. pneumoniae were higher in the DM group, and these
findings are consistent with previous studies.34,3942 These results
could be explained by the hypothesis of intimal vascular defects in
patients who underwent colonoscopy, the percentage of colonic DM patients, which predispose to the hematogenous seeding of
tumors was 21.6% (8 patients; 6 patients with colon cancer, and 2 Klebsiella,40 the serotype K1 of Klebsiella,41 and the chromosomal
patients with LST with high-grade dysplasia). The percentage of heterogeneity of tissue-invasive Klebsiella strains.42
patients with DM and K. pneumoniae of colonic origin was sig- Finally, the percentage of colonic origin patients with both
nificantly higher than that of patients with K. pneumoniae and DM K. pneumoniae and DM was significantly higher than the percent-
with other causes. age among patients with cryptogenic and all other causes.
A considerable portion of pyogenic liver abscess had a crypto- We hypothesized that three factors are related to pyogenic liver
genic origin. Therefore, colonoscopy should be recommended in abscess in colon tumor patients with DM: (i) mucosal disruption
case of cryptogenic abscess to rule out a colonic origin, which and underlying blood vessel exposure due to colon tumor, (ii)
might be colon cancer, large adenoma, colon ulcers, diverticulitis, increased episodes of infectious disease in DM patients by
or inflammatory bowel disease. impaired PMN chemotaxis and phagocytosis; and (iii) the charac-
Colonoscopies have been actively performed since 1990, and in teristics of Klebsiella pathogen: DM affinity and chromosomal
many cases, colon cancer or large adenomas associated with pyo- heterogeneity of tissue invasiveness.
genic liver abscess have been reported. However, concrete data or However, colonoscopic investigation is not generally performed
guidelines for colonoscopic investigations in cryptogenic pyo- to search for the colonic origin. Lai et al.22 reported that only
genic liver abscess have not yet been elucidated. Recently, Lai 19.3% of patients with cryptogenic pyogenic liver abscess under-
et al. reported that cryptogenic pyogenic liver abscess might signal went endoscopic procedures or fecal testing analysis, and Rahim-
colorectal cancer. In their population-based, 5-year follow-up ian et al.43 reported that only 3.8% of all their pyogenic liver
study, the hazard of colorectal cancer was 3.36 times greater for abscess patients received colonoscopy.
patients with cryptogenic pyogenic liver abscess than for the com- We also performed colonoscopic investigation in only 45.7% of
parison group.22 cryptogenic pyogenic liver abscess patients. If we perform the
To our knowledge, the present study is the first to show concrete colonoscopy actively in deemed cryptogenic pyogenic liver
colonoscopic results and microbiological data regarding colonic abscess to detect a hidden colonic cause, we might be able to more
causes of cryptogenic pyogenic liver abscess. In our study, the accurately detect the colonic cause.
overall percentage of DM was 22.6% (52/230). However, the rate Although this study showed that the percentage of patients
of DM in patients with liver abscess of colonic origin was 77.8% with DM and K. pneumoniae in colonic origin was significantly
(7/9), which was higher than in patients with liver abscess of other higher than that of patients with other causes, K. pneumoniae is
or cryptogenic cause. Impaired polymorphonuclear neutrophil the most common pathogen in a pyogenic liver abscess, and DM
(PMN) chemotaxis and phagocytosis in diabetic patients might patients are more likely to have abscess, so high rates of DM and
increase the risk of infectious episodes.23 Also, DM and impaired K. pneumoniae are not unexpected in patients with pyogenic
glucose tolerance have been reported to be associated with an abscess of colonic origin. We feel that all patients with crypto-
increased incidence of colonic adenoma and cancer by hyperin- genic pyogenic liver abscess, regardless of the presence of DM or
sulinemia promoting colorectal carcinogenesis.2426 The associa- K. pneumoniae, should undergo colonoscopy to rule out an occult
tion with infection and colon cancer in DM might be the colonic etiology.
predisposing factor for pyogenic liver abscess with colon cancer. This study had several limitations. First, the data were collected
However, the reason all colon cancer patients with metastatic retrospectively from the medical records of a single tertiary care
liver cancer do not have evidence of liver abscesses might be the center where all patients did not undergo colonoscopy. Second, the

Journal of Gastroenterology and Hepatology 27 (2012) 248255 253


2011 Journal of Gastroenterology and Hepatology Foundation and Blackwell Publishing Asia Pty Ltd
Colon cancer in cryptogenic liver abscess SW Jeong et al.

colonoscopic investigation was not performed in all cryptogenic 16 Siegert CE, Overbosch D. Carcinoma of the colon presenting as
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