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Contents lists available at ScienceDirect

Digestive and Liver Disease

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

Oncology

The fecal immunochemical test has high accuracy for detecting

advanced colorectal neoplasia before age 50
Nam Hee Kim, Jung Ho Park, Dong Il Park, Chong Il Sohn, Kyuyong Choi, Yoon Suk Jung
Division of Gastroenterology, Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Republic
of Korea

a r t i c l e i n f o a b s t r a c t

Article history: Background: In contrast to the decreasing incidence of colorectal cancer (CRC) in adults 50 years, the
Received 13 October 2016 CRC incidence in young adults <50 years is increasing. The fecal immunochemical test (FIT) may be useful
Received in revised form for advanced colorectal neoplasia (ACRN) screening in a young population.
13 December 2016
Aims: To evaluate the diagnostic accuracy of FIT in a young population.
Accepted 15 December 2016
Methods: The diagnostic performance of FIT for detecting ACRN was compared among the following age
Available online xxx
groups who underwent FIT and colonoscopy as part of a comprehensive health screening program: 3039,
4049, and 50 years.
Keywords:
Advanced colorectal neoplasia
Results: Of 26,316 participants, 464 (1.8%) had ACRN and 805 (3.1%) showed positive FIT results. No
Fecal immunochemical test signicant differences in the sensitivity (22.1%, 17.2%, and 22.0%; p = 0.435) and specicity (97.2%, 97.4%,
Young population and 96.9%; p = 0.344) of FIT for detecting ACRN were observed among the groups. However, 3039 age
group had a signicantly higher accuracy of FIT for ACRN (96.7%) than 4049 and 50 age groups (95.9%
and 93.8%; p < 0.001). The areas under the receiver operating characteristic curves of FIT for ACRN of three
age groups were not signicantly different (67.2, 66.2, and 61.7; p = 0.952).
Conclusions: The diagnostic performance of FIT for ACRN in a young population (<50 years) was not inferior
to that in the current screening-age population (50 years). The FIT may be a good choice for detecting
ACRN in a young population.
2016 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.

1. Introduction screening method because of its high diagnostic accuracy, and it

Colorectal cancer (CRC) is the third most common cancer in
male sex and the second most common in female sex, and it is the
fourth most common cause of death from cancer worldwide [1,2].
Moreover, CRC incidence in Asian countries has steeply increased
in recent years [3]. Therefore, prevention and early detection of CRC
has been an important global issue of substantial interest.
The fecal immunochemical test (FIT) is regarded as the most
effective, non-invasive CRC screening strategy currently available
[4,5]. FIT screening detects a large portion of CRC occurring in
asymptomatic average-risk populations and reduces the mortal-
ity rates of CRC [6,7]. In addition, a recent trial has shown that FIT
is similar to colonoscopy in detecting CRC as the rst-round CRC
Corresponding author at: Division of Gastroenterology, Department of
Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University
School of Medicine, 29, Saemunan-Ro, Jongno-Gu, Seoul, Republic of Korea.
Fax: +82 2 2001 2049.
E-mail addresses: ys810.jung@samsung.com, dodojys@hanmail.net (Y.S. Jung).
even has higher participation rates [8].
The current guidelines recommend CRC screening of average-
risk individuals starting at the age of 50 [6,9,10]; accordingly, CRC
incidence has decreased in adults aged 50 [2,11]. In contrast, the
CRC incidence in adults aged <50 has increased [2,1214]. More-
over, younger patients with CRC have been reported to have a
more aggressive disease course and worse outcomes than older
patients [15,16]. Considering that adults aged <50 comprise the
bulk of the economically active population, an increase in CRC inci-
dence in young adults may result in a socioeconomic burden in
the future. Therefore, clinicians should be concerned about young-
onset advanced colorectal neoplasia (ACRN), including CRC.
Recently, several studies have reported that male sex, smok-
ing, obesity, and metabolic factors are associated with a high risk
of colorectal neoplasia (CRN) [1721], and some researchers have
suggested that individuals with these risk factors benet from
undergoing screening colonoscopies starting at an age <50 [2225].
However, the most important concern with screening colono-
scopies performed before the age of 50 is low cost-effectiveness
because the likelihood of young individuals developing ACRN or

http://dx.doi.org/10.1016/j.dld.2016.12.020
1590-8658/ 2016 Editrice Gastroenterologica Italiana S.r.l. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Kim NH, et al. The fecal immunochemical test has high accuracy for detecting advanced colorectal
neoplasia before age 50. Dig Liver Dis (2016), http://dx.doi.org/10.1016/j.dld.2016.12.020
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CRC is relatively much lower than that of older individuals [2].
Thus, we speculated that FIT rather than colonoscopy may be a
good choice for ACRN screening in a young population because of
its advantages of non-invasiveness and low cost. However, data on
the diagnostic performance of FIT in a young population are very
limited. Therefore, in this study, we aimed to compare the diagnos-
tic accuracy of FIT for detecting ACRN in the following age groups:
3039, 4049, and 50 years, and we sought to conrm whether
FIT is useful even in a young population.
2. Patients and methods
2.1. Study population
We analyzed the prospectively established electronic medical
records of participants who underwent colonoscopy and FIT as part
of a comprehensive health screening program at the Total Health-
care Center of Kangbuk Samsung Hospital, Seoul and Suwon, Korea,
between 2010 and 2014 (N = 30,066). In Korea, the Industrial Safety
and Health Law requires employees to participate in annual or bien-
nial health examinations. Approximately 80% of the participants
were employees of various companies and local government orga-
nizations and their spouses, and the remaining participants were
those who volunteered to register individually in the screening
program. Before colonoscopy, interviews by general practitioners
were conducted to ensure that all participants were asymptomatic
(i.e., no lower abdominal pain or hematochezia). Participants with
intestinal symptoms were urged to seek medical care.
For this analysis, the exclusion criteria were as follows: poor
bowel preparation (n = 2574), lack of an adequate biopsy (n = 144), a
history of CRC or colorectal surgery (n = 190), a history of inamma-
tory bowel disease (n = 74), diagnosed with ischemic or infectious
colitis during this study (n = 13), and subjects <30 years (n = 755).
Finally, the total number of eligible subjects for this study was
26,316 (Fig. 1). Poor bowel preparation was dened as large
amounts of solid fecal matter found, precluding a satisfactory
study; unacceptable preparation; <90% of mucosa seen [26].
This study was approved by the Institutional Review Board of
Kangbuk Samsung Hospital.
2.2. Fecal immunochemical test
Participants collected a one-time stool sample in a sampling
tube (Eiken Chemical Company, Tokyo, Japan) within 3 days before
colonoscopy; the tube contained 2.0 mL of buffer, which minimized
hemoglobin degradation. The collected fecal material, sealed in
a plastic bag, was sent to the laboratory. Fecal hemoglobin con-
centration was quantitated using an OC-SENSOR DIANATM (Eiken
Chemical Company, Tokyo, Japan), and FIT results were expressed
in nanograms of hemoglobin per milliliter of buffer (ng Hb/mL). The
FIT-positivity cutoff value was 100 ng Hb/mL (equivalent to twenty
micrograms of hemoglobin per gram of feces) [27].
2.3. Measurements and denitions
Data on medical history and health-related behaviors were
collected through a self-administered questionnaire, whereas the
physical and serum biochemical parameter measurements were
obtained by trained staff. The participants smoking status was cat-
egorized as never, formerly, or currently, and family history of CRC
was dened as CRC in one or more rst-degree relatives at any
age. Self-reported use of non-steroidal anti-inammatory drugs
(NSAIDs; regular use over the previous month) was also assessed.
Body mass index (BMI) was calculated as measured weight (kg)
divided by the square of the height (m2 ), and obesity was dened as
Please cite this article in press as: Kim NH, et al. The fecal immunochemical test has high accuracy for detecting advanced colorectal
neoplasia before age 50. Dig Liver Dis (2016), http://dx.doi.org/10.1016/j.dld.2016.12.020
BMI 25 kg/m2 , which is the proposed cutoff value for the diagnosis
of obesity in Asians [28].
2.4. Colonoscopy and histologic examination
All colonoscopies were performed by experienced board-
certied endoscopists, using the Evis Lucera CV-260 colonoscope
(Olympus Medical Systems, Tokyo, Japan). The participants took
4 L of polyethylene glycol solution for bowel preparation.
All detected polypoid lesions were biopsied or removed and
histologically assessed by experienced pathologists. Polyps were
classied by number, size, and histologic characteristics (tubular,
tubulovillous, or villous adenoma; hyperplastic polyp; inamma-
tory polyp; and sessile serrated adenoma or traditional serrated
adenoma). Hyperplastic polyps, inammatory polyps, or lipomas
were considered normal ndings. The grade of dysplasia was classi-
ed as low or high. Advanced adenoma was dened as the presence
of one of the following features: >10 mm diameter, tubulovillous or
villous structure, and high-grade dysplasia [29]. ACRN was dened
as a cancer or advanced adenoma, and overall CRN was dened as
a cancer or any adenoma.
2.5. Statistical analysis
Data are expressed as mean standard deviation or frequency
(%). Baseline characteristics of the three age groups (i.e., 3039,
4049, and 50 years) were compared by chi-squared analysis or
Fishers exact test for categorical variables and by Students t-test
for continuous variables.
The major outcome variables were the sensitivity, specicity,
positive predictive value (PPV), negative predictive value (NPV),
and corresponding 95% condence intervals (CIs) of the FITs in
predicting colorectal lesions in the age groups. The diagnostic per-
formances of FIT for ACRN, advanced adenoma, CRC, and overall
CRN in the age groups were compared using chi-squared tests.
The area under the receiver operating characteristic curve (AUROC)
was also calculated in each age group to evaluate the differences
in the diagnostic accuracy of FIT for detecting ACRN. We deter-
mined whether statistically signicant differences exist among the
age groups using chi-squared test of homogeneity of areas.
All statistical analyses were performed using STATA version 14.0
(StataCorp LP, College Station, Texas, USA), and p values <0.05 were
considered statistically signicant.
3. Results
3.1. Baseline characteristics of the study population
Of 26,316 eligible participants (Fig. 1), 805 (3.1%) showed pos-
itive FIT results (100 ng Hb/mL). The mean age of the study
population was 42.1 years, and the proportion of male subjects was
72.3%. The number of participants aged 3039, 4049, and 50 was
11,404, 10,538, and 4374, respectively. Baseline characteristics and
colorectal lesions of the participants according to the age groups are
summarized in Table 1. The proportion of male subjects was higher
in the 3039 age group than in the older age groups, while the pro-
portion of participants with family history of CRC and use of NSAIDs
was higher in the 50 age group than in the younger age groups.
The proportion of current or ex-smoker was higher in the 4049
age group than in the other age groups.
The prevalence of advanced adenoma, CRC, ACRN, and over-
all CRN in the study population was 1.7%, 0.1%, 1.8%, and 16.9%,
respectively. The prevalence of advanced adenoma, CRC, ACRN, and
overall CRN was higher in the 50 age group than in the younger age
groups. The prevalence of ACRN in the 3039, 4049, and 50 age
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Fig. 1. Flow diagram illustrating the selection of study subjects.

Table 1 in the 3039, 4049, and 50 age groups, respectively; p = 0.007),

Comparison of baseline characteristics and colorectal lesions according to the age
and the proportion of positive FIT results was also higher in the 50
groups.
age group than in the younger age groups (2.9%, 2.9%, and 3.9% in
3039 4049 50 p value the 3039, 4049, and 50 age groups, respectively; p = 0.003).
(n = 11,404) (n = 10,538) (n = 4374)

Male sex 8651 (75.9) 7651 (72.6) 2728 (62.4) <0.001

Current or 5299 (48.6) 5329 (54.3) 1771 (47.7) <0.001
3.2. Diagnostic accuracy of the FIT according to the
ex-smoker participants characteristics
Family history 377 (3.3) 475 (4.5) 220 (5.0) <0.001
of CRC The diagnostic accuracy and predictive values of FIT for detect-
Use of NSAIDs 430 (3.8) 395 (3.8) 278 (6.4) <0.001
ing colorectal lesions according to the age groups are summarized
BMI 24.0 3.3 24.1 3.0 24.2 2.8 0.001
Obesity 4026 (35.3) 3745 (35.6) 1573 (36.0) 0.732 in Table 2. No signicant differences in the sensitivity and speci-
(BMI 25.0 kg/m )
2 city of FIT for detecting ACRN according to the age groups were
f-Hb 17.3 96.9 17.5 100.3 22.7 117.2 0.007 observed. The sensitivity of FIT for detecting ACRN in the 3039,
concentrations,
4049, and 50 age groups was 22.1%, 17.2%, and 22.0%, respec-
ng Hb/mL
FIT 100 ng 332 (2.9) 304 (2.9) 169 (3.9) 0.003
tively (p = 0.435). The specicity of FIT for detecting ACRN in the
Hb/mL 3039, 4049, and 50 age groups was 97.2%, 97.4%, and 96.9%,
respectively (p = 0.344). However, the 3039 age group had higher
Adenoma characteristics
LGD 1064 (9.3) 1922 (18.2) 1357 (31.0) <0.001 accuracy of FIT for detecting ACRN compared to the older age
Serrated 24 (0.2) 20 (0.2) 30 (0.7) <0.001 groups (96.7%, 95.9%, and 93.8% in the 3039, 4049, and 50 age
adenoma groups, respectively; p < 0.001).
HGD 3 (0.0) 16 (0.2) 14 (0.3) <0.001 No signicant differences in the sensitivity and specicity for
TVA or VA 1 (0.0) 10 (0.1) 18 (0.4) <0.001
Size 10 mm 81 (0.7) 176 (1.7) 173 (4.0) <0.001
detecting advanced adenoma, sensitivity for detecting CRC, and
3 adenomas 25 (0.2) 101 (1.0) 185 (4.2) <0.001 specicity for detecting overall CRN according to the age groups
Advanced 83 (0.7) 190 (1.8) 181 (4.1) <0.001 were observed. In contrast, the specicity of FIT for detecting CRC
adenoma was signicantly higher in the 3039 age group than in the older
Cancer 1 (0.0) 4 (0.0) 11 (0.3) <0.001
age groups (97.1%, 97.0%, and 96.3% in the 3039, 4049, and 50
ACRN 86 (0.8) 192 (1.8) 186 (4.3) <0.001
Overall CRN 1091 (9.6) 1956 (18.6) 1394 (31.9) <0.001 age groups, respectively; p = 0.013). The sensitivity of FIT for detect-
ing overall CRN was signicantly higher in the 50 age group than
Values are presented as numbers and percentages.
CRC, colorectal cancer; NSAIDs, non-steroidal anti-inammatory drugs; BMI, body
in the younger age groups (5.4%, 4.3%, and 6.2% in the 3039, 4049,
mass index; BP, blood pressure; FBG, fasting blood glucose; HDL-C, high-density and 50 age groups, respectively; p = 0.040). The 3039 age group
lipoprotein cholesterol; FIT, fecal immunochemical test; LGD, low-grade dyspla- had lower PPVs and higher NPVs for detecting ACRN, advanced
sia; HGD, high-grade dysplasia; TVA, tubulovillous adenoma; VA, villous adenoma; adenoma, CRC, and overall CRN compared to the older age groups.
ACRN, advanced colorectal neoplasia; CRN, colorectal neoplasia.
Similar to that for detecting ACRN, the accuracy of FIT for detect-
ing advanced adenoma (96.7%, 95.9%, and 93.8% in the 3039,
groups was 0.8%, 1.8%, and 4.3%, respectively (p < 0.001). Mean fecal 4049, and 50 age groups, respectively; p < 0.001), CRC (97.1%,
hemoglobin concentration was signicantly higher in the 50 age 97.1%, and 96.2% in the 3039, 4049, and 50 age groups, respec-
group than in the younger age groups (17.3, 17.5, and 22.7 ng Hb/mL tively; p = 0.006), and overall CRN (88.6%, 80.2%, and 68.2% in the

Please cite this article in press as: Kim NH, et al. The fecal immunochemical test has high accuracy for detecting advanced colorectal
neoplasia before age 50. Dig Liver Dis (2016), http://dx.doi.org/10.1016/j.dld.2016.12.020
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Table 2
FIT sensitivities, specicities, positive predictive values, and negative predictive values for different colonoscopy ndings by age groups.

Sensitivity (95% CI) p value Specicity (95% CI) p value PPV (95% CI) p value NPV (95% CI) p value Accuracy (95% CI) p value

ACRN 0.435 0.344 <0.001 <0.001 <0.001

3039 22.1 (13.932.3) 97.2 (96.997.5) 5.72 (3.58.8) 99.4 (99.299.5) 96.7 (96.397.0)
4049 17.2 (12.123.3) 97.4 (97.197.7) 10.9 (7.614.9) 98.4 (98.298.7) 95.9 (95.596.3)
50 22.0 (16.328.7) 96.9 (96.497.4) 24.3 (18.031.4) 96.6 (96.097.1) 93.8 (93.094.5)

Advanced 0.374 0.306 <0.001 <0.001 <0.001

adenoma
3039 21.7 (13.432.1) 97.2 (96.997.5) 5.42 (3.28.43) 99.4 (99.399.5) 96.7 (96.397.0)
4049 16.3 (11.422.4) 97.4 (97.097.7) 10.2 (7.014.2) 98.4 (98.298.7) 95.9 (95.596.3)
50 21.5 (15.828.3) 96.9 (96.397.4) 23.1 (17.030.2) 96.6 (96.097.1) 93.8 (93.094.5)

Cancer 0.999 0.013 0.003 0.002 0.006

3039 100 (2.5100.0) 97.1 (96.897.5) 0.30 (0.01.7) 100.0 (100.0100.0) 97.1 (96.897.4)
4049 75 (19.499.4) 97.0 (96.897.4) 0.99 (0.22.9) 100.0 (99.9100.0) 97.1 (96.897.4)
50 63.6 (30.889.1) 96.3 (95.796.8) 4.14 (1.78.4) 99.9 (99.8100.0) 96.2 (95.696.8)

Overall CRN 0.040 0.847 <0.001 <0.001 <0.001

3039 5.4 (4.16.9) 97.4 (97.097.7) 17.8 (13.822.3) 90.7 (90.191.2) 88.6 (88.089.1)
4049 4.3 (3.45.3) 97.4 (97.197.8) 27.6 (22.733.0) 81.7 (80.982.5) 80.2 (79.480.9)
50 6.2 (5.07.6) 97.2 (96.697.8) 51.5 (43.759.2) 68.9 (67.570.3) 68.2 (66.869.6)

Values are presented as percentages (95% condence interval).

ACRN, advanced colorectal neoplasia; CRN, colorectal neoplasia; PPV, positive predictive value; NPV, negative predictive value.

Fig. 2. Receiver operating characteristic curves of FIT for ACRN according to the age
groups (3039, 4049, and 50 years).
3039, 4049, and 50 age groups; p < 0.001) was higher in the
younger age group than in the older age groups.
We also calculated the AUROC in each age group to deter-
mine whether differences in the diagnostic accuracy for ACRN exist
(Fig. 2). The FIT AUROC for ACRN was 67.2 (95% CI, 60.673.8),
66.2 (95% CI, 61.970.4), and 61.7 (95% CI, 61.770.2) in the 3039,
4049, and 50 age groups, respectively. The FIT AUROCs for ACRN
in the three age groups were not signicantly different (p = 0.952).
4. Discussion
This large-scale study on 26,316 asymptomatic screened sub-
jects investigated the diagnostic performance of FIT according to
age groups. To the best of our knowledge, this is the rst study
to focus on the diagnostic performance of FIT in young adults <50
years. We found that at a 100 ng Hb/mL threshold, no signicant dif-
ferences in the sensitivity and specicity of FIT for detecting ACRN
according to age groups exist. However, the younger age group
(3039 years) had a signicantly higher accuracy of FIT for ACRN
compared to the older age groups (4049 and 50 years). Moreover,
the FIT AUROCs for ACRN of the age groups were not signicantly
different. In summary, the diagnostic performance of FIT for detect-
ing ACRN in a young population (<50 years) was not inferior to that
in the current screening-age population (50 years). Our results
suggest that FIT may be a useful screening strategy even in a young
population.
The current guidelines recommend CRC screening in average-
risk individuals starting at the age of 50 years based on a
signicantly increased risk of developing CRC or ACRN in adults
aged 50 compared with adults <50 years [6,9]; accordingly, the
incidence and mortality rates of CRC have been decreasing in adults
50 years over the past few decades [2,11]. However, in contrast
to the decreasing CRC incidence in adults 50 years, the CRC inci-
dence in young adults <50 years is increasing [2]. One researcher
predicted that by 2030, colon and rectal cancer incidence rates will
increase by 27.7% and 46.0%, respectively, for the 3549 age group
[14]. The majority of CRC occurring in young adults are sporadic,
and the exact etiology remains unclear [2]. The contribution of
behavioral and environmental factors, such as unhealthy dietary
choices and red meat consumption, physical inactivity, and obe-
sity, to the increasing incidence of CRC in young adults has been
proposed [2]. Considering that young adults <50 years are an eco-
nomically active population, an increase in CRC incidence in young
adults may result in a socioeconomic burden in the future. It is time
to be concerned about young-onset ACRN, including CRC.
Screening colonoscopies in young adults <50 years is not consid-
ered cost-effective because the likelihood of individuals <50 years
developing CRC or ACRN is relatively much lower than that of indi-
viduals >50 [2]. Thus, FIT, which is non-invasive, inexpensive, and
easy to perform, rather than colonoscopy, may be a good choice for
ACRN screening in a young population. However, few studies eval-
uating the diagnostic performance of FIT in young adults <50 years
exist. Our study is the rst to show that the diagnostic performance
of FIT for detecting ACRN in the 3039 and 4049 age groups is not
inferior to that in the 50 age group. A study in Taiwan on 6096
asymptomatic adults >40 years reported that the sensitivity of FIT
for ACRN in 4049 and 50 age groups was 32.1% and 19.2%, respec-
tively [30]. Similar to our results, the study demonstrated that the
sensitivity of FIT in the 4049 age group was not inferior to that in
the 50 age group. However, the studys focus was not on the FIT
accuracy in the <50 age group, and adults aged 3039 years were
not included [30].

Please cite this article in press as: Kim NH, et al. The fecal immunochemical test has high accuracy for detecting advanced colorectal
neoplasia before age 50. Dig Liver Dis (2016), http://dx.doi.org/10.1016/j.dld.2016.12.020
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Based on our ndings, FIT results may be helpful for the selection
of adults <50 years who could benet from undergoing screen-
ing colonoscopy. Recently, a few studies reported that male sex,
smoking, and obesity are the risk factors for CRN in a young popu-
lation; thus, individuals with these risk factors and family history
of CRC may benet from undergoing screening colonoscopies start-
ing at an age <50 [2225]. The combination of clinical risk factor
identication and FIT results may be more helpful for the selec-
tion of individuals who should begin screening colonoscopy earlier
than age 50. In other words, the strategy that young adults with
a high clinical risk of CRN undergo a FIT and then, those with a
positive FIT undergo a conrmative colonoscopy may improve the
cost-effectiveness of FIT performed before the age of 50.
This valuable study provides a better understanding of the
predictive performance of FIT in a young population. Nonethe-
less, this study has several limitations. First, it was hospital-based
rather than population-based, and our cohort was recruited at two
medical examination centers in Korea. Therefore, this may result
in some degree of selection bias. Thus, readers should take care
not to generalize on the basis of our results alone. To reach a
denitive conclusion, conducting validation studies in other pop-
ulations, including Western countries, may be necessary. Second,
cost-effectiveness of FIT was not evaluated in this study. Consid-
ering that the proportion of positive FIT results in adults aged <50
was relatively lower than that in adults aged 50 (2.9% vs. 3.9%),
further research that will give us more information about the cost-
effectiveness of FIT in a young population should be undertaken.
Lastly, we adopted a one-specimen FIT; therefore, the sensitivity of
FIT for detecting ACRN may have been underestimated.
In conclusion, the diagnostic performance of FIT for detecting
ACRN in a young population was not inferior to that in the cur-
rent screening-age population (50 years). The FIT may be a good
choice for ACRN screening even in a young population. Further
studies are needed to test the feasibility and cost-effectiveness of
FIT performed before the age of 50.
Conict of interest
None declared.
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