CC BY 4.0 · Journal of Digestive Endoscopy 2024; 15(01): 18-26
DOI: 10.1055/s-0044-1779617
Research Article

Correlative Factors of Severity of Air Bubbles in the Large Intestine during Colonoscopy

1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Atsushi Yamauchi
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Kumi Itami
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Shinichiro Odo
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Yoshihiro Soma
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Kosuke Tanaka
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Kazuki Negoro
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Yuki Mori
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Kazuki Osawa
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Ryou Itou
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Yuya Kawai
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Sota Nakagami
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Shunjiro Azuma
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Toshihiro Morita
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Kenshiro Hirohashi
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Katsutoshi Kuriyama
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Ken Takahashi
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Tadayuki Kou
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
Toshiro Katayama
2   Help Center of Medical Research, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
,
1   Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital, PIIF Tazuke Kofukai, Ohgimachi, Kita-ku, Osaka, Japan
› Author Affiliations
Funding None.
 

Abstract

Objectives The condition of air bubbles in the large intestine is an influential factor for good quality of colonoscopy. However, the correlative factors of severity of air bubbles during colonoscopy in the large intestine are not established. Therefore, this study aimed to elucidate the correlative factors influencing the severity of air bubbles in the large intestine.

Materials and Methods A total of 314 examinees who underwent colonoscopy between August and September 2022 were enrolled (median age [range], 65 [18–88] years). Air bubbles were scored using the Colon Endoscopic Bubble Scale (CEBuS) and the clinical factors associated with the CEBuS scores, especially in the ileocecum, were analyzed.

Results In this study, 39.8% (125/314) of examinees harbored severe air bubbles in the ileocecum. Multiple linear regression analysis revealed that the CEBuS scores in the ileocecum were positively associated with the interval time from completion of bowel preparation to intubation of the cecum (p = 0.0016) and a history of cholecystectomy (p = 0.0198). Logistic regression analysis between no, mild, and moderate air bubbles group (n = 189) and severe air bubbles group (n = 125) also showed that severity was positively associated with the interval time from completion of bowel preparation to intubation of the cecum (p = 0.0332) and a history of cholecystectomy (p = 0.0095).

Conclusion Interval time and history of cholecystectomy were associated with severity of air bubbles in the large intestine after bowel preparation.


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Introduction

Colorectal cancer (CRC) is the third major cause of cancer and the second major cause of cancer death.[1] The incidence and mortality of CRC are estimated to increase worldwide.[2] CRC screening has the potential to reduce the mortality rate.[3] Colonoscopy and polypectomy significantly decrease the incidence and mortality of CRC.[4] [5]

Bowel preparation prior to colonoscopy is indispensable. Its quality and visualization are related to the cecal intubation rate,[6] cecal intubation time,[6] [7] withdrawal time,[6] polyp detection rate (PDR),[8] adenoma detection rate (ADR),[9] and detection rate of sessile serrated lesion.[10] Adequate bowel preparation quality is required for high-quality colonoscopy. Previous studies demonstrated that clinical factors could cause inadequate bowel preparation. The predictors of inadequate bowel preparation were the American Society of Anesthesiologists-Physical Status (ASA-PS) score[6]; age; reported failure to follow preparation instructions; inpatient status; procedural indication of constipation; use of tricyclic antidepressants; use of opioids; male sex; and history of cirrhosis, stroke, or dementia.[11] [12] However, air bubbles in the large intestine could be also an obstacle to visibility in colonoscopy and increase the risk of missed lesions, endoscopist fatigue, and flushing dose.[13] [14] [15] However, these studies focused on the influence of air bubbles on the quality and trouble of colonoscopy and the measures to reduce air bubbles during colonoscopy, not the risk factors of incidence and severity of air bubbles themselves. Clinical, procedural, timing, and medicinal factors affecting bowel bubble severity were not well identified.

Therefore, this study aimed to elucidate the correlative factors of severity of air bubbles in the large intestine after bowel preparation.


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Methods

Examinees

This retrospective cohort study was conducted at a single institution. First, we recruited 459 examinees who underwent colonoscopy in an outpatient setting at the Medical Research Institute Kitano Hospital (Osaka, Japan) between August and September 2022. Clinical data were collected from their medical records, endoscopic videos, and endoscopic reports. We recorded almost all endoscopic videos from 2017, and that made it possible to collect the precise time from the videos.

The inclusion criteria of this study were as follows: ≥18 years of age, scheduled bowel preparation as mentioned in the bowel preparation section, successful total colonoscopy (the intubation of the cecum or anastomosis in case of ileocecal resection), and successful record of entire endoscopic videos. Examinees with colectomy (low anterior resection, n = 8; right hemicolectomy, n = 5; ileocolic resection, n = 1; resection of the transverse, n = 1; left hemicolectomy, n = 1; sigmoid colectomy, n = 1) were included except those with ileostomy (n = 1). A flowchart of enrollment in this study is illustrated in [Fig. 1].

Zoom Image
Fig. 1 The flowchart of enrollment and selection of examinees in this study.

The exclusion criteria and the number of examinees excluded from this study were as follows: no submission or inadequate bowel preparation data (n = 84), no video (n = 25), not accomplishing complete bowel preparation (n = 18), no bowel preparation (n = 10), bowel preparation besides our designated regimen (i.e., Moviprep, Visiclear; n = 5), failure to perform cecal intubation (n = 2), and after ileostomy (n = 1). A total of 314 examinees were enrolled in this study. Two examinees underwent colonoscopy with designated bowel preparation for observing only the lesion near the ileocecal valve. They were counted in all variables but excluded from the analysis of withdrawal time. Exceptionally, we included all examinees with designated bowel preparation and without ileostomy (n = 448) only when we calculated the cecal or anastomotic intubation rate as a clinical indicator.


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Bowel Preparation

We generally instructed examinees to perform bowel preparation as follows. First, they were required to eat low-residue diets 3 and 2 days before colonoscopy. They purchased and consumed the diet for colonoscopy (Clear Through; Kewpie, Tokyo, Japan) and were permitted to eat dinner the day before the colonoscopy. After dinner, 10 mL of 0.75% sodium picosulfate hydrate (Nichi-Iko Pharmaceutical Company, Toyama, Japan) and 24 mg of sennoside A/B calcium (Pfizer, New York City, New York, United States) were taken at 8 p.m. Second, the examinees began to take 2,000 mL of isotonic polyethylene glycol (PEG; NIFLEC; EA Pharma, Tokyo, Japan) at 7 a.m. Finally, colonoscopy was performed in the afternoon. Our bowel preparation method did not include simethicone. Only examinees who obeyed our designated bowel preparation method were included in this study, whereas we excluded those who required another isotonic PEG dose because of poor preparation.

The examinees were required to rate their stools in accordance with our instruction pamphlet. In our pamphlets, figures and figure legends of stool were illustrated and scored from 1 to 5 ([Supplementary Fig. S1], available in online version only). The examinees wrote the scores and timing in the pamphlets. We regarded 5 as complete bowel preparation. If the score did not reach 5 at the reserved time, colonoscopy was postponed and the examinees took another isotonic PEG dose. We retrieved the pamphlets and corrected the data regarding the first time a “5” was scored. No submission or inadequate data of bowel preparation pamphlets (n = 84) and colonoscopy that started before the examinees scored 5 (n = 18) were excluded from this study ([Fig. 1]).


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Evaluation of Air Bubbles and Bowel Preparation in the Large Intestine

To assess air bubbles associated with bowel preparation in the large intestine, we adopted the Colon Endoscopic Bubble Scale (CEBuS),[16] which is thought to have good intra- and interobserver reliabilities ([Supplementary Fig. S2], available in online version only). The grade is defined as follows:

  • CEBuS-0 = No or minimal bubbles covering less than 5% of the surface not hampering mucosa visibility.

  • CEBuS-1 = Moderate number of bubbles covering between 5 and 50% of the surface, affecting mucosa visibility and requiring additional time for removal.

  • CEBuS-2 = Severe bubbling, covering more than 50% of the surface, obscuring mucosa visibility, and requiring additional time for removal.

We scored CEBuS in the ileocecum or anastomosis, transverse colon or splenic flexure, and rectum from the video when inserting the colonoscope because flushing and suctioning of fluid when withdrawing the colonoscope affected the assessment of CEBuS.

To assess bowel preparation as a whole, we adopted the Boston Bowel Preparation Scale (BBPS),[17] a well-validated scale for assessment of bowel preparation and considered to have high intra- and interobserver agreement.[17] [18] [19] The grade is defined as follows:

  • BBPS-0 = Unprepared colon segment with mucosa not seen due to solid stool that cannot be cleared.

  • BBPS-1 = Portion of mucosa of the colon segment seen, but other areas of the colon segment not well seen due to staining, residual stool, and/or opaque liquid.

  • BBPS-2 = Minor amount of residual staining, small fragments of stool, and/or opaque liquid, but mucosa of colon segment seen well.

  • BBPS-3 = Entire mucosa of colon segment seen well with no residual staining, small fragments of stool, or opaque liquid.

We scored the BBPS in the ileocecum or anastomosis, transverse colon or splenic flexure, and rectum. We assessed BBPS from the video when withdrawing the colonoscope because flushing and suctioning of fluid were needed to assess the accurate BBPS. Endoscopic videos were blinded, and CEBuS and BBPS were evaluated by six experts after learning the scales from the original articles.[16] [17]

The large intestine is a long organ, and it is difficult to express total situation of air bubbles. Because air bubbles in the ileocecum and ascending colon are more difficult to clear, we focused on CEBuS in the ileocecum or anastomosis when attempting to elucidate its correlative factors.

We validated the quality of colonoscopy based on the success rate of cecal or anastomotic intubation,[20] [21] withdrawal time,[20] frequency of adverse events,[20] and PDR, an alternative index of ADR with a high degree of correlation,[22] [23] asserted as clinical indicators.


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Data Collection and Values

The following variables were collected from medical records: age, sex, ASA-PS, body mass index (BMI), Eastern Cooperative Oncology Group-Performance Status (ECOG-PS), comorbidity, medication, history of abdominal surgery including colectomy and cholecystectomy, and history of abdominal radiotherapy. The following variables were collected from endoscopic records: cecal or anastomosis intubation, diverticulosis, polyp detection, and adverse events. The following variables were collected from endoscopic videos: CEBuS, BBPS, intubation time, withdrawal time, and the time interval of colonoscopy. We defined the time interval of colonoscopy as the gap between the time when examinees scored 5 first on the bowel preparation in the pamphlets and the time when colonoscopy reached the cecum or anastomosis.


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Statistics

The Spearman's rank correlation coefficient was used to determine the correlation between continuous data of two groups. The Mann–Whitney U test was performed to compare the differences between the two independent groups. Single and multiple linear regression analyses were performed to predict the association between continuous or categorized explanatory variables and continuous objective variables. Logistic regression analysis was performed to predict the association of continuous or categorized explanatory variables with the binary group. For multivariate analysis, we included age, sex, ASA-PS, ECOG-PS, BMI, comorbidities, past history of operation including colectomy and cholecystectomy, past history of radiation, diverticulosis, medication, and the time interval of colonoscopy (minutes) as explanatory variables.

The Spearman's rank correlation coefficient and the Mann–Whitney U test were performed using GraphPad Prism (version 6.07 for Windows; GraphPad Software, San Diego, California, United States). Linear and logistic regression analyses were performed using EZR (version 1.51; Jichi Medical University, Saitama, Japan).[24] p-Values of <0.05 were considered statistically significant.


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Study Approval

Opt-out informed consent protocol was used for this study. This consent procedure was reviewed and approved by the Kitano Hospital (approval number [2209004], date of decision [September 14, 2022]). The study was conducted in accordance with the Declaration of Helsinki.


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Results

Patient Characteristics

The examinees' characteristics are summarized in [Table 1]. The mean age (range) was 65 (18–88) years, and 179/314 (57.0%) patients were men. A total of 312 examinees (99.4%) maintained a good (0, 1) ECOG-PS. A total of 187 (59.6%) examinees had comorbidities. Eighty-seven (27.7%) examinees had undergone abdominal surgery before colonoscopy, including colectomy (n = 17 [5.4%]) and cholecystectomy (n = 17 [5.4%]).

Table 1

Clinical characteristics of examinees

Examinees, n

314

Median age, y (range)

65 (88–18)

Sex (male/female), n

179/135

Median ASA-PS (range)

2 (1–3)

ASA-PS (0–2/3–4), n

220/94

Median ECOG-PS (range)

0 (0–2)

ECOG-PS (0–1/2–4), n

312/2

BMI (mean ± SD), kg/m2

23.3 ± 3.0

Comorbidity, n (%)

 Hypertension

109 (34.7)

 Diabetes

61 (19.4)

 Cardiovascular disease

40 (12.7)

 Cerebrovascular disease

24 (7.6)

 Renal disease

18 (5.7)

 Liver disease

6 (1.9)

 Dyslipidemia

77 (24.5)

 Respiratory disease

18 (5.7)

 Other malignancy

22 (7.0)

Having any comorbidities, n (%)

187 (59.6)

Having two or more comorbidities, n (%)

110 (35.0)

Abdominal operation, n (%)

87 (27.7)

Colectomy, n (%)

17 (5.4)

Ileocecal resection, n (%)

2 (0.6)

Cholecystectomy, n (%)

17 (5.4)

Abdominal radiation, n (%)

3 (1.0)

Diverticulosis, n (%)

109 (34.7)

Medication, n (%)

 Antithrombotic drugs

52 (16.6)

 Tricyclic antidepressants

0 (0.0)

 Opioids

3 (1.0)

 Proton pump inhibitors

72 (22.9)

 Laxative

49 (15.6)

Abbreviations: ASA-PS, American Society of Anesthesiologists-Physical Status; BMI, body mass index; ECOG-PS, Eastern Cooperative Oncology Group-Performance Status; SD, standard deviation.



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Quality of Colonoscopy

The clinical indicators of colonoscopy are listed in [Table 2]. The bowel preparation adequacy rate (BBPS score ≥ 6) was 99.7% (313/314). The cecal or anastomosis intubation rate was 99.6% (447/449) during the research period. The mean withdrawal time was 13 (5–60) minutes. Furthermore, 99.4% (310/312) of the withdrawal times were ≥6 minutes, whereas 89.4% (279/312) were ≥9 minutes. In this study, the PDR was 52.9% (165/312). For the examinees with no polyps detected, the mean withdrawal time was 11 (5–33) minutes; 99.3% (146/147) of the withdrawal times were ≥6 minutes ([Supplementary Table S1], available in online version only). No adverse events were observed. The clinical indicators in this study met the optimal standards for colonoscopy[25] and ensured that each colonoscopy was of high quality.

Table 2

Quality of colonoscopy

Median BBPS (range)

9 (5–9)

BBPS ≥ 6, n (%)

313/314 (99.7)

Cecal or anastomosis intubation rate, n (%)

446/448 (99.6)

Median withdrawal time (range), min

13 (5–60)

Withdrawal time ≥ 6 min, n (%)

310/312 (99.4)

Withdrawal time ≥ 9 min, n (%)

279/312 (89.4)

PDR, % (n)

52.9% (165/312)

Adverse event, n (%)

0/314 (0.0)

Abbreviations: BBPS, Boston Bowel Preparation Scale; PDR, polyp detection rate.



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Assessment of Air Bubbles in the Large Intestine

The results of the bowel bubble assessment are summarized in [Table 3]. The median time interval of colonoscopy (range) was 237 (30–456) minutes. In addition, 6.7% (21/314), 23.9% (75/314), and 39.8% (125/314) of the examinees had a CEBuS of 2 in the rectum, transverse colon or splenic flexure, and ileocecum or anastomosis, respectively. The correlation coefficients of CEBuS at the three locations are shown in [Supplementary Table S2] (available in online version only). The correlation coefficient of the rectum and transverse colon or splenic flexure was 0.4433 (p < 0.0001), and that of the rectum and ileocecum or anastomosis was 0.3309 (p < 0.0001); however, that of the transverse colon or splenic flexure and ileocecum or anastomosis was 0.6658 (p < 0.0001).

Table 3

Assessment of air bubbles in the large intestine

Median time interval of colonoscopy (range), min

237 (30–456)

CEBuS

Rectum, n (%)

 0

221 (70.4)

 1

72 (22.9)

 2

21 (6.7)

Transverse colon or splenic flexure, n (%)

 0

84 (26.8)

 1

155 (49.4)

 2

75 (23.9)

Ileocecum or anastomosis, n (%)

 0

60 (19.1)

 1

129 (41.1)

 2

125 (39.8)

Abbreviation: CEBuS, Colon Endoscopic Bubble Scale.


CEBuS at the three locations were not significantly correlated with polyp detection ([Supplementary Table S3], available in online version only).


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Correlative Factors for Air Bubbles in the Ileocecum or Anastomosis

We considered the CEBuS score a ranked variable and performed linear regression analysis. The single linear regression analysis showed that the time interval of colonoscopy was significantly correlated with the CEBuS score (p = 0.0004, [Fig. 2]). The results of the multiple linear regression analysis are summarized in [Table 4]. The time interval of colonoscopy (p = 0.0016) and a history of cholecystectomy (p = 0.0198) were significantly correlated with the CEBuS score.

Zoom Image
Fig. 2 The single linear regression analysis of CEBuS and the time interval between the time when examinees scored 5 on the preparation in the pamphlets and the time when colonoscopy reached the cecum or anastomosis. CEBuS, Colon Endoscopic Bubble Scale.
Table 4

Multiple linear regression analysis

Coefficients (±Std. error)

p-Value

Age

0.003340 ± 0.003863

0.3802

Sex

−0.04166 ± 0.09691

0.6677

ASA-PS

−0.1413 ± 0.08877

0.1127

ECOG-PS

0.006209 ± 0.1399

0.9646

BMI

−0.01588 ± 0.01272

0.2130

Hypertension

0.06835 ± 0.1161

0.5568

Diabetes

0.2271 ± 0.1258

0.0724

Cardiovascular disease

0.07227 ± 0.1647

0.6612

Cerebrovascular disease

0.02798 ± 0.2020

0.8899

Renal disease

−0.1433 ± 0.2015

0.4776

Liver disease

−0.2346 ± 0.3255

0.4718

Dyslipidemia

−0.1611 ± 0.1162

0.1668

Respiratory disease

0.02578 ± 0.2025

0.8988

Other malignancy

−0.06530 ± 0.1852

0.7247

Abdominal operation

−0.05301 ± 0.1207

0.6610

Colectomy

−0.2719 ± 0.2118

0.2003

Cholecystectomy

0.5561 ± 0.2371

0.0198

Abdominal radiation

0.3449 ± 0.4600

0.4541

Diverticulosis

0.08932 ± 0.1019

0.3817

Antithrombotic drugs

0.08197 ± 0.1673

0.6247

Opioids

−0.09589 ± 0.4698

0.8384

Proton pump inhibitors

−0.09242 ± 0.1198

0.4413

Laxative

0.01980 ± 0.1336

0.8823

Time interval

0.001234 ± 0.0005088

0.0016

BBPS

0.01309 ± 0.1088

0.9043

Abbreviations: ASA-PS, American Society of Anesthesiologists-Physical Status; BBPS, Boston Bowel Preparation Scale; BMI, body mass index; ECOG-PS, Eastern Cooperative Oncology Group-Performance Status.


Since the difference between CEBuS-0 and CEBuS-1 is only 5% of bubbles covering the surface, we divided examinees into two groups: CEBuS-0 or 1 group (n = 189) and CEBuS-2 group (n = 125) in the ileocecum or anastomosis. We compared the CEBuS-2 group to the CEBuS-0 and CEBuS-1 groups. The results of the multivariate logistic regression analysis are summarized in [Table 5]. The time interval of colonoscopy (p = 0.033) and a history of cholecystectomy (p = 0.0095) were positively correlated with the CEBuS score.

Table 5

Logistic regression analysis

Coefficients (±std. error)

Odds ratio (95% CI)

p-Value

Age

0.0105 ± 0.0115

1.011 (0.9880–1.033)

0.3624

Sex

0.0342 ± 0.290

1.035 (0.5850–1.830)

0.9064

ASA-PS

−0.385 ± 0.273

0.6803 (0.3984–1.162)

0.1581

ECOG-PS

0.0189 ± 0.433

1.019 (0.4363–2.380)

0.9653

BMI

−0.0351 ± 0.0392

0.9655 (0.8940–1.043)

0.3711

Hypertension

0.116 ± 0.355

1.123 (0.5603–2.252)

0.7434

Diabetes

0.703 ± 0.391

2.020 (0.9387–4.347)

0.0721

Cardiovascular disease

0.209 ± 0.518

1.232 (0.4462–3.403)

0.6870

Cerebrovascular disease

0.136 ± 0.638

1.146 (0.3281–4.000)

0.8313

Renal disease

−0.692 ± 0.673

0.5004 (0.1337–1.873)

0.3039

Liver disease

−0.251 ± 0.992

0.7778 (0.1113–5.437)

0.8001

Dyslipidemia

−0.451 ± 0.362

0.6373 (0.3133–1.296)

0.2136

Respiratory disease

−0.113 ± 0.632

0.8928 (0.2583–3.086)

0.8578

Other malignancy

−0.334 ± 0.575

0.7160 (0.2318–2.212)

0.5615

Abdominal operation

−0.0760 ± 0.368

0.9268 (0.4505–1.907)

0.8363

Colectomy

−0.552 ± 0.677

0.5756 (0.1526–2.170)

0.4146

Cholecystectomy

2.28 ± 0.877

9.735 (1.746–54.29)

0.0095

Abdominal radiation

1.97 ± 1.53

7.184 (0.3590–143.7)

0.1971

Diverticulosis

0.357 ± 0.308

1.430 (0.7820–2.613)

0.2456

Antithrombotic drugs

0.00853 ± 0.538

1.009 (0.3511–2.897)

0.9874

Opioids

−0.226 ± 1.46

0.7974 (0.04552–13.97)

0.8768

Proton pump inhibitors

−0.495 ± 0.375

0.6094 (0.2921–1.271)

0.1866

Laxative

−0.260 ± 0.414

0.7714 (0.3429–1.736)

0.5304

Time interval

0.00329 ± 0.00155

1.003 (1.0003–1.0063)

0.0332

BBPS

0.255 ± 0.340

1.290 (0.6623–2.513)

0.4541

Abbreviations: ASA-PS, American Society of Anesthesiologists-Physical Status; BBPS, Boston Bowel Preparation Scale; BMI, body mass index; CI, confidence interval; ECOG-PS, Eastern Cooperative Oncology Group-Performance Status.


We compared the 25% longer time interval of colonoscopy examinees and the 25% shorter time interval of colonoscopy examinees in terms of CEBuS at ileocecum in [Supplementary Table S4] (available in online version only). The analysis showed that a longer time interval of colonoscopy was significantly associated with a high CEBuS score (p = 0.0137).

Finally, we compared the examinees with less than 240-minute time interval of colonoscopy (<240-minute group) and those with more than 240 minutes (>240-minute group, [Table 6]). The analysis showed that <240-minute group scored lower CEBuS at the ileocecum or anastomosis than >240-minute group.

Table 6

240-minute time interval and Colon Endoscopic Bubble Scale at the ileocecum or anastomosis

0

1

2

Total

<240 min, n (%)

41 (25.9)

65 (41.1)

52 (32.9)

158 (100)

>240 min, n (%)

19 (12.2)

64 (41.0)

73 (46.8)

156 (100)

p = 0.0013


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Discussion

In this study, we confirmed that a longer time interval from the completion of bowel preparation to intubation is positively associated with the severity of air bubbles in the large intestine. Therefore, it is important to promptly perform colonoscopy if bowel preparation is completed.

The American Gastroenterological Association (AGA) stipulates preferred standards for colonoscopy screening.[25] Accordingly, more than 95% of the BBPS scores should be ≥6 points for aspirational quality of bowel preparation. In the present study, the median BBPS score was 9 points, and 99.7% of the examinations scored ≥6 points. The results validated that bowel preparation was performed at an aspirational level. The standards of AGA also refer to the quality of colonoscopy.[25] Aspirational cecal intubation rate is above 95% and withdrawal time is above 9 minutes, and optimal PDR is 30 to 40%.[22] [26] In our study, cecal intubation rate was 99.6%, mean withdrawal time was 13 minutes, and PDR was 52.9%. Our study was also validated in terms of colonoscopy quality.

In the present study, we analyzed the correlation between the CEBuS score at three locations. The correlation of the rectum and transverse colon or splenic flexure, and that of the rectum and ileocecum or anastomosis were low.[27] However, that of the transverse colon or splenic flexure and ileocecum or anastomosis was moderate.[27] Therefore, it is difficult, but not impossible, to estimate the oral side CEBuS from the anal side CEBuS when the colonoscope is intubated.

We found that the time interval of colonoscopy is an important factor for good bubble condition during colonoscopy. One hypothesis is that air bubbles in the large intestine are associated with bile secretion after bowel preparation. Bile is composed of bilirubin, fats, bile acids, and water. Bile is a natural detergent because bile salts contain both polar and nonpolar regions.[28] [29] Therefore, bile can easily form bubbles, which are typically seen in the duodenum. Accordingly, our hypothesis is reinforced by the fact that postcholecystectomy is another correlative factor for severe air bubbles after bowel preparation. Postcholecystectomy, patients cannot store bile during fasting. Constant bile secretion toward the gastrointestinal tract occurs after the completion of bowel preparation. Therefore, it is important to start colonoscopy immediately after the completion of bowel preparation.

Previous reports also pointed out the importance of the time interval between completion of bowel preparation and colonoscopy.[30] [31] These previous reports showed that too-long intervals (≥6 hours or the day prior to the procedure) worsen the quality of bowel preparation. Bowel preparation quality was assessed using the Ottawa Bowel Preparation Scale score[8] or a unique score featuring liquid or solid material. These studies have focused on residual fluid, stool, mucus, and chyme. In our study, we confirmed that air bubbles were also affected by the interval time. In addition, our study suggested that within 240-minute intubation after completion of bowel preparation might be appropriate for PEG-based and simethicone-free regimen.

This study had some limitations. First, this was a retrospective single-center study. Second, we collected stool scores from the self-assessments of the examinees. The timing of a score of 5 in the pamphlets did not have objective reliability, even though the BBPS score in this study was excellent. Third, our method used only PEG as the bowel preparation drug and simethicone was not administered on the day of colonoscopy. Although PEG is a popular bowel preparation drug, it is also known as a nonionic detergent. Simethicone is a safe oral antifoaming drug, and previous reports have shown that simethicone-mixed preparation improves air bubbles and bowel preparation quality.[32] [33] If another regimen was used or simethicone was added to the PEG regimen, the results might have been affected. Fourth, we could not collect the speed of PEG intake from the pamphlets. We could not investigate the association between the CEBuS score and the speed of PEG intake.


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Conclusion

In conclusion, here we analyzed the correlative factors of severity of air bubbles in the large intestine during colonoscopy. We found that the time interval of colonoscopy and cholecystectomy were correlative factors of severe bubbles. Therefore, it is important not to wait long before starting at the reserved time if the bowel preparation is accomplished.


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Conflict of Interest

None declared.

Acknowledgments

We truly appreciate the staff of the Minimally Invasive Center at the Medical Research Institute Kitano Hospital for safety colonoscopy and correction of data.

Authors' Contributions

Conceptualization: T.Y., A.Y.; collection of data: K.I., S.O., Y.S., K.Tanaka, K.N.; data analysis: T.Y., A.Y., Y.M., K.O., R.I., Y.K., S.N., S.A., T.M., K.H., K.K., K.Takahashi, T.Kou, T.Katayama, S.Y.; writing-original draft: T.Y.


Ethics Approval

Opt-out informed consent protocol was used for this study. This consent procedure was reviewed and approved by Kitano Hospital (approval No. 2209004).


Data Availability Statement

The datasets generated and analyzed in the current study are available from the corresponding author on reasonable request.


Supplementary Material

  • References

  • 1 Sung H, Ferlay J, Siegel RL. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71 (03) 209-249
  • 2 Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol 2021; 14 (10) 101174
  • 3 Edwards BK, Ward E, Kohler BA. et al. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 2010; 116 (03) 544-573
  • 4 Zauber AG, Winawer SJ, O'Brien MJ. et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med 2012; 366 (08) 687-696
  • 5 Winawer SJ, Zauber AG, Ho MN. et al; The National Polyp Study Workgroup. Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med 1993; 329 (27) 1977-1981
  • 6 Froehlich F, Wietlisbach V, Gonvers JJ, Burnand B, Vader JP. Impact of colonic cleansing on quality and diagnostic yield of colonoscopy: the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study. Gastrointest Endosc 2005; 61 (03) 378-384
  • 7 Lee HL, Eun CS, Lee OY. et al. Significance of colonoscope length in cecal insertion time. Gastrointest Endosc 2009; 69 (3 Pt 1): 503-508
  • 8 Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest Endosc 2004; 59 (04) 482-486
  • 9 Clark BT, Rustagi T, Laine L. What level of bowel prep quality requires early repeat colonoscopy: systematic review and meta-analysis of the impact of preparation quality on adenoma detection rate. Am J Gastroenterol 2014; 109 (11) 1714-1723 , quiz 1724
  • 10 Clark BT, Laine L. High-quality bowel preparation is required for detection of sessile serrated polyps. Clin Gastroenterol Hepatol 2016; 14 (08) 1155-1162
  • 11 Ness RM, Manam R, Hoen H, Chalasani N. Predictors of inadequate bowel preparation for colonoscopy. Am J Gastroenterol 2001; 96 (06) 1797-1802
  • 12 Mahmood S, Farooqui SM, Madhoun MF. Predictors of inadequate bowel preparation for colonoscopy: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2018; 30 (08) 819-826
  • 13 Matro R, Tupchong K, Daskalakis C, Gordon V, Katz L, Kastenberg D. The effect on colon visualization during colonoscopy of the addition of simethicone to polyethylene glycol-electrolyte solution: a randomized single-blind study. Clin Transl Gastroenterol 2012; 3 (11) e26
  • 14 Yoo IK, Jeen YT, Kang SH. et al. Improving of bowel cleansing effect for polyethylene glycol with ascorbic acid using simethicone: a randomized controlled trial. Medicine (Baltimore) 2016; 95 (28) e4163
  • 15 Mohammad F, Madhoun MH, Ali AA. Higher dose of simethicone decreases colonic bubbles and increases prep tolerance and quality of bowel prep: meta-analysis of randomized controlled trials. World J Metaanal 2019; 31: 10
  • 16 Taveira F, Hassan C, Kaminski MF. et al. The Colon Endoscopic Bubble Scale (CEBuS): a two-phase evaluation study. Endoscopy 2022; 54 (01) 45-51
  • 17 Lai EJ, Calderwood AH, Doros G, Fix OK, Jacobson BC. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc 2009; 69 (3 Pt 2): 620-625
  • 18 Kastenberg D, Bertiger G, Brogadir S. Bowel preparation quality scales for colonoscopy. World J Gastroenterol 2018; 24 (26) 2833-2843
  • 19 Calderwood AH, Jacobson BC. Comprehensive validation of the Boston Bowel Preparation Scale. Gastrointest Endosc 2010; 72 (04) 686-692
  • 20 Rex DK, Schoenfeld PS, Cohen J. et al. Quality indicators for colonoscopy. Gastrointest Endosc 2015; 81 (01) 31-53
  • 21 Baxter NN, Sutradhar R, Forbes SS, Paszat LF, Saskin R, Rabeneck L. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140 (01) 65-72
  • 22 Williams JE, Le TD, Faigel DO. Polypectomy rate as a quality measure for colonoscopy. Gastrointest Endosc 2011; 73 (03) 498-506
  • 23 Francis DL, Rodriguez-Correa DT, Buchner A, Harewood GC, Wallace M. Application of a conversion factor to estimate the adenoma detection rate from the polyp detection rate. Gastrointest Endosc 2011; 73 (03) 493-497
  • 24 Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013; 48 (03) 452-458
  • 25 Keswani RN, Crockett SD, Calderwood AH. AGA clinical practice update on strategies to improve quality of screening and surveillance colonoscopy: expert review. Gastroenterology 2021; 161 (02) 701-711
  • 26 Williams JE, Holub JL, Faigel DO. Polypectomy rate is a valid quality measure for colonoscopy: results from a national endoscopy database. Gastrointest Endosc 2012; 75 (03) 576-582
  • 27 Mukaka MM. Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J 2012; 24 (03) 69-71
  • 28 Hofmann AF, Small DM. Detergent properties of bile salts: correlation with physiological function. Annu Rev Med 1967; 18: 333-376
  • 29 Camilleri M. Bile acid detergency: permeability, inflammation, and effects of sulfation. Am J Physiol Gastrointest Liver Physiol 2022; 322 (05) G480-G488
  • 30 Kim TK, Kim HW, Kim SJ. et al. Importance of the time interval between bowel preparation and colonoscopy in determining the quality of bowel preparation for full-dose polyethylene glycol preparation. Gut Liver 2014; 8 (06) 625-631
  • 31 Parra-Blanco A, Nicolas-Perez D, Gimeno-Garcia A. et al. The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study. World J Gastroenterol 2006; 12 (38) 6161-6166
  • 32 Yeh JH, Hsu MH, Tseng CM. et al. The benefit of adding oral simethicone in bowel preparation regimen for the detection of colon adenoma: a systematic review and meta-analysis. J Gastroenterol Hepatol 2019; 34 (05) 830-836
  • 33 Tongprasert S, Sobhonslidsuk A, Rattanasiri S. Improving quality of colonoscopy by adding simethicone to sodium phosphate bowel preparation. World J Gastroenterol 2009; 15 (24) 3032-3037

Address for correspondence

Takaaki Yoshikawa, MD, PhD
Department of Gastroenterology and Hepatology, Medical Research Institute Kitano Hospital
PIIF Tazuke-Kofukai, 2-4-20, Ohgimachi, Kita-ku, Osaka 530-8480
Japan   

Publication History

Article published online:
02 April 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Sung H, Ferlay J, Siegel RL. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021; 71 (03) 209-249
  • 2 Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol 2021; 14 (10) 101174
  • 3 Edwards BK, Ward E, Kohler BA. et al. Annual report to the nation on the status of cancer, 1975-2006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates. Cancer 2010; 116 (03) 544-573
  • 4 Zauber AG, Winawer SJ, O'Brien MJ. et al. Colonoscopic polypectomy and long-term prevention of colorectal-cancer deaths. N Engl J Med 2012; 366 (08) 687-696
  • 5 Winawer SJ, Zauber AG, Ho MN. et al; The National Polyp Study Workgroup. Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med 1993; 329 (27) 1977-1981
  • 6 Froehlich F, Wietlisbach V, Gonvers JJ, Burnand B, Vader JP. Impact of colonic cleansing on quality and diagnostic yield of colonoscopy: the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study. Gastrointest Endosc 2005; 61 (03) 378-384
  • 7 Lee HL, Eun CS, Lee OY. et al. Significance of colonoscope length in cecal insertion time. Gastrointest Endosc 2009; 69 (3 Pt 1): 503-508
  • 8 Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest Endosc 2004; 59 (04) 482-486
  • 9 Clark BT, Rustagi T, Laine L. What level of bowel prep quality requires early repeat colonoscopy: systematic review and meta-analysis of the impact of preparation quality on adenoma detection rate. Am J Gastroenterol 2014; 109 (11) 1714-1723 , quiz 1724
  • 10 Clark BT, Laine L. High-quality bowel preparation is required for detection of sessile serrated polyps. Clin Gastroenterol Hepatol 2016; 14 (08) 1155-1162
  • 11 Ness RM, Manam R, Hoen H, Chalasani N. Predictors of inadequate bowel preparation for colonoscopy. Am J Gastroenterol 2001; 96 (06) 1797-1802
  • 12 Mahmood S, Farooqui SM, Madhoun MF. Predictors of inadequate bowel preparation for colonoscopy: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 2018; 30 (08) 819-826
  • 13 Matro R, Tupchong K, Daskalakis C, Gordon V, Katz L, Kastenberg D. The effect on colon visualization during colonoscopy of the addition of simethicone to polyethylene glycol-electrolyte solution: a randomized single-blind study. Clin Transl Gastroenterol 2012; 3 (11) e26
  • 14 Yoo IK, Jeen YT, Kang SH. et al. Improving of bowel cleansing effect for polyethylene glycol with ascorbic acid using simethicone: a randomized controlled trial. Medicine (Baltimore) 2016; 95 (28) e4163
  • 15 Mohammad F, Madhoun MH, Ali AA. Higher dose of simethicone decreases colonic bubbles and increases prep tolerance and quality of bowel prep: meta-analysis of randomized controlled trials. World J Metaanal 2019; 31: 10
  • 16 Taveira F, Hassan C, Kaminski MF. et al. The Colon Endoscopic Bubble Scale (CEBuS): a two-phase evaluation study. Endoscopy 2022; 54 (01) 45-51
  • 17 Lai EJ, Calderwood AH, Doros G, Fix OK, Jacobson BC. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc 2009; 69 (3 Pt 2): 620-625
  • 18 Kastenberg D, Bertiger G, Brogadir S. Bowel preparation quality scales for colonoscopy. World J Gastroenterol 2018; 24 (26) 2833-2843
  • 19 Calderwood AH, Jacobson BC. Comprehensive validation of the Boston Bowel Preparation Scale. Gastrointest Endosc 2010; 72 (04) 686-692
  • 20 Rex DK, Schoenfeld PS, Cohen J. et al. Quality indicators for colonoscopy. Gastrointest Endosc 2015; 81 (01) 31-53
  • 21 Baxter NN, Sutradhar R, Forbes SS, Paszat LF, Saskin R, Rabeneck L. Analysis of administrative data finds endoscopist quality measures associated with postcolonoscopy colorectal cancer. Gastroenterology 2011; 140 (01) 65-72
  • 22 Williams JE, Le TD, Faigel DO. Polypectomy rate as a quality measure for colonoscopy. Gastrointest Endosc 2011; 73 (03) 498-506
  • 23 Francis DL, Rodriguez-Correa DT, Buchner A, Harewood GC, Wallace M. Application of a conversion factor to estimate the adenoma detection rate from the polyp detection rate. Gastrointest Endosc 2011; 73 (03) 493-497
  • 24 Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013; 48 (03) 452-458
  • 25 Keswani RN, Crockett SD, Calderwood AH. AGA clinical practice update on strategies to improve quality of screening and surveillance colonoscopy: expert review. Gastroenterology 2021; 161 (02) 701-711
  • 26 Williams JE, Holub JL, Faigel DO. Polypectomy rate is a valid quality measure for colonoscopy: results from a national endoscopy database. Gastrointest Endosc 2012; 75 (03) 576-582
  • 27 Mukaka MM. Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med J 2012; 24 (03) 69-71
  • 28 Hofmann AF, Small DM. Detergent properties of bile salts: correlation with physiological function. Annu Rev Med 1967; 18: 333-376
  • 29 Camilleri M. Bile acid detergency: permeability, inflammation, and effects of sulfation. Am J Physiol Gastrointest Liver Physiol 2022; 322 (05) G480-G488
  • 30 Kim TK, Kim HW, Kim SJ. et al. Importance of the time interval between bowel preparation and colonoscopy in determining the quality of bowel preparation for full-dose polyethylene glycol preparation. Gut Liver 2014; 8 (06) 625-631
  • 31 Parra-Blanco A, Nicolas-Perez D, Gimeno-Garcia A. et al. The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study. World J Gastroenterol 2006; 12 (38) 6161-6166
  • 32 Yeh JH, Hsu MH, Tseng CM. et al. The benefit of adding oral simethicone in bowel preparation regimen for the detection of colon adenoma: a systematic review and meta-analysis. J Gastroenterol Hepatol 2019; 34 (05) 830-836
  • 33 Tongprasert S, Sobhonslidsuk A, Rattanasiri S. Improving quality of colonoscopy by adding simethicone to sodium phosphate bowel preparation. World J Gastroenterol 2009; 15 (24) 3032-3037

Zoom Image
Fig. 1 The flowchart of enrollment and selection of examinees in this study.
Zoom Image
Fig. 2 The single linear regression analysis of CEBuS and the time interval between the time when examinees scored 5 on the preparation in the pamphlets and the time when colonoscopy reached the cecum or anastomosis. CEBuS, Colon Endoscopic Bubble Scale.