Scandinavian Journal of Gastroenterology. 2014; 49: 485–491
ORIGINAL ARTICLE
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Can nutritional supplements and rectal enema be used as bowel cleansing for colonoscopy? – results of a randomized controlled pilot study
ULF O. GUSTAFSSON1, JOSEFIN SEGELMAN2, OLLE LJUNGQVIST3, ANDERS THORELL1 & JONAS NYGREN1 1
Department of surgery, Ersta Hospital & Department of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, Sweden, 2Department of Surgery, Ersta Hospital & Department of Molecular Medicine and Surgery, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden, and 3Department of Surgery, Örebro University and University Hospital, Örebro & Inst. of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
Abstract Objective. Currently available preparations for colonoscopy have low tolerability and may cause fluid and electrolyte shifts. An alternative method of bowel cleansing is required. Material and methods. Preparation of the gut using oral nutritional supplements (ONS) and rectal enema was tested as an alternative method of bowel cleansing. During 2008–2012, patients were randomized to oral nutritional supplements (n = 27) for 5 days and rectal enema or polyethylene glycol (PEG) (n = 23) prior to colonoscopy. Blinded endoscopists rated the degree of bowel cleansing according to the Ottawa bowel preparation scale (OBS) (primary outcome). Tolerability of either preparation was also assessed (ClinicalTrials.gov. Identifier no: NCT00123456). Results. Due to a high rate of bowel cleansing failure among patients receiving ONS, the study was interrupted prematurely. Colonoscopies were incomplete due to stools in 6 of 27 patients in the ONS group compared to 1 of 23 in the PEG group (ns). The mean total OBS were 8.3 ± 3.3 and 5.3 ± 2.8, respectively (p = 0.002). Four patients (15%) in the ONS group and eight patients (35%) receiving PEG had an OBS score £4 (good preparation) (ns). ONS was better tolerated than PEG with more patients reporting acceptable taste (27 of 27 [100%] vs. 15 of 23 [65%], p = 0.001), and fewer reporting difficulties with the intake (0 of 27 [0%] vs. 10 of 23 [43%], p < 0.001) and nausea (5 of 27 [19%] vs. 13 of 23 [57%], p < 0.008). Conclusions. For routine use, ONS with enema instead of traditional preparation for colonoscopy with PEG cannot be generally recommended.
Key Words: Bowel preparation, colonoscopy, nutritional drinks
Introduction The rate of endoscopic investigations used for detecting various colonic conditions is increasing in quantity worldwide. In some countries, the proportion of individuals aged ‡50 years who have undergone colonoscopy for cancer screening exceeds 60% [1]. A clean bowel is crucial for the efficacy of such clinical investigations [2]. The ideal preparation for colonoscopy should reliably empty the colon and avoid causing
discomfort or shifts in fluids or electrolytes. Unfortunately, none of the currently available preparations meet all of these requirements. Currently, the two predominant preparations for colonoscopy, oral sodium phosphate (OSP) and polyethylene glycol (PEG), have been shown equally effective in terms of bowel cleansing [3,4]. However, preparation with OSP can cause significant fluid and electrolyte shifts and should be used with caution in patients with heart and renal failure [5,6]. In addition,
Correspondence: Ulf Gustafsson, MD PHD, Department of surgery, Ersta Hospital & Department of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Centre for Gastrointestinal Disease, 116 91, Box 4622 Stockholm, Sweden. Tel: +46 8 7146582. Fax: +4687146665. E-mail: [email protected]
(Received 8 January 2014; accepted 19 January 2014) ISSN 0036-5521 print/ISSN 1502-7708 online 2014 Informa Healthcare DOI: 10.3109/00365521.2014.886720
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the patient tolerability of PEG is generally low. Some studies report a 40% failure of ingesting the full dose of prescribed preparation [7]. Colonoscopy is sometimes indicated in older patients who may have a poor compliance for the intake of the bowel preparation and may suffer from heart and renal disease. Therefore, a more tolerable bowel preparation with less severe side effects is desirable. Further, in rectal cancer, patients are currently preoperatively prepared with traditional bowel cleansing, which is proven harmful in colonic surgery [8]. A new preparation without risk of side effects would provide a clean colon, thus minimizing potential anastomotic problems. Low-fiber diet in addition to traditional preparation has been shown beneficial in bowel cleansing for colonoscopy [9–11]. Further, one study reports that a 7-day preoperative low-fiber diet alone provides similar quality of surgical field exposure as traditional preparation [12]. However, no studies have evaluated a low-fiber diet without concurrent traditional preparation as an alternative method of bowel cleansing for colonoscopy. This single-blinded, randomized controlled pilot study compares the degree of bowel cleansing and tolerability between oral nutritional supplements (ONS) and PEG. The aim was to evaluate if ONS can be used as an alternative choice in preparing patients for colonoscopy. Material and methods A feasibility study, conducted before the current study, included seven patients and showed a high degree of bowel cleansing with the use of nutritional supplements prior to colonoscopy. The research protocol was approved by the Karolinska Institute Ethics Committee and carried out in accordance with the Declaration of Helsinki of the World Association (1989) (clinical trial number: NCT00675324, www.clinicaltrials.gov). Patients between the age of 18 and 90 years referred for elective colonoscopy to Ersta Hospital, Stockholm, Sweden, were considered for inclusion in the study. Patients with a known history of diabetes, acute colitis, acute ileus, ostomy and those unable to comply with the study protocol (owing to psychiatric disease, dementia and/or limited ability to understand Swedish) were not eligible. Due to a high level of workload at the clinic and several other concurrent studies, the inclusion rate was slower than expected. Between April 2008 and February 2012, 53 patients aged 38–80 years were included in the study. Computer-generated randomization was conducted to assign patients to either ONS (Fresubin)
(29 patients) or PEG (Laxabon) (24 patients), with allocation concealment maintained by the use of consecutively numbered sealed envelopes. Three patients were excluded after randomization: two in the ONS arm (one who misunderstood the study protocol and had full meals and one who refused colonoscopy due to anal pain), and one in the PEG arm, due to high international normalized ratio (Figure 1). An interim analysis in February 2009 showed unsatisfactory bowel cleansing in patients randomized to ONS. Therefore, in the last 8 of the 27 subjects in the ONS group, the protocol was modified to additional treatment with oral macrogol (Forlax), 10 g, twice daily for 5 days. Due to an assumed continuous failure of cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, the study was interrupted ahead of protocol in February 2012.
Study design Patients were randomized to one of two study arms: (1) ONS only, fiber-free (Fresubin, energy drink) 200 ml/bottle; 1, 5 kcal/ml (protein 5, 6 g; carbohydrates 18, 8 g; fat 5, 8 g), 30 kcal/kg bodyweight/day, for 5 days. Rectal enema, Klyx (1 mg/ml docusate sodium, 250 mg/ml sorbitol) 240 ml was administered the day before and on the same morning as the planned colonoscopy. Additional clear fluids were allowed ad libitum. (2) PEG (Laxabon), 4 l solution, 2 l (2–3 p.m.), 2 l (6–7 p.m.) after a light breakfast, single soup for lunch followed by clear fluids only, the day prior to colonoscopy. From 9 p.m. on the day prior to colonoscopy, only clear fluids were allowed and from midnight all patients were fasting regardless of study arm. All endoscopic investigations were carried out between 8–10 a.m. in the morning. Before the investigation, patients were requested to fill in a bowel symptoms questionnaire (selected questions, Rome III criteria’s) and a feces form and frequency questionnaire (modified Bristol scale) [13] and after investigation, patients were requested to fill a Patient Acceptance Questionnaire. Blood samples were taken before and after investigation. All colonoscopic investigations were conducted by four highly experienced endoscopists blinded to study arm allocation. A calibration exercise ensured that the endoscopists understood and agreed on the rating of bowel preparation using the Ottawa bowel preparation scale [14]. In addition to the rating, the endoscopists were requested to decide whether a new colonoscopy was required or not.
Bowel preparation and nutritional drinks
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Assessed for eligibility n = 93 Excluded n = 40 Did not meet inclusion criteria n = 6 Refused to participate n = 16 Other reasons n = 18
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Randomized n = 53 1:1 (ONS: PEG)
Allocated to ONS n = 29 Received intervention n = 27 Did not receive intervention n = 2 -No colonoscopy, full meals n = 1 -No colonoscopy, anal pain n = 1
Lost to follow-up n = 0
Allocated to PEG n = 24 Received intervention n = 23 Did not receive intervention n =1 -No colonoscopy due to high international normalized ratio (INR) n = 1
Lost to follow-up n = 0
Analysed n = 27
Analysed n = 23
Figure1. Study flow chart is shown. ONS = Oral nutritional supplements. PEG = Polyethylene glycol.
The Ottawa scale was used to rate the level of bowel cleansing in the right-, mid-, and recto-sigmoid colon on a 5-point scale (0–4). Further, the scale rates a global 3-point rating for overall colonic fluid (0–2). Thus, the total score ranges from 0 to 14. A score 0 to 1 is considered an excellent preparation, 2 to 4 a good preparation, whereas scores >4 indicate progressively worsening bowel preparation. A score between 11 and14 indicates a completely unprepared colon depending on the amount of colonic fluid [15]. Statistical analysis We were not aware of any preexisting data available on ONS preparation for colonoscopy. The power analysis was made on an estimated least detectable difference in bowel cleansing of 25% in favor of PEG. With 80% power at a two-sided alpha of 0.05, the number of patients needed to treat was estimated to be 65 in each group. Results are presented as mean (SD) and rate (%). Shapiro–Wilk’s testing for normal distribution was conducted. Two-tailed t-test of unequal variance was used for crude comparisons of normally distributed continuous variables. Non-parametric Wilcoxon
rank-sum test was used for categorical variables and continuous data without normal distribution. A score £4 is considered a good bowel cleansing. However, in order to find possible common variables in patients receiving ONS resulting in acceptable (score £5) compared to unacceptable (score >5) bowel cleansing, adjusted comparisons with logistic regression was used. Between groups comparisons of laboratory data were analyzed using paired t-test and signed-rank test. The eight patients in the ONS group receiving additional treatment with orally administrated macrogol were analyzed together with all ONS patients, if not particularly specified. A p-Value of < 0.05 was considered statistically significant. All data were analyzed using Stata version 12 (Stata Corporation, Collage Station, Texas, USA). Results With the exception of a higher rate of morbidity (fewer American Society of Anesthesiologists (ASA) physical status 1) in patients receiving ONS, p = 0.029, there were no significant differences in basic characteristics in patients randomized to ONS (n = 27) and PEG
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(n = 23), respectively. No differences between groups with regard to self-reported pre-preparation bowel evacuation, defecations/week or Bristol classification were found (Table I).
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Tolerability Among patients receiving ONS, 22 of 27 (81%) had complete intake of prescribed nutrition drinks (mean total number of bottles 36.4 ± 8.5 SD). Nineteen patients (83%) receiving PEG had a full dose of 4 l of PEG, whereas the remaining four patients (17%) had a total intake of 3 l. Of the 27 patients in the ONS group, 26 were treated with rectal enema. A significantly higher rate of patients receiving ONS found the taste of the preparation acceptable (27 of 27 (100%) vs. 15 of 23 (65%), p = 0.001) and fewer patients reported difficulties with intake of the preparation (0 of 27 (0%) vs. 10 of 23 (43%), p < 0.001) and nausea (5 of 27 (19%) vs. 13 of 23 (27%), p = 0.008), compared with patients receiving PEG. A total of 23 patients (85%) in the ONS group and 17 (74%) in the PEG group would consider to undergo the same bowel preparation again (Table II). Laboratory data Within groups, a mean decrease in plasma-potassium, S-Ca2+, and plasma-chloride compared to the preTable I. Patient characteristics.
Age, mean, SD BMI, mean, SD Gender (M/F) ASA1 ASA2 ASA3 Systemic disease Previous colonoscopy Previous abdominal surgery Previous colonic resection Defecations/week Bristol classification Incomplete evacuation Indication: bleeding Indication: control Indication: pain Indication: bowel habits Indication: heredity
ONS (n = 27)
PEG (n = 23)
p
60.8 ± 11.1 26.4 ± 3.8 11/16 13 13 1 14(51.9) 17(63.0) 12(44.7)
61.1 ± 11.0 24.7 ± 4.3 11/12 18 5 0 6(26) 14(60.9) 8(34.8)
0.910a 0.139a 0.615b 0.029b 0.053b 1.000m 0.064b 0.829b 0.487b
6(22.2)
6(26.1)
0.750b
12.9 ± 8.4 4.0 ± 1.2 8(29.6) 10 11 2 3 1
14.3 ± 10.8 4.2 ± 4.2 8(34.8) 9 10 2 2 0
0.732$ 0.494$ 0.697b 0.879b 0.845b 1.000m 1.000m 1.000m
Abbreviations: ASA = American Society of Anesthesiologists physical status; BMI = body mass index; Bristol classification: (1–7), 1 = Separate hard lumps, 7 = fluid only. Incomplete evacuation = self-reported status; a = Two tailed t-test; b =Pearson’s c2 test; $ = Wilcoxon rank-sum test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise.
preparation baseline in patients receiving ONS and PEG was statistically significant, p < 0.05. Also, an increase in plasma-urea and plasma-creatinine among patients receiving ONS and the decrease in plasmaalbumin and plasma-urea among patients receiving PEG was significant, p < 0.05. However, all values were still within a normal reference interval. Between groups, only a difference between the enhanced plasma-urea among patients in the ONS group and a decreased plasma-urea in the PEG group was statistically significant, p < 0.0001, however without clinical importance (data not shown). Quality of the bowel preparation Among patients receiving ONS, 6 of 27 (22%) of the investigations cecum could not be intubated due to stools versus 1 of 23 (4%) in the PEG group (ns). Thus, cecum could be intubated in the majority of patients receiving ONS. There was a need for new colonoscopy (i.e. to exclude minor lesions) in 15 of 27 (55 %) and 1 of 23 (4%) patients in the ONS and PEG arms, respectively, p < 0.001 (Table III). The mean total Ottawa preparation scores were 8.3 ± 3.3 in the ONS group compared with 5.3 ± 2.8 in the PEG group, p = 0.002 (Figure 2). The right colon and the transverse colon/descendens was significantly more difficult to clean in the ONS group compared to the PEG group, whereas no significant difference was found in the recto-sigmoid colon between groups. Less fluid in the colon was found among patients receiving ONS compared to PEG. Four patients (15%) in the ONS group and eight patients (35%) receiving PEG had an Ottawa bowel score (OBS) score £4 (ns) (Table III). In a subanalysis of the eight patients in the ONS group who received additional treatment with a low dose of oral macrogol, the mean total OBS score was 8.3 ± 3.1 (SD) versus 8.3 ± 3.5 (SD) in patients without additional treatment. There was neither a difference in OBS score of separate parts of colon between these two groups. In multivariate analysis, no common variables were found in patients receiving ONS resulting in acceptable (score £5) compared to unacceptable (score >5) bowel cleansing. Discussion Due to failure of bowel cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, this single-blinded, randomized controlled study was prematurely interrupted at a pilot stage. Additional treatment with a low-dose oral macrogol did not seem to substantially improve the degree of bowel cleansing. Although patients
Bowel preparation and nutritional drinks
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Table II. Compliance to preparation.
Full intake of prescribed bowel preparation Treatment with prescribed enema Acceptable taste of preparation Difficulty in taking preparation Off work precluding colonoscopy Nausea Regurgitation Abdominal pain Need for help with bowel preparation Would consider same bowel preparation
ONS (n = 27
PEG (n = 23)
22(81.5)
19(82.6)
26(96.3)
p 0.974b
0
27(100)
15(65.2)
0.001b
0(0)
10(43.5)
< 0.001m
4*(30.8)
7**(63.6)
0.217m
5(18.5) 0(0) 5(18.5) 3(11.1)
13(56.5) 1(4.3) 9(39.1) 1(4.3)
0.008m 0.460m 0.126m 0.614m
23(85.2)
17(73.9)
0.480m
Abbreviations: b = Pearson’s c2 test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise. *n = 13; **n = 11.
receiving ONS showed a high rate of tolerability for the preparation, only 15% had an OBS score £4 (good preparation), and in 55% of the patients a new colonoscopy was considered required (i.e. to exclude minor lesions). The OBS [14] is a validated tool for evaluating quality of bowel preparation. Previous studies reporting OBS score using PEG preparation have shown a mean total score between 3.2 and 5.2 [15–17]. In the current study, the mean total OBS score in patients receiving PEG was 5.3 and only 35% of the patients had a score £4. This indicates that the majority of patients in the group with traditional preparation (PEG) had an unsatisfactory bowel preparation. These results could in part be explained by the fact Table III. Primary outcome.
Duration of colonoscopy, mean, min Incomplete colonoscopy (stools) Right colon OBS (0–4) Transverse colon/descendens OBS (0–4) Rectosigmoid colon OBS (0–4) Fluid in colon OBS (0–2) Total score OBS (0–14) OBS score £4 OBS score £5 New colonoscopy required
ONS (n = 27)
PEG (n = 23)
33 ± 13
35 ± 15
0.937$
1(4.3)
< 0.107m
3.7 ± 0.5 3.0 ± 1.3
1.8 ± 0.9 1.3 ± 0.9
< 0.001$ < 0.001$
1.4 ± 1.4
1.3 ± 1.0
0.800$
0.4 ± 0.6 8.3 ± 3.3 4(14.8) 7(25.9) 15(55.5)
0.8 ± 0.7 5.3 ± 2.8 8(34.8) 10(43.5) 1(4.3)
0.034$ 0.002$ 0.183m 0.192m < 0.001m
6(22.2)
p
Abbreviations: OBS = Ottawa bowel score; $ = Wilcoxon rank-sum test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise.
489
that our patients received PEG in a single-dose regimen instead of a split-dose regimen, which is proven favorable in some studies [18]. However, the current data suggest that PEG (at least in a single-dose regimen), the only recommended preparation in patients with heart and renal failure [19], is insufficient in bowel cleansing before colonoscopy in a substantial proportion of patients. In addition to the failing efficacy of PEG, the discomfort and inconvenience associated with ingesting the required 4-l fluid regimen calls for new alternative ways of preparing the bowel for colonoscopy. Particularly, in the view of an increasingly old population with concurrent diseases and possibly wider indications for participation in screening programs, tolerability to the bowel preparation may affect the acceptability and inclusion of these patients [20]. In addition, development of minimally invasive surgical techniques and perioperative care allow surgical treatment also in the very frail patients, and thus screening for colorectal malignancy in this group of patients should be performed with as little risk and discomfort as possible. There were several reasons for investigating the effect of ONS and rectal enema as an alternative method of preparation. First, as shown in the current study, the tolerability of ONS is good and would allow the patient to work or continue social activities until the day of colonoscopy. Second, ONS in combination with PEG has shown improved bowel cleansing compared with PEG alone [9,11] or with a clear liquid diet [21]. Also, in one previous study, similar quality of surgical field exposure as traditional preparation was reported after ONS [12], indicating that practice of this new regimen in rectal cancer surgery may allow bowel cleansing without side effects along with a clean bowel that may reduce risks of morbidity associated with anastomotic leakage. Although, the current study showed failure of bowel cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, 26% had an acceptable OBS score (£5). Further, intubation of cecum could be obtained in 78% of patients receiving ONS. Despite this, ONS may not be recommended in old and/or seriously ill patients who cannot be expected to tolerate traditional preparation for colonoscopy, since complications caused by a colonoscopic procedure in an unclean colon may be deleterious in these fragile patients. However, the use of ONS in rectal cancer surgery should be explored more closely. In summary, ONS is a procedure with high tolerability and compliance that allow intubation of cecum in the majority of patients. ONS cannot be recommended in general due to limited visibility in the right colon in 50% of the patients, with an expected
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4 3.5
p < 0.001
OBS-score
3 2.5 p = 0.800
2 1.5
ONS PEG
1 0.5 0
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Right
Trsv-desc
Recto-Sigm
Figure 2. OBS: differences in right colon, transverse/descendant colon and recto-sigmoidal colon between ONS and PEG, respectively are shown. The difference in total score between ONS, mean SD = 8.3 ± 3.3, and PEG, mean SD = 5.3 ± 2.8, was significant (p = 0.002). Total score range from 0 to 14). Score 0–1 is considered an excellent preparation, 2–4 is considered a good preparation, whereas scores >4 indicates progressively worsening bowel preparations. A score of 11–14 equals a completely unprepared colon depending on the amount of colonic fluid.
reduced detection rate of minor lesions. However, other fields of application, such as in rectal cancer surgery, remain to be studied.
Acknowledgments The authors express their gratitude to Lars-Erik Ahlgren, Gunilla Nyström Strand, Ann-Sofie Andersson, Anette Bratt, Monica Johansson, and Nina Blomme for excellent nursing and technical assistance. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This work (design and conduct of the study; collection, management, analysis and interpretation of the data; preparation, review, and approval of the manuscript) was supported by funds from the Swedish Research Council (#09101), Stockholm County Council (SLL), Hans Mellström, Sweden, and Familjen Erling-Persson’s Foundation.
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[4] Belsey J, Epstein O, Heresbach D. Systematic review: oral bowel preparation for colonoscopy. Aliment Pharmacol Ther 2007;25:373–84. [5] Curran MP, Plosker GL. Oral sodium phosphate solution: a review of its use as a colorectal cleanser. Drugs 2004;64: 1697–714. [6] Wexner SD, Beck DE, Baron TH, Fanelli RD, Hyman N, Shen B, et al. A consensus document on bowel preparation before colonoscopy: prepared by a task force from the American Society of Colon and Rectal Surgeons (ASCRS), the American Society for Gastrointestinal Endoscopy (ASGE), and the Society of American Gastrointestinal and Endoscopic Surgeons (SAGES). Surg Endosc 2006;20:1147–60. [7] Kastenberg D, Barish C, Burack H, Dalke DD, Duckor S, Putnam W, et al. Tolerability and patient acceptance of sodium phosphate tablets compared with 4-L PEG solution in colon cleansing: combined results of 2 identically designed, randomized, controlled, parallel group, multicenter phase 3 trials. J Clin Gastroenterol 2007;41:54–61. [8] Holte K, Nielsen KG, Madsen JL, Kehlet H. Physiologic effects of bowel preparation. Dis Colon Rectum 2004;47: 1397–402. [9] Adams WJ, Meagher AP, Lubowski DZ, King DW. Bisacodyl reduces the volume of polyethylene glycol solution required for bowel preparation. Dis Colon Rectum 1994; 37:229–33; discussion 33-4. [10] Melicharkova A, Flemming J, Vanner S, Hookey L. A lowresidue breakfast improves patient tolerance without impacting quality of low-volume colon cleansing prior to colonoscopy: a randomized trial. Am J Gastroenterol 2013;108: 1551–5. [11] Wu KL, Rayner CK, Chuah SK, Chiu KW, Lu CC, Chiu YC. Impact of low-residue diet on bowel preparation for colonoscopy. Dis Colon Rectum 2011;54:107–12. [12] Lijoi D, Ferrero S, Mistrangelo E, Casa ID, Crosa M, Remorgida V, et al. Bowel preparation before laparoscopic gynaecological surgery in benign conditions using a 1-week low fibre diet: a surgeon blind, randomized and controlled trial. Arch Gynecol Obstet 2009;280:713–18. [13] Heaton KW, Radvan J, Cripps H, Mountford RA, Braddon FE, Hughes AO. Defecation frequency and timing, and stool form in the general population: a prospective study. Gut 1992;33:818–24. [14] Rostom A, Jolicoeur E. Validation of a new scale for the assessment of bowel preparation quality. Gastrointest Endosc 2004;59:482–6. [15] Rostom A, Jolicoeur E, Dube C, Gregoire S, Patel D, Saloojee N, et al. A randomized prospective trial comparing different regimens of oral sodium phosphate and polyethylene glycol-based lavage solution in the preparation of patients for colonoscopy. Gastrointest Endosc 2006;64:544–52. [16] Cesaro P, Hassan C, Spada C, Petruzziello L, Vitale G, Costamagna G. A new low-volume isosmotic polyethylene glycol solution plus bisacodyl versus split-dose 4 L polyethylene glycol for bowel cleansing prior to colonoscopy: a randomised controlled trial. Dig Liver Dis 2013;45:23–7. [17] Kim HJ, Kim TO, Shin BC, Woo JG, Seo EH, Joo HR, et al. Efficacy of prokinetics with a split-dose of polyethylene glycol in bowel preparation for morning colonoscopy: a randomized controlled trial. Digestion 2012;86:194–200. [18] Kilgore TW, Abdinoor AA, Szary NM, Schowengerdt SW, Yust JB, Choudhary A, et al. Bowel preparation with splitdose polyethylene glycol before colonoscopy: a meta-analysis of randomized controlled trials. Gastrointest Endosc 2011; 73:1240–5.
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[19] Hassan C, Bretthauer M, Kaminski MF, Polkowski M, Rembacken B, Saunders B, et al. Bowel preparation for colonoscopy: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy 2013;45: 142–50. [20] Senore C, Ederle A, Fantin A, Andreoni B, Bisanti L, Grazzini G, et al. Acceptability and side-effects of
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ORIGINAL ARTICLE
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Can nutritional supplements and rectal enema be used as bowel cleansing for colonoscopy? – results of a randomized controlled pilot study
ULF O. GUSTAFSSON1, JOSEFIN SEGELMAN2, OLLE LJUNGQVIST3, ANDERS THORELL1 & JONAS NYGREN1 1
Department of surgery, Ersta Hospital & Department of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Stockholm, Sweden, 2Department of Surgery, Ersta Hospital & Department of Molecular Medicine and Surgery, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden, and 3Department of Surgery, Örebro University and University Hospital, Örebro & Inst. of Molecular Medicine and Surgery, Karolinska Institutet, Stockholm, Sweden
Abstract Objective. Currently available preparations for colonoscopy have low tolerability and may cause fluid and electrolyte shifts. An alternative method of bowel cleansing is required. Material and methods. Preparation of the gut using oral nutritional supplements (ONS) and rectal enema was tested as an alternative method of bowel cleansing. During 2008–2012, patients were randomized to oral nutritional supplements (n = 27) for 5 days and rectal enema or polyethylene glycol (PEG) (n = 23) prior to colonoscopy. Blinded endoscopists rated the degree of bowel cleansing according to the Ottawa bowel preparation scale (OBS) (primary outcome). Tolerability of either preparation was also assessed (ClinicalTrials.gov. Identifier no: NCT00123456). Results. Due to a high rate of bowel cleansing failure among patients receiving ONS, the study was interrupted prematurely. Colonoscopies were incomplete due to stools in 6 of 27 patients in the ONS group compared to 1 of 23 in the PEG group (ns). The mean total OBS were 8.3 ± 3.3 and 5.3 ± 2.8, respectively (p = 0.002). Four patients (15%) in the ONS group and eight patients (35%) receiving PEG had an OBS score £4 (good preparation) (ns). ONS was better tolerated than PEG with more patients reporting acceptable taste (27 of 27 [100%] vs. 15 of 23 [65%], p = 0.001), and fewer reporting difficulties with the intake (0 of 27 [0%] vs. 10 of 23 [43%], p < 0.001) and nausea (5 of 27 [19%] vs. 13 of 23 [57%], p < 0.008). Conclusions. For routine use, ONS with enema instead of traditional preparation for colonoscopy with PEG cannot be generally recommended.
Key Words: Bowel preparation, colonoscopy, nutritional drinks
Introduction The rate of endoscopic investigations used for detecting various colonic conditions is increasing in quantity worldwide. In some countries, the proportion of individuals aged ‡50 years who have undergone colonoscopy for cancer screening exceeds 60% [1]. A clean bowel is crucial for the efficacy of such clinical investigations [2]. The ideal preparation for colonoscopy should reliably empty the colon and avoid causing
discomfort or shifts in fluids or electrolytes. Unfortunately, none of the currently available preparations meet all of these requirements. Currently, the two predominant preparations for colonoscopy, oral sodium phosphate (OSP) and polyethylene glycol (PEG), have been shown equally effective in terms of bowel cleansing [3,4]. However, preparation with OSP can cause significant fluid and electrolyte shifts and should be used with caution in patients with heart and renal failure [5,6]. In addition,
Correspondence: Ulf Gustafsson, MD PHD, Department of surgery, Ersta Hospital & Department of Clinical Sciences, Danderyd Hospital, Karolinska Institutet, Centre for Gastrointestinal Disease, 116 91, Box 4622 Stockholm, Sweden. Tel: +46 8 7146582. Fax: +4687146665. E-mail: [email protected]
(Received 8 January 2014; accepted 19 January 2014) ISSN 0036-5521 print/ISSN 1502-7708 online 2014 Informa Healthcare DOI: 10.3109/00365521.2014.886720
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the patient tolerability of PEG is generally low. Some studies report a 40% failure of ingesting the full dose of prescribed preparation [7]. Colonoscopy is sometimes indicated in older patients who may have a poor compliance for the intake of the bowel preparation and may suffer from heart and renal disease. Therefore, a more tolerable bowel preparation with less severe side effects is desirable. Further, in rectal cancer, patients are currently preoperatively prepared with traditional bowel cleansing, which is proven harmful in colonic surgery [8]. A new preparation without risk of side effects would provide a clean colon, thus minimizing potential anastomotic problems. Low-fiber diet in addition to traditional preparation has been shown beneficial in bowel cleansing for colonoscopy [9–11]. Further, one study reports that a 7-day preoperative low-fiber diet alone provides similar quality of surgical field exposure as traditional preparation [12]. However, no studies have evaluated a low-fiber diet without concurrent traditional preparation as an alternative method of bowel cleansing for colonoscopy. This single-blinded, randomized controlled pilot study compares the degree of bowel cleansing and tolerability between oral nutritional supplements (ONS) and PEG. The aim was to evaluate if ONS can be used as an alternative choice in preparing patients for colonoscopy. Material and methods A feasibility study, conducted before the current study, included seven patients and showed a high degree of bowel cleansing with the use of nutritional supplements prior to colonoscopy. The research protocol was approved by the Karolinska Institute Ethics Committee and carried out in accordance with the Declaration of Helsinki of the World Association (1989) (clinical trial number: NCT00675324, www.clinicaltrials.gov). Patients between the age of 18 and 90 years referred for elective colonoscopy to Ersta Hospital, Stockholm, Sweden, were considered for inclusion in the study. Patients with a known history of diabetes, acute colitis, acute ileus, ostomy and those unable to comply with the study protocol (owing to psychiatric disease, dementia and/or limited ability to understand Swedish) were not eligible. Due to a high level of workload at the clinic and several other concurrent studies, the inclusion rate was slower than expected. Between April 2008 and February 2012, 53 patients aged 38–80 years were included in the study. Computer-generated randomization was conducted to assign patients to either ONS (Fresubin)
(29 patients) or PEG (Laxabon) (24 patients), with allocation concealment maintained by the use of consecutively numbered sealed envelopes. Three patients were excluded after randomization: two in the ONS arm (one who misunderstood the study protocol and had full meals and one who refused colonoscopy due to anal pain), and one in the PEG arm, due to high international normalized ratio (Figure 1). An interim analysis in February 2009 showed unsatisfactory bowel cleansing in patients randomized to ONS. Therefore, in the last 8 of the 27 subjects in the ONS group, the protocol was modified to additional treatment with oral macrogol (Forlax), 10 g, twice daily for 5 days. Due to an assumed continuous failure of cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, the study was interrupted ahead of protocol in February 2012.
Study design Patients were randomized to one of two study arms: (1) ONS only, fiber-free (Fresubin, energy drink) 200 ml/bottle; 1, 5 kcal/ml (protein 5, 6 g; carbohydrates 18, 8 g; fat 5, 8 g), 30 kcal/kg bodyweight/day, for 5 days. Rectal enema, Klyx (1 mg/ml docusate sodium, 250 mg/ml sorbitol) 240 ml was administered the day before and on the same morning as the planned colonoscopy. Additional clear fluids were allowed ad libitum. (2) PEG (Laxabon), 4 l solution, 2 l (2–3 p.m.), 2 l (6–7 p.m.) after a light breakfast, single soup for lunch followed by clear fluids only, the day prior to colonoscopy. From 9 p.m. on the day prior to colonoscopy, only clear fluids were allowed and from midnight all patients were fasting regardless of study arm. All endoscopic investigations were carried out between 8–10 a.m. in the morning. Before the investigation, patients were requested to fill in a bowel symptoms questionnaire (selected questions, Rome III criteria’s) and a feces form and frequency questionnaire (modified Bristol scale) [13] and after investigation, patients were requested to fill a Patient Acceptance Questionnaire. Blood samples were taken before and after investigation. All colonoscopic investigations were conducted by four highly experienced endoscopists blinded to study arm allocation. A calibration exercise ensured that the endoscopists understood and agreed on the rating of bowel preparation using the Ottawa bowel preparation scale [14]. In addition to the rating, the endoscopists were requested to decide whether a new colonoscopy was required or not.
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Assessed for eligibility n = 93 Excluded n = 40 Did not meet inclusion criteria n = 6 Refused to participate n = 16 Other reasons n = 18
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Randomized n = 53 1:1 (ONS: PEG)
Allocated to ONS n = 29 Received intervention n = 27 Did not receive intervention n = 2 -No colonoscopy, full meals n = 1 -No colonoscopy, anal pain n = 1
Lost to follow-up n = 0
Allocated to PEG n = 24 Received intervention n = 23 Did not receive intervention n =1 -No colonoscopy due to high international normalized ratio (INR) n = 1
Lost to follow-up n = 0
Analysed n = 27
Analysed n = 23
Figure1. Study flow chart is shown. ONS = Oral nutritional supplements. PEG = Polyethylene glycol.
The Ottawa scale was used to rate the level of bowel cleansing in the right-, mid-, and recto-sigmoid colon on a 5-point scale (0–4). Further, the scale rates a global 3-point rating for overall colonic fluid (0–2). Thus, the total score ranges from 0 to 14. A score 0 to 1 is considered an excellent preparation, 2 to 4 a good preparation, whereas scores >4 indicate progressively worsening bowel preparation. A score between 11 and14 indicates a completely unprepared colon depending on the amount of colonic fluid [15]. Statistical analysis We were not aware of any preexisting data available on ONS preparation for colonoscopy. The power analysis was made on an estimated least detectable difference in bowel cleansing of 25% in favor of PEG. With 80% power at a two-sided alpha of 0.05, the number of patients needed to treat was estimated to be 65 in each group. Results are presented as mean (SD) and rate (%). Shapiro–Wilk’s testing for normal distribution was conducted. Two-tailed t-test of unequal variance was used for crude comparisons of normally distributed continuous variables. Non-parametric Wilcoxon
rank-sum test was used for categorical variables and continuous data without normal distribution. A score £4 is considered a good bowel cleansing. However, in order to find possible common variables in patients receiving ONS resulting in acceptable (score £5) compared to unacceptable (score >5) bowel cleansing, adjusted comparisons with logistic regression was used. Between groups comparisons of laboratory data were analyzed using paired t-test and signed-rank test. The eight patients in the ONS group receiving additional treatment with orally administrated macrogol were analyzed together with all ONS patients, if not particularly specified. A p-Value of < 0.05 was considered statistically significant. All data were analyzed using Stata version 12 (Stata Corporation, Collage Station, Texas, USA). Results With the exception of a higher rate of morbidity (fewer American Society of Anesthesiologists (ASA) physical status 1) in patients receiving ONS, p = 0.029, there were no significant differences in basic characteristics in patients randomized to ONS (n = 27) and PEG
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(n = 23), respectively. No differences between groups with regard to self-reported pre-preparation bowel evacuation, defecations/week or Bristol classification were found (Table I).
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Tolerability Among patients receiving ONS, 22 of 27 (81%) had complete intake of prescribed nutrition drinks (mean total number of bottles 36.4 ± 8.5 SD). Nineteen patients (83%) receiving PEG had a full dose of 4 l of PEG, whereas the remaining four patients (17%) had a total intake of 3 l. Of the 27 patients in the ONS group, 26 were treated with rectal enema. A significantly higher rate of patients receiving ONS found the taste of the preparation acceptable (27 of 27 (100%) vs. 15 of 23 (65%), p = 0.001) and fewer patients reported difficulties with intake of the preparation (0 of 27 (0%) vs. 10 of 23 (43%), p < 0.001) and nausea (5 of 27 (19%) vs. 13 of 23 (27%), p = 0.008), compared with patients receiving PEG. A total of 23 patients (85%) in the ONS group and 17 (74%) in the PEG group would consider to undergo the same bowel preparation again (Table II). Laboratory data Within groups, a mean decrease in plasma-potassium, S-Ca2+, and plasma-chloride compared to the preTable I. Patient characteristics.
Age, mean, SD BMI, mean, SD Gender (M/F) ASA1 ASA2 ASA3 Systemic disease Previous colonoscopy Previous abdominal surgery Previous colonic resection Defecations/week Bristol classification Incomplete evacuation Indication: bleeding Indication: control Indication: pain Indication: bowel habits Indication: heredity
ONS (n = 27)
PEG (n = 23)
p
60.8 ± 11.1 26.4 ± 3.8 11/16 13 13 1 14(51.9) 17(63.0) 12(44.7)
61.1 ± 11.0 24.7 ± 4.3 11/12 18 5 0 6(26) 14(60.9) 8(34.8)
0.910a 0.139a 0.615b 0.029b 0.053b 1.000m 0.064b 0.829b 0.487b
6(22.2)
6(26.1)
0.750b
12.9 ± 8.4 4.0 ± 1.2 8(29.6) 10 11 2 3 1
14.3 ± 10.8 4.2 ± 4.2 8(34.8) 9 10 2 2 0
0.732$ 0.494$ 0.697b 0.879b 0.845b 1.000m 1.000m 1.000m
Abbreviations: ASA = American Society of Anesthesiologists physical status; BMI = body mass index; Bristol classification: (1–7), 1 = Separate hard lumps, 7 = fluid only. Incomplete evacuation = self-reported status; a = Two tailed t-test; b =Pearson’s c2 test; $ = Wilcoxon rank-sum test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise.
preparation baseline in patients receiving ONS and PEG was statistically significant, p < 0.05. Also, an increase in plasma-urea and plasma-creatinine among patients receiving ONS and the decrease in plasmaalbumin and plasma-urea among patients receiving PEG was significant, p < 0.05. However, all values were still within a normal reference interval. Between groups, only a difference between the enhanced plasma-urea among patients in the ONS group and a decreased plasma-urea in the PEG group was statistically significant, p < 0.0001, however without clinical importance (data not shown). Quality of the bowel preparation Among patients receiving ONS, 6 of 27 (22%) of the investigations cecum could not be intubated due to stools versus 1 of 23 (4%) in the PEG group (ns). Thus, cecum could be intubated in the majority of patients receiving ONS. There was a need for new colonoscopy (i.e. to exclude minor lesions) in 15 of 27 (55 %) and 1 of 23 (4%) patients in the ONS and PEG arms, respectively, p < 0.001 (Table III). The mean total Ottawa preparation scores were 8.3 ± 3.3 in the ONS group compared with 5.3 ± 2.8 in the PEG group, p = 0.002 (Figure 2). The right colon and the transverse colon/descendens was significantly more difficult to clean in the ONS group compared to the PEG group, whereas no significant difference was found in the recto-sigmoid colon between groups. Less fluid in the colon was found among patients receiving ONS compared to PEG. Four patients (15%) in the ONS group and eight patients (35%) receiving PEG had an Ottawa bowel score (OBS) score £4 (ns) (Table III). In a subanalysis of the eight patients in the ONS group who received additional treatment with a low dose of oral macrogol, the mean total OBS score was 8.3 ± 3.1 (SD) versus 8.3 ± 3.5 (SD) in patients without additional treatment. There was neither a difference in OBS score of separate parts of colon between these two groups. In multivariate analysis, no common variables were found in patients receiving ONS resulting in acceptable (score £5) compared to unacceptable (score >5) bowel cleansing. Discussion Due to failure of bowel cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, this single-blinded, randomized controlled study was prematurely interrupted at a pilot stage. Additional treatment with a low-dose oral macrogol did not seem to substantially improve the degree of bowel cleansing. Although patients
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Table II. Compliance to preparation.
Full intake of prescribed bowel preparation Treatment with prescribed enema Acceptable taste of preparation Difficulty in taking preparation Off work precluding colonoscopy Nausea Regurgitation Abdominal pain Need for help with bowel preparation Would consider same bowel preparation
ONS (n = 27
PEG (n = 23)
22(81.5)
19(82.6)
26(96.3)
p 0.974b
0
27(100)
15(65.2)
0.001b
0(0)
10(43.5)
< 0.001m
4*(30.8)
7**(63.6)
0.217m
5(18.5) 0(0) 5(18.5) 3(11.1)
13(56.5) 1(4.3) 9(39.1) 1(4.3)
0.008m 0.460m 0.126m 0.614m
23(85.2)
17(73.9)
0.480m
Abbreviations: b = Pearson’s c2 test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise. *n = 13; **n = 11.
receiving ONS showed a high rate of tolerability for the preparation, only 15% had an OBS score £4 (good preparation), and in 55% of the patients a new colonoscopy was considered required (i.e. to exclude minor lesions). The OBS [14] is a validated tool for evaluating quality of bowel preparation. Previous studies reporting OBS score using PEG preparation have shown a mean total score between 3.2 and 5.2 [15–17]. In the current study, the mean total OBS score in patients receiving PEG was 5.3 and only 35% of the patients had a score £4. This indicates that the majority of patients in the group with traditional preparation (PEG) had an unsatisfactory bowel preparation. These results could in part be explained by the fact Table III. Primary outcome.
Duration of colonoscopy, mean, min Incomplete colonoscopy (stools) Right colon OBS (0–4) Transverse colon/descendens OBS (0–4) Rectosigmoid colon OBS (0–4) Fluid in colon OBS (0–2) Total score OBS (0–14) OBS score £4 OBS score £5 New colonoscopy required
ONS (n = 27)
PEG (n = 23)
33 ± 13
35 ± 15
0.937$
1(4.3)
< 0.107m
3.7 ± 0.5 3.0 ± 1.3
1.8 ± 0.9 1.3 ± 0.9
< 0.001$ < 0.001$
1.4 ± 1.4
1.3 ± 1.0
0.800$
0.4 ± 0.6 8.3 ± 3.3 4(14.8) 7(25.9) 15(55.5)
0.8 ± 0.7 5.3 ± 2.8 8(34.8) 10(43.5) 1(4.3)
0.034$ 0.002$ 0.183m 0.192m < 0.001m
6(22.2)
p
Abbreviations: OBS = Ottawa bowel score; $ = Wilcoxon rank-sum test; m = Fisher’s exact test. Values in parentheses are percentages, unless indicated otherwise.
489
that our patients received PEG in a single-dose regimen instead of a split-dose regimen, which is proven favorable in some studies [18]. However, the current data suggest that PEG (at least in a single-dose regimen), the only recommended preparation in patients with heart and renal failure [19], is insufficient in bowel cleansing before colonoscopy in a substantial proportion of patients. In addition to the failing efficacy of PEG, the discomfort and inconvenience associated with ingesting the required 4-l fluid regimen calls for new alternative ways of preparing the bowel for colonoscopy. Particularly, in the view of an increasingly old population with concurrent diseases and possibly wider indications for participation in screening programs, tolerability to the bowel preparation may affect the acceptability and inclusion of these patients [20]. In addition, development of minimally invasive surgical techniques and perioperative care allow surgical treatment also in the very frail patients, and thus screening for colorectal malignancy in this group of patients should be performed with as little risk and discomfort as possible. There were several reasons for investigating the effect of ONS and rectal enema as an alternative method of preparation. First, as shown in the current study, the tolerability of ONS is good and would allow the patient to work or continue social activities until the day of colonoscopy. Second, ONS in combination with PEG has shown improved bowel cleansing compared with PEG alone [9,11] or with a clear liquid diet [21]. Also, in one previous study, similar quality of surgical field exposure as traditional preparation was reported after ONS [12], indicating that practice of this new regimen in rectal cancer surgery may allow bowel cleansing without side effects along with a clean bowel that may reduce risks of morbidity associated with anastomotic leakage. Although, the current study showed failure of bowel cleansing and an unacceptable high rate of need for a new colonoscopy in patients receiving ONS, 26% had an acceptable OBS score (£5). Further, intubation of cecum could be obtained in 78% of patients receiving ONS. Despite this, ONS may not be recommended in old and/or seriously ill patients who cannot be expected to tolerate traditional preparation for colonoscopy, since complications caused by a colonoscopic procedure in an unclean colon may be deleterious in these fragile patients. However, the use of ONS in rectal cancer surgery should be explored more closely. In summary, ONS is a procedure with high tolerability and compliance that allow intubation of cecum in the majority of patients. ONS cannot be recommended in general due to limited visibility in the right colon in 50% of the patients, with an expected
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4 3.5
p < 0.001
OBS-score
3 2.5 p = 0.800
2 1.5
ONS PEG
1 0.5 0
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Right
Trsv-desc
Recto-Sigm
Figure 2. OBS: differences in right colon, transverse/descendant colon and recto-sigmoidal colon between ONS and PEG, respectively are shown. The difference in total score between ONS, mean SD = 8.3 ± 3.3, and PEG, mean SD = 5.3 ± 2.8, was significant (p = 0.002). Total score range from 0 to 14). Score 0–1 is considered an excellent preparation, 2–4 is considered a good preparation, whereas scores >4 indicates progressively worsening bowel preparations. A score of 11–14 equals a completely unprepared colon depending on the amount of colonic fluid.
reduced detection rate of minor lesions. However, other fields of application, such as in rectal cancer surgery, remain to be studied.
Acknowledgments The authors express their gratitude to Lars-Erik Ahlgren, Gunilla Nyström Strand, Ann-Sofie Andersson, Anette Bratt, Monica Johansson, and Nina Blomme for excellent nursing and technical assistance. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper. This work (design and conduct of the study; collection, management, analysis and interpretation of the data; preparation, review, and approval of the manuscript) was supported by funds from the Swedish Research Council (#09101), Stockholm County Council (SLL), Hans Mellström, Sweden, and Familjen Erling-Persson’s Foundation.
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