Abstract
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Purpose
- Low anterior resection syndrome (LARS) manifests with evacuation disorder symptoms and continence problems. However, no prior study has focused on evacuation disorders in patients with LARS. This study investigated the prevalence of evacuation disorders and their association with the LARS score.
-
Methods
- This study included patients with defecation per anus at the time of the survey, which was conducted between November 2020 and April 2021. These patients had undergone anus-preserving surgery for rectal tumors between 2014 and 2019 at a tertiary university hospital. The severity of evacuation disorders and LARS was evaluated using the Constipation Scoring System and the LARS score, respectively. The primary endpoint was the prevalence of evacuation disorders, defined as evacuation difficulty, feeling of incomplete evacuation, and abnormally long time on the toilet. The secondary endpoints were the associations between these symptoms and the LARS score.
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Results
- Of 332 eligible patients, 238 (71.7%) completed the questionnaire. The overall prevalence of evacuation disorders was 48.3%. The rates of feeling incomplete evacuation, evacuation difficulty, and prolonged time on the toilet were 45.6%, 15.5%, and 8.4%, respectively. Patients with minor or major LARS had a significantly higher prevalence of evacuation disorders than those with no LARS, particularly regarding feeling incomplete evacuation.
-
Conclusion
- Evacuation disorders were present in 48.3% of patients following anus-preserving surgery. Greater severity of LARS was associated with a higher prevalence of evacuation disorders, especially a feeling of incomplete evacuation. Patients should be informed about the potential for both evacuation disorders and continence-related symptoms following anus-preserving surgery.
-
Keywords: Low anterior resection syndrome; Evacuation disorder; Evacuation difficulty; Feeling of incomplete evacuation; Long time on the toilet
INTRODUCTION
Patients who have undergone rectal resection experience a range of symptoms collectively termed low anterior resection syndrome (LARS). Bryant et al. [1] defined LARS as “disordered bowel function after rectal resection, leading to a detriment in quality of life.” The symptoms of LARS substantially impair patients’ quality of life (QoL) [2]. The severity of LARS is typically assessed using the LARS score, developed by Emmertsen and Laurberg [3], which includes 5 questions pertaining to incontinence to flatus, incontinence to liquid stool, bowel movement frequency, clustering of stools, and urgency.
Among the 5 components of the LARS score, only “clustering of stools” pertains to evacuation disorder, while the remaining 4 items address continence-related symptoms. Patients with LARS may also report symptoms akin to constipation, with evacuation disorder being the most common complaint. In a systematic review by Keane et al. [4], the most frequently reported outcomes were fecal incontinence (97%), increased stool frequency (80%), fecal urgency (67%), and evacuatory dysfunction (47%). The most commonly evaluated aspects of evacuatory dysfunction were incomplete emptying, evacuation difficulty, and evacuation time, in that order. Additionally, the international consensus definition of LARS proposed by the LARS International Collaborative Group in 2020 [5] includes evacuation difficulty as “emptying difficulties” among the 8 key symptoms of LARS. Nonetheless, no study has specifically focused on the symptoms of evacuation disorders in patients with LARS, and it remains unclear whether the LARS score accurately reflects these symptoms.
The aim of this study was to determine the prevalence of evacuation disorders and evaluate the association between these disorders and the LARS score.
METHODS
Ethics statement
All study protocols were approved by the Jichi Medical University Central Clinical Research Ethics Committee (No. 20-039). Written informed consent was obtained from all participants via a consent form included with the questionnaire.
Study setting
This single-institution study was conducted in the Department of Surgery at Jichi Medical University Hospital (Shimotsuke, Japan). It represents a subanalysis of previously reported data that described the prevalence of LARS and its association with QoL in patients following anus-preserving surgery for rectal tumors [6,7].
Patients
Candidates for the study were patients who underwent anus-preserving surgery for rectal tumors between January 1, 2014, and December 31, 2019. They were identified using a prospectively maintained departmental database. Questionnaires were sent by postal mail, excluding those with a history of stoma creation or those who were deceased according to medical records. Only patients who fully completed the LARS score survey were considered valid responders and included in the analysis. Patients who did not complete the LARS survey, had moved, died, or otherwise did not return a complete questionnaire were excluded.
Parameters to evaluate LARS and evacuation disorders
The prevalence and severity of LARS symptoms were assessed using the LARS score (range, 0–42), which is categorized as no LARS (score, 0–20), minor LARS (score, 21–29), and major LARS (score, 30–42) [3]. Constipation symptoms were evaluated with the Constipation Scoring System (CSS), which ranges from 0 (no symptoms) to 30 (most severe symptoms) [8]. Evacuation disorder was assessed using 3 CSS items: “evacuation difficulty” (reflecting painful evacuation effort), “feeling of incomplete evacuation,” and “time on toilet” (defined as minutes spent in the lavatory per attempt). In the CSS, both evacuation difficulty and the feeling of incomplete evacuation are rated on a 5-point scale: 0, never; 1, rarely (less than once a month); 2, sometimes (at least once a month but less than once a week); 3, usually (at least once a week but less than once a day); and 4, always (at least once a day). In this study, a score of 3 or 4 on these items was considered diagnostic for evacuation difficulty or feeling of incomplete evacuation. Time on toilet was rated on a separate 5-point scale: 0, less than 5 minutes; 1, 5 to 9 minutes; 2, 10 to 19 minutes; 3, 20 to 29 minutes; and 4, at least 30 minutes. A score of 3 or 4 on the CSS was considered indicative of spending an abnormally long time on the toilet.
Study design and endpoints
Questionnaires were distributed and collected from November 2020 to April 2021. Clinical and surgical data, including age, sex, comorbidities, type of rectal tumor, tumor location, and neoadjuvant treatment, were compared between valid and invalid responders. Tumor location was classified as upper, middle, or lower rectum in accordance with the Japanese Classification of Colorectal Carcinoma [9]. This classification relies on landmarks such as the sacral promontory, the inferior border of the second sacral vertebra, the peritoneal reflection, and the upper border of the anal canal, thereby dividing the rectum into 3 sections. Surgical data encompassed the type of surgical procedure, the type of mesorectal excision, the type of anastomosis, and the presence of a diverting stoma, among other factors. The surgical procedures were categorized as high anterior resection, low anterior resection, ultralow anterior resection, or intersphincteric resection. In high anterior resection, the anastomosis was performed above the peritoneal reflection; in low anterior resection, between the peritoneal reflection and 1 cm above the anorectal junction; in ultralow anterior resection, within 1 cm above the anorectal junction; and in intersphincteric resection, with partial or total resection of the internal anal sphincter.
The primary endpoints were the prevalence rates, among all valid responders, of the 3 evacuation disorder symptoms: evacuation difficulty, feeling of incomplete evacuation, and an abnormally long time on the toilet. The secondary endpoints involved examining the association between each of these symptoms and LARS severity, as measured by the LARS score. To assess these associations, the prevalence of each symptom was compared among the no LARS, minor LARS, and major LARS groups, and the LARS score was compared between patients with and without each evacuation disorder symptom. Additionally, correlation analysis between the LARS score and the CSS score for each symptom was performed to evaluate the association between LARS and symptom severity.
Statistical analysis
Data were treated as nonparametric and are expressed as median and range. The Mann-Whitney U-test was used for comparisons of continuous data between 2 groups, while the Fisher exact probability test or the chi-square test was employed for categorical data, as appropriate. Spearman correlation analysis was used to calculate correlation coefficients and evaluate the association between the LARS score and the severity of each of the 3 symptoms. All statistical analyses were performed using GraphPad Prism ver. 8.0 (GraphPad Software).
RESULTS
Questionnaires were sent to 332 eligible patients out of 377 candidates identified in the database, after excluding 45 individuals who had died, undergone stoma creation, or had an unclosed stoma (Fig. 1). Among these 332 patients, 238 (71.7%) completed the LARS questionnaire in full and were considered valid responders, while 94 (28.3%) were deemed invalid responders for the reasons outlined in Fig. 1.
Demographic data were compared between the 238 valid responders and 93 invalid responders. One invalid responder was excluded due to declining participation. Overall, the demographic characteristics were similar between the groups, except for age, central nervous system comorbidities, and psychiatric disorders (Table 1). Invalid responders were significantly older than valid responders, and they also had higher frequencies of central nervous system comorbidities and psychiatric disorders.
Characteristics of valid responders
The 238 valid responders constituted the analysis cohort. The median age was 67 years (range, 29–91 years), and 149 (62.6%) were male (Table 1). Tumor locations were evenly distributed among the upper, middle, and lower rectum. Only 24 patients (10.1%) had received neoadjuvant chemoradiotherapy. Low anterior resection was the most frequently performed procedure (40.8%), while intersphincteric resection was the least common (2.9%). A diverting stoma was created in 78 patients (32.8%), and anastomotic leakage occurred in only 5 patients (2.1%). The median interval since rectal resection or stoma closure was 44.7 months (range, 3.0–81.5 months). Among the 238 patients, 48 (20.2%) reported having undergone some treatment for their bowel problems, including evacuation disorders.
Prevalence of evacuation disorders
Among 234 of the 238 valid responders, the median CSS score was 6 (range, 0–19). Evacuation disorders were present in 115 patients (48.3%), with these patients exhibiting at least one of the following symptoms: evacuation difficulty, feeling of incomplete evacuation, or prolonged time on the toilet. The most common symptom was a feeling of incomplete evacuation, reported by 45.6% (108 of 237 patients), followed by evacuation difficulty at 15.5% (37 of 238), and long time on the toilet at 8.4% (20 of 238) (Fig. 2).
Association between evacuation disorders and LARS
The median LARS score among the 238 valid responders was 16 (range, 0–41). The prevalence rates of no, minor, and major LARS were 58.4% (139 patients), 19.7% (47 patients), and 21.8% (52 patients), respectively. The prevalence rates of the 3 evacuation disorder symptoms were compared among the no, minor, and major LARS groups (Fig. 3). Patients with either minor or major LARS had significantly higher prevalence rates of all 3 symptoms than those with no LARS. The prevalence of a feeling of incomplete evacuation was significantly higher in the major LARS group than in the minor LARS group, while no significant differences were found between groups regarding evacuation difficulty or prolonged time on the toilet. Consequently, the prevalence of a feeling of incomplete evacuation decreased in the order of major, minor, and no LARS, indicating that more severe LARS is associated with a higher prevalence of this symptom. Additionally, when comparing LARS scores between patients with and without each of the 3 symptoms, the scores were significantly higher in patients presenting each symptom (Table 2). Among those with positive evacuation disorder symptoms, the LARS score was significantly higher in patients with prolonged time on the toilet (median score, 33) than in those with evacuation difficulty (median score, 26; P=0.005) or feeling of incomplete evacuation (median score, 27; P=0.027). No significant difference was observed between evacuation difficulty and feeling of incomplete evacuation (P=0.209).
In correlation analyses, the feeling of incomplete evacuation was moderately associated with the LARS score (r=0.58), whereas the associations with LARS score were weak for evacuation difficulty (r=0.21) and prolonged time on the toilet (r=0.31) (Fig. 4).
DISCUSSION
This study demonstrated that evacuation disorders occurred in 48.3% of patients following anus-preserving surgery for rectal tumors. Among the evaluated symptoms, a feeling of incomplete evacuation was the most common (45.6%), followed by evacuation difficulty (15.5%) and prolonged time on the toilet (8.4%). More severe LARS was linked to a higher prevalence of evacuation disorders, especially a feeling of incomplete evacuation. Moreover, the LARS score was significantly higher in patients exhibiting each of these 3 symptoms compared to those without them, with patients who spent an abnormally long time on the toilet showing the highest scores.
Typically, only continence-related symptoms such as frequent bowel movements, fecal incontinence, and fecal urgency are assessed in LARS evaluations, while evacuation disorder symptoms like a feeling of incomplete evacuation and evacuation difficulty are often overlooked. In a review of 128 studies on LARS, Keane et al. [4] found that only 26% of the papers evaluated incomplete emptying, noting that most studies focused on incontinence while ignoring other symptoms that affect QoL. Although the widely used LARS score includes only clustering of stools as a marker of evacuation disorder, with the other 4 items pertaining to continence-related symptoms, evacuation disorders remain important because they can significantly impair QoL as part of constipation symptoms [10]. This significance likely contributed to the inclusion of emptying difficulties as one of the 8 key symptoms in the international consensus definition of LARS [5]. Although several studies have examined evacuation disorder symptoms within broader assessments of LARS [11–14], no study has exclusively focused on evacuation disorders. To our knowledge, this is the first study to specifically address evacuation disorders in LARS, providing clinically valuable data that can help in explaining these issues to affected patients.
Adachi et al. [11] reported very high prevalence rates of difficulty in emptying (81%) and incomplete evacuation (75%) among patients with LARS. These elevated rates likely reflect the definitions used for positive symptoms, which included patients with a “mild or severe” degree of difficulty in emptying and those reporting “sometimes or often” for incomplete evacuation. In contrast, in the present study, only patients reporting “usually or always” for evacuation difficulty and for the feeling of incomplete evacuation were included, resulting in prevalence rates of 16% and 45%, respectively. Sato et al. [12] from the same institute as Adachi et al. [11] employed different surgical techniques, preserving the pelvic autonomic nerves and foregoing high ligation of the inferior mesenteric artery, as suggested by Adachi et al. [11], and reported lower prevalence rates of “difficulty in emptying” (67%) and “incomplete evacuation” (58%). These findings imply that surgical techniques may influence the occurrence of evacuation disorders. Miacci et al. [13] evaluated 7 LARS symptoms in 64 patients who underwent anterior resection of the rectum and found that incomplete evacuation was the most frequently reported symptom (60%), followed by fecal urgency (55%). However, their analysis did not include other evacuation disorder symptoms such as evacuation difficulty or prolonged time on the toilet. Ohigashi et al. [14] reported a prevalence of “feeling of incomplete defecation” of 78.6% and a prevalence of “time for evacuation of more than 15 minutes” of 16.7%. However, the term “feeling of incomplete defecation” was not explicitly defined, and the definition of prolonged evacuation time (>15 minutes) differs from that used in the present study (≥20 minutes). Overall, comparing the results of evacuation disorders across the literature is challenging because definitions regarding frequency and severity differ widely. Despite these variations, the clinical importance of evacuation disorders is undeniable given the high number of affected patients. Standardized definitions are therefore needed to facilitate proper comparisons among studies.
In the present study, more severe LARS—as assessed by the LARS score—was associated with higher prevalence rates of evacuation disorders, particularly the feeling of incomplete evacuation. Patients with each of the 3 evaluated symptoms had significantly higher LARS scores compared to those without these symptoms. This association is likely due to the inclusion of “clustering of stools” in the LARS score, which is related to evacuation disorders. Patients experiencing a feeling of incomplete evacuation tend to revisit the toilet shortly after defecation, resulting in clustered stools. The original LARS score paper stated that items were grouped into 4 domains— incontinence, emptying difficulties, urgency, and frequency [3]. Although several items addressing emptying difficulties were initially considered, the final LARS score retained “clustering of stools” as the representative item for this domain. Moreover, this item can contribute up to 11 points of the total 42 points (26.1%), making it the second most heavily weighted component. This weighting may explain why more severe LARS is associated with a higher incidence of evacuation disorders, particularly the feeling of incomplete evacuation, which was the most prevalent symptom (45%).
Several limitations of this study should be noted. First, the results may not represent all patients who underwent anus-preserving surgery because significant differences in age and comorbidities—including central nervous system and psychiatric disorders—were observed between valid and invalid responders. This discrepancy may stem from the use of a self-administered questionnaire, as older patients or those with such comorbidities might have difficulty completing it accurately. Second, preoperative evacuation disorders were not evaluated, and their presence could have influenced postoperative outcomes. Third, the true prevalence of evacuation disorders might be higher than the reported 48.3%, as some patients may have experienced improvement following treatment; among the 238 patients, 48 (20.2%) had received treatment for bowel problems, but it is unclear how many were treated specifically for evacuation disorders or whether those treatments were effective. Fourth, only 3 symptoms of evacuation disorders were assessed; additional symptoms, such as the need for digital assistance or unsuccessful attempts at evacuation, should also be evaluated. Fifth, “time on the toilet” may not be an optimal measure of evacuation disorder because frequent bowel movements in LARS patients might result in prolonged toilet time even in the absence of evacuation difficulty or a feeling of incomplete evacuation. Sixth, the CSS and LARS scores used in this study were not validated in Japanese, although a separate validation may not be necessary for these simple scoring systems. Seventh, constipation-specific QoL was not evaluated because this study was a subanalysis of the main study focusing on LARS prevalence and its association with fecal incontinence-specific QoL [6,7]. Future research should address constipation-specific QoL.
In conclusion, this study demonstrated that 48.3% of patients experienced evacuation disorders following anus-preserving surgery for rectal tumors. Among these symptoms, the feeling of incomplete evacuation was the most common (45.6%), followed by evacuation difficulty (15.5%) and prolonged time on the toilet (8.4%). More severe LARS, as measured by the LARS score, was associated with a higher prevalence of evacuation disorders, particularly the feeling of incomplete evacuation. Patients with each of the 3 symptoms had significantly higher LARS scores than those without. Patients with rectal tumors should be informed about the potential for both evacuation disorders and continence-related symptoms following anus-preserving surgery. It is essential that both types of symptoms are thoroughly evaluated and managed postoperatively.
ARTICLE INFORMATION
-
Conflict of interest
No potential conflict of interest relevant to this article was reported.
-
Funding
None.
-
Acknowledgments
The authors greatly appreciate the secretarial staff of the surgery department for their support in sending and collecting the questionnaires.
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Author contributions
Conceptualization: YH, TM, HH, NS; Data curation: YH, TM, KK, HH; Formal analysis: YH, TM; Investigation: YH; Methodology: TM, KK, HH; Project administration: YH; Visualization: YH, TM; Writing–original draft: YH, TM; Writing–review & editing: TM, KK, HH, NS; All authors read and approved the final manuscript.
Fig. 1.Flowchart of patient selection. LARS, low anterior resection syndrome.
Fig. 2.Prevalence of evacuation disorders. Usually, at least once a week but less than once a day; always, at least once a day.
Fig. 3.Comparison of evacuation disorder prevalence among patients with no, minor, and major low anterior resection syndrome (LARS). (A) Evacuation difficulty. (B) Feeling of incomplete evacuation (n=237). (C) Long time on the toilet. Usually, at least once a week but less than once a day; always, at least once a day. *P<0.05.
Fig. 4.Correlation between each evacuation disorder symptom and the low anterior resection syndrome (LARS) score. (A) Evacuation difficulty. (B) Feeling of incomplete evacuation. (C) Long time on the toilet.
Table 1.Baseline demographic characteristics of the valid and invalid responders (n=332)
|
Characteristic |
Valid responder (n=238) |
Invalid responder (n=93) |
P-value |
|
Age (yr) |
67 (29–91) |
70 (31–89) |
0.012*
|
|
Sex |
|
|
0.454 |
|
Male |
149 (62.6) |
54 (58.1) |
|
|
Female |
89 (37.4) |
39 (41.9) |
|
|
Comorbidity |
|
|
|
|
Diabetes mellitus |
43 (18.1) |
20 (21.5) |
0.533 |
|
Hypertension |
96 (40.3) |
23 (24.7) |
0.215 |
|
Coronary disease |
10 (4.2) |
5 (5.4) |
0.769 |
|
Spinal cord impairment |
11 (4.6) |
4 (4.3) |
>0.999 |
|
Central nervous system disorder |
7 (2.9) |
12 (12.9) |
0.001*
|
|
Psychiatric disorder |
2 (0.8) |
7 (7.5) |
0.003*
|
|
Type of rectal tumor |
|
|
0.499 |
|
Adenocarcinoma |
230 (96.6) |
92 (98.9) |
|
|
Neuroendocrine tumor |
7 (2.9) |
1 (1.1) |
|
|
Benign tumor |
1 (0.4) |
0 (0) |
|
|
Tumor location |
|
|
0.308 |
|
Upper |
82 (34.5) |
32 (34.4) |
|
|
Middle |
74 (31.1) |
36 (38.7) |
|
|
Lower |
82 (34.5) |
25 (26.9) |
|
|
Neoadjuvant chemoradiotherapy |
24 (10.1) |
5 (5.4) |
0.200 |
|
Surgical procedure for rectal resection |
|
|
0.579 |
|
High anterior resection |
84 (35.3) |
37 (39.8) |
|
|
Low anterior resection |
97 (40.8) |
38 (40.9) |
|
|
Ultralow anterior resection |
50 (21.0) |
14 (15.1) |
|
|
Intersphincteric resection |
7 (2.9) |
4 (4.3) |
|
|
Type of mesorectal excision |
|
|
0.465 |
|
Partial mesorectal excision |
181 (76.1) |
75 (80.6) |
|
|
Total mesorectal excision |
57 (23.9) |
18 (19.4) |
|
|
Type of anastomosis |
|
|
0.455 |
|
Double-stapling technique |
221 (92.9) |
89 (95.7) |
|
|
Hand-sewn |
17 (7.1) |
4 (4.3) |
|
|
Diverting stoma |
78 (32.8) |
25 (26.9) |
0.685 |
|
Ileostomy |
72 |
22 |
|
|
Colostomy |
6 |
3 |
|
|
Anastomotic leak |
5 (2.1) |
3 (3.2) |
0.691 |
|
TNM classification (n=237)a)
|
|
|
0.171 |
|
Stage 0 |
2 (0.8) |
0 (0) |
|
|
Stage I |
100 (42.0) |
35 (37.6) |
|
|
Stage II |
51 (21.4) |
29 (31.2) |
|
|
Stage III |
78 (32.8) |
24 (25.8) |
|
|
Stage IV |
6 (2.5) |
5 (5.4) |
|
|
Adjuvant chemotherapy |
71 (29.8) |
21 (22.6) |
0.220 |
|
Interval since rectal resection or diverting stoma closure (mo) |
44.7 (3.0–81.5) |
46.4 (10.7–82.0) |
0.410 |
Table 2.Comparison of LARS scores between patients with and without evacuation disorder symptoms (n=238)
|
Symptom |
No. of patients |
LARS score |
P-value |
|
Evacuation difficulty (n=238) |
|
|
0.006*
|
|
Yes |
37 |
26 (2–39) |
|
|
No |
201 |
15 (0–41) |
|
Feeling of incomplete evacuation (n=237)a)
|
|
|
<0.001*
|
|
Yes |
108 |
27 (0–41) |
|
|
No |
129 |
11 (0–41) |
|
Long time on the toilet (n=238) |
|
|
<0.001*
|
|
Yes |
20 |
33 (0–41) |
|
|
No |
218 |
14 (0–41) |
REFERENCES
- 1. Bryant CL, Lunniss PJ, Knowles CH, Thaha MA, Chan CL. Anterior resection syndrome. Lancet Oncol 2012;13:e403–8. ArticlePubMed
- 2. Al Rashid F, Liberman AS, Charlebois P, Stein B, Feldman LS, Fiore JF Jr, et al. The impact of bowel dysfunction on health-related quality of life after rectal cancer surgery: a systematic review. Tech Coloproctol 2022;26:515–27. ArticlePubMedPDF
- 3. Emmertsen KJ, Laurberg S. Low anterior resection syndrome score: development and validation of a symptom-based scoring system for bowel dysfunction after low anterior resection for rectal cancer. Ann Surg 2012;255:922–8. ArticlePubMed
- 4. Keane C, Wells C, O’Grady G, Bissett IP. Defining low anterior resection syndrome: a systematic review of the literature. Colorectal Dis 2017;19:713–22. ArticlePubMedPDF
- 5. Keane C, Fearnhead NS, Bordeianou LG, Christensen P, Basany EE, Laurberg S, et al. International consensus definition of low anterior resection syndrome. Dis Colon Rectum 2020;63:274–84. ArticlePubMedPMC
- 6. Homma Y, Mimura T, Koinuma K, Horie H, Lefor AK, Sata N. Low anterior resection syndrome: incidence and association with quality of life. Ann Gastroenterol Surg 2024;8:114–23. ArticlePubMedPMC
- 7. Homma Y, Mimura T, Koinuma K, Horie H, Sata N. Incidence of low anterior resection syndrome and its association with the quality of life in patients with lower rectal tumors. Surg Today 2024;54:857–65. ArticlePubMedPDF
- 8. Agachan F, Chen T, Pfeifer J, Reissman P, Wexner SD. A constipation scoring system to simplify evaluation and management of constipated patients. Dis Colon Rectum 1996;39:681–5. ArticlePubMed
- 9. Japanese Society for Cancer of the Colon and Rectum. Japanese classification of colorectal, appendiceal, and anal carcinoma: the 3d English edition [secondary publication]. J Anus Rectum Colon 2019;3:175–95. ArticlePubMedPMC
- 10. Wald A, Scarpignato C, Kamm MA, Mueller-Lissner S, Helfrich I, Schuijt C, et al. The burden of constipation on quality of life: results of a multinational survey. Aliment Pharmacol Ther 2007;26:227–36. ArticlePubMed
- 11. Adachi Y, Kakisako K, Sato K, Shiraishi N, Miyahara M, Kitano S. Factors influencing bowel function after low anterior resection and sigmoid colectomy. Hepatogastroenterology 2000;47:155–8. PubMed
- 12. Sato K, Inomata M, Kakisako K, Shiraishi N, Adachi Y, Kitano S. Surgical technique influences bowel function after low anterior resection and sigmoid colectomy. Hepatogastroenterology 2003;50:1381–4. PubMed
- 13. Miacci FL, Guetter CR, Moreira PH, Sartor MC, Savio MC, Baldin Júnior A, et al. Predictive factors of low anterior resection syndrome following anterior resection of the rectum. Rev Col Bras Cir 2020;46:e20192361. ArticlePubMed
- 14. Ohigashi S, Hoshino Y, Ohde S, Onodera H. Functional outcome, quality of life, and efficacy of probiotics in postoperative patients with colorectal cancer. Surg Today 2011;41:1200–6. ArticlePubMedPDF
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