Disparities in long‑term outcomes between benign and malignant diseases after Hartmann's procedure: A retrospective observational study
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- Published online on: May 15, 2025 https://doi.org/10.3892/mco.2025.2859
- Article Number: 64
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Copyright: © Imaizumi et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
There is a worldwide increase in the incidence of colorectal cancer and diverticulosis on the left side of the colon. Hartmann's procedure (HP) is a surgery used to reduce the risk of postoperative complications in patients undergoing surgery for left-sided colonic benign disease, patients with colorectal cancer who have oncologic emergencies, and those with poor general condition (frail or older adults) (1-3). Although HP remains an important surgical option, the achievement of stoma reversal is significantly lower than that of stoma closure after primary anastomosis (4). A permanent stoma significantly impairs patient quality of life and increases medical costs. Furthermore, previous studies have demonstrated that the achievement of stoma reversal is significantly different between benign and malignant diseases (5,6). The reason for this may be that the long-term course after stoma reversal varies depending on the underlying disease conditions.
Colostomy reversal after HP is considered a challenging surgery with a high risk of anastomotic complications and mortality (7,8). However, even in successful reversal cases in which the patient is stoma-free, several complications, such as cancer recurrence or death, can occur during follow-up, particularly in case of malignant diseases. Only a few studies have examined the long-term outcomes after reversal (9,10). To the best of our knowledge, no study has investigated long-term outcomes after reversal in benign and malignant diseases.
Therefore, in this study, we aimed to compare the achievement of stoma reversal and examine the long-term outcomes after reversal between benign and malignant disease groups in a cohort from a single institution.
Patients and methods
Study design and patient population
This retrospective observational study was conducted at the Hakodate Municipal Hospital (Hakodate, Japan). The study and manuscript adheres to the STROBE guidelines for observational studies. Patients who underwent HP for any disease between January 2005 and December 2021 in our hospital were included. HP was defined as the removal of a damaged colonic segment with the abandonment of the sutured distal colon stump and creation of an end colostomy in the upstream colonic segment (3). We excluded patients who underwent HP for gynecological or recurrent malignant diseases (because there were no cases of colostomy reversal) and died during hospitalization after HP. The patients were classified into benign and malignant disease groups according to the disease for which HP was indicated. In our department, both colorectal and general surgeons performed HP, and indications for colostomy reversal after HP were good patient condition and no major pelvic complications after HP (such as dehiscence of the rectal stump). The following situations were also considered in cases of malignant disease: no disease recurrence for at least 6 months from HP after adjuvant chemotherapy in patients who underwent curative cancer surgery, and no disease for which systemic treatment was being received in patients with distant metastasis. After HP, patients with malignant disease were regularly followed up for treatment or examination. Conversely, patients with benign disease were followed up by irregular visits alone for various reasons (including visit for any other disease and visit by emergency) or were contacted during the anorectal function survey.
Study endpoints
The primary endpoint was the difference in stoma-reversal rate between benign and malignant diseases. The secondary endpoints were predictive factors for the achievement of stoma reversal and stoma-free survival (SFS) and anorectal function after reversal in patients with benign and malignant diseases.
Data collection and assessments
Data on patient characteristics collected from the medical records included age, sex, body mass index (BMI), American Society of Anesthesiologists physical status (ASA-PS), Charlson comorbidity index (CCI), indication for HP, type of surgery for HP, surgical approach for HP, adjacent organ resection during HP, length of residual stump, postoperative complications (intra-abdominal abscess and dehiscence of residual stump), and discharge location. Surgical outcomes of stoma reversal included the surgical approach, anastomotic method, and diverting loop ileostomy. Data on postoperative complications and mortality rates were also collected. The calculation of CCI has been previously reported (11). The CCI cut-off values for predicting stoma reversal were determined based on the receiver operating characteristic curves in the benign disease and malignant disease groups separately. The CCI was classified into low and high scores according to the cut-off values (4 and 6 points in benign and malignant diseases, respectively). Residual stumps were classified as located above the sacral promontory, between the sacral promontory and peritoneal reflection, and below the peritoneal reflection. Postoperative complications were assessed using the Clavien-Dindo classification (12). The observational period was calculated from HP or stoma reversal to the last follow-up date. The SFS rate was measured based on the time from reversal.
Anorectal function was evaluated before HP (pre-HP) and after reversal (post-reversal) using the low anterior resection syndrome (LARS) score, a categorical scoring system. The patients' LARS scores were graded into three categories: No LARS (LARS score <20), minor LARS (LARS score between 21 and 29) and major LARS (LARS score >20). The survey targeted patients who were alive in September 2022. Pre-HP function was retraced and assessed at the time of the survey.
Statistical analysis
Categorical variables are summarized as frequencies and percentages. Continuous variables are summarized as mean ± standard deviation or median (interquartile range). Between-group comparisons were performed using Welch's t-test for continuous variables or Mann-Whitney U test for categorical variables. In addition, Fisher's exact test was used to compare the frequencies of categorical variables. Comparisons of two measurements between pre-HP and post-reversal functions from the same patient were performed using Wilcoxon signed rank test. Comparisons between the three groups were performed using Kruskal-Wallis rank sum test. The cumulative stoma-reversal rate was estimated and compared between the groups using the Gray test. Predictive factors for stoma reversal were analyzed using univariate and multivariate analyses with the Fine-Gray regression model. Variables with P<0.05 in the univariate analysis were entered into the multivariate analysis as covariates. The SFS was calculated using the Kaplan-Meier method and compared between the groups using the log-rank test. P<0.05 was considered to indicate a statistically significant difference. All statistical analyses were performed using EZR (version 1.61; Saitama Medical Center, Jichi Medical University, Saitama, Japan), a graphical user interface for R (version 4.2.2; The R Foundation for Statistical Computing, Vienna, Austria) and a modified version of R Commander (version 2.8-0) designed to add statistical functions frequently used in biostatistics (13).
Results
Patient flow and characteristics between the benign and malignant disease groups
A total of 324 patients who underwent HP for any disease between January 2005 and December 2021 were eligible for the study. However, 23 patients who underwent HP for gynecological or recurrent malignant diseases and 40 who died during hospitalization were excluded. Eventually, 261 patients were included in this study. Among these, 102 and 159 patients were included in the benign disease and malignant disease groups, respectively. The stoma reversal was performed in 44 patients (16.9%). Among them, 24 (77.4%) of the 31 survivors in September 2022 underwent assessments of anorectal function. The patient flowchart is shown in Fig. 1. The characteristics of the 261 patients are presented in Table I. There were significant differences in sex, ASA-PS, type of surgery for HP, surgical approach for HP, adjacent organs resection during HP, length of the residual stump, and discharge location between the benign and malignant disease groups.
Predictive factors for stoma reversal and cumulative stoma-reversal rate between the benign and malignant disease groups
The results of univariate and multivariate analyses of the predictive factors for stoma reversal are summarized in Table II. CCI, indication for HP, type of surgery for HP, and discharge location were independent predictive factors for stoma reversal. Fig. 2 shows that the cumulative stoma-reversal rate in the malignant disease group was significantly lower than that in the benign disease group (26.4% vs. 7.3% at 1 year after HP and 33.6% vs. 16.7% at 3 years after HP, P<0.001 by the Gray test). The indications for HP, stoma-reversal rate, and time-to-reversal are shown in Table III. The most common indications for HP were diverticular disease and colorectal cancer with obstruction in patients with benign and malignant diseases, respectively. The mean time-to-reversal for benign and malignant diseases were 11.0 and 12.6 months, respectively (P=0.526). Among 159 patients with malignant diseases, very few patients with distant metastasis underwent stoma reversal compared to those without distant metastasis (4.5% vs. 17.2%, P=0.023). External causes had a high reversal rate (57.1%) regardless of the primary cause.
Surgical outcomes of stoma reversal and stoma-free survival after reversal
The surgical outcomes in the 44 patients who underwent stoma reversal are shown in Table IV. The laparoscopic approach was the most common surgical approach in the benign disease group, and open surgery the most common strategy in the malignant disease group. The length of the residual stump, anastomotic method, diverting stoma, postoperative complication grade, mortality rate, and duration of postoperative follow-up were not significantly different between the benign and malignant disease groups. One patient with diverting loop ileostomy during reversal underwent ileostomy closure approximately 4 months after colostomy reversal. Owing to anastomotic complications on day 1 after reversal, one of the 25 patients with benign disease underwent stoma recreation (second Hartmann's operation). However, the patient's stoma was not reversed. Among the 19 patients with malignant disease, 1 underwent stoma recreation (ileostomy) because of anastomotic complications on day 7 after reversal, and the stoma was closed approximately 3 years after the recreation. Three patients underwent stoma recreation owing to cancer recurrence in the pelvis (transverse colostomy for peritoneal recurrence in one patient with stage III cancer with a 7.9-month interval to reversal, a second Hartmann's operation for local recurrence in a patient with stage II cancer with an 11.3-month interval, and Mile's operation for local recurrence in a patient with stage IV cancer with an interval of 10 months). Their stomas became permanent. Fig. 3 shows the Kaplan-Meier curves for SFS after reversal in the benign and malignant disease groups. The SFS was significantly decreased in the malignant disease group with time elapsing from reversal, compared with the benign disease group (benign disease vs. malignant disease using the log-rank test, 1-year SFS: 96.0% vs. 83.9%, P=0.214; 3-year SFS: 83.1% vs. 50.6%, P=0.036; 5-year SFS: 83.1% vs. 50.6%, P=0.036, 10-year SFS: 83.1% vs. 36.4%, P=0.004).
Assessments of anorectal function
The post-reversal LARS scores of the 24 patients were significantly worse than their pre-HP scores (P=0.017). Post-reversal minor LARS occurred in four patients (16.7%), and post-reversal major LARS in four patients (16.7%). The post-reversal LARS scores and the occurrence of post-reversal LARS were not significantly different between the benign and malignant disease groups. Subsequent analysis based on the length of the residual stump revealed that post-reversal LARS scores were significantly lower when the residual stump was short by Kruskal-Wallis rank sum test (P=0.023). Residual stumps below the peritoneal reflection were associated with major LARS. The results of anorectal function are summarized in Table V.
Discussion
This study revealed that malignant disease was an independent significant predictive factor for stoma reversal in the multivariate analysis. Moreover, the cumulative stoma-reversal rate was lower for malignant than for benign disease, although After reversal, SFS was significantly reduced in the malignant disease group compared to benign disease group as the time from reversal elapsed. The was comparable in terms of functional outcomes between the groups.
The HP remains an important surgical option due to the increasing incidence of colorectal cancer and diverticulosis of the left colon worldwide and in Asian countries, respectively (14). The rate of stoma closure was reported to be lower after HP than after primary anastomosis (4). In particular, the stoma closure rate after HP was different between benign and malignant diseases (5,6). Our findings showed that the cumulative stoma-reversal rate was significantly different between benign and malignant diseases. Additionally, among malignant diseases, advanced cancers with distant metastasis have significantly lower rates of stoma reversal. This may be because the timing of stoma reversal is missed owing to ongoing treatment for distant metastasis after HP.
Furthermore, our findings demonstrated that low CCI, urgent surgery, and home discharge were independently associated with a higher stoma-reversal rate. The CCI score reflects the age and comorbidities of the individual and represents their background (11). Royo-Aznar et al (5) reported that patients with a low CCI had a higher rate of stoma reversal. In this study, the achievement of stoma reversal was not significantly associated with ASA-PS at the time of HP while it was significantly associated with CCI. If patients with severe systemic disease at the time of HP (high ASA-PS) recovered, had a low CCI, and were discharged home, they had a good chance of reversal. Urgent surgery meant that HP had to be performed and it was a lifesaving procedure. In such cases, the patient has a good chance of reversal if they recover. Our data could help surgeons provide accurate information for patients and their families about the prospect of colostomy closure or a permanent stoma prior to obtaining informed consent.
The colostomy reversal after HP is a difficult surgery with a high risk of anastomotic complications and mortality (7,8). However, with the introduction of minimally invasive techniques (14-18), the incidence of complications after reversal has lowered (19-22). Therefore, the indications of colostomy reversal after HP can now be expanded. Although there are many reports on short-term outcomes after reversal (22,23), only a few studies have examined its long-term outcomes (9,10). We speculate that the long-term follow-up of patients after reversal may result in the identification of complications such as cancer recurrence in patients with malignant disease and anorectal disorders. These issues require further investigation.
Because patients with malignant disease undergoing HP often have colorectal obstruction or perforation, subsequent disease recurrence may occur even if the reversal is successful (24,25). In this study, stoma recreation was required in three cases of cancer recurrence in the pelvis. For malignant diseases, an appropriate indication for colostomy reversal, such as setting an adequate interval between surgeries, may avoid unnecessary challenging surgery. As mentioned earlier, in our center, colostomy reversal after HP is indicated when there is no disease recurrence for at least 6 months post-HP and after adjuvant chemotherapy in patients who underwent curative cancer surgery, and there is no disease progression in patients with distant metastasis controlled by systemic therapy. Although there was no significant difference, the interval from HP to reversal in the 3 patients who underwent stoma recreation owing to cancer recurrence was shorter than that in the remaining 16 patients in the malignant disease group (9.6 months vs. 13.1 months, P=0.090). A previous study reported the time-to-reversal of 282 days (9.3 months) for malignant disease (6). Determining the appropriate interval for reversal could be the object of future research. Additionally, it is important to obtain informed consent before stoma reversal in patients with malignant disease owing to the risk of recurrence.
Few studies have examined anorectal function after reversal. In their study of 64 patients with colostomy reversal, Van Hoof et al (10) reported that 15.6 and 17.2% of patients had minor LARS and major LARS, respectively. Caille et al (9) stated that among 21 patients who underwent reversal after HP due to failure of the previous anastomosis, 33.3% reported minor LARS and 23.8% reported major LARS. In our study, 16.7% of 24 patients reported minor LARS and 16.7% reported major LARS. This result is comparable to those shown in previous studies. Furthermore, the present study revealed no significant differences in anorectal function between those with benign and malignant diseases. However, a short residual rectal stump could be associated with poor function. Although there were only two patients with residual stumps below the peritoneal reflection, they experienced major LARS. Interestingly, a previous study demonstrated that the length of the rectal stump did not differ significantly among patients with no, minor, and major LARS (10). Further studies will be required to investigate the association between anorectal function and the length of residual stump. Based on our finding of predictive factors for stoma reversal, we suggest that interventions such as pelvic floor muscle exercises should be considered before reversal for patients with a high likelihood of reversal and a short residual stump.
This study had some limitations. First, we retrospectively collected data from the surgical database and medical records in a single center. Second, the number of participants was small and the rate of stoma reversal was low to examine each variable related to the outcomes. Multicenter studies with large samples and minimal bias are required for more reliable statistical analyses. Third, due to the retrospective nature of this study, it was difficult to obtain data on whether patients desired stoma reversal. Some patients may have been satisfied with a permanent stoma and therefore did not seek reversal, which could have resulted in an underestimation of the stoma reversal rate. Fourth, both colorectal and general surgeons performed HP, and stoma reversal decisions were primarily based on patient condition rather than surgeon specialty. However, colorectal surgeons predominantly treated malignant diseases, and their surgical strategies may have influenced the observed trends. Fifth, the time between stoma reversal and the survey for post-reversal anorectal function varied from case to case, which may have influenced the functional results. Sixth, because pre-HP anorectal function was retraced and assessed at the time of the survey, the actual function may not have been accurately represented. Further prospective studies are required to overcome these limitations. Seventh, follow-up methods differed between benign and malignant diseases. In particular, patients with benign diseases were not followed up regularly. This may underestimate the stoma-reversal rate in patients with benign diseases. However, because the follow-up period for benign diseases was relatively long and there was no significant difference in the follow-up period, we believe that this impact was not so large. The reason for this is that our hospital is located in the southern area of Hokkaido, which has few healthcare resources, and patients have few opportunities to visit other medical institutions.
In conclusion, our findings indicated that the stoma-reversal rate and SFS after reversal could be worse in patients with malignant disease than in those with benign disease, although anorectal function after reversal was not significantly different. The postoperative long-term course of HP may vary between patients according to the indication for HP. Enforcement of HPs should be carefully considered, taking these circumstances into account.
Acknowledgements
The authors would like to thank Professor Yohei Kawasaki, Ph.D. (Institute for Assistance of Academic and Education) for the advice on statistical analysis.
Funding
Funding: This study was supported by the Japanese Society for the Promotion of Science KAKENHI (grant no. 23K19492).
Availability of data and materials
The data generated in the present study may be requested from the corresponding author.
Authors' contributions
KIm, HK, AS, KS, KIt, TF, KIc, TO, DY, YT, MU, MK and KN conceptualized and designed the study. KIm and HK confirm the authenticity of all the raw data. KIm wrote the manuscript and performed the statistical analyses. KIm, HK, AS, KS, KIt, TF, KIc, TO, DY, YT, MU, MK and KN performed the operations and collected clinicopathological data. KN supervised the study. KIm, HK, AS, KS, KIt, TF, KIc, TO, DY, YT, MU, MK and KN interpreted the results and wrote the report. All authors read and approved the final version of the manuscript.
Ethics approval and consent to participate
The present study was approved by the Human Research Ethics Committee of Hakodate Municipal Hospital (Hakodate, Japan; approval nos. 2021-84 and 2022-228). Furthermore, the study was conducted in accordance with the tenets of the 1964 Declaration of Helsinki and its later amendments. All patients gave their consent through the opt-out method.
Patient consent for publication
All patients gave their consent through the opt-out method.
Competing interests
The authors declare that they have no competing interests.
Authors' information
ORCID IDs: KEN IMAIZUMI, 0000-0002-7751-6270; AYA SATO, 0000-0002-4231-2315; KENTARO SATO, 0000-0002-1765-7477; KENTARO ICHIMURA, 0000-0002-2838-4240.
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