Research Article
Austin J Radiat Oncol & Cancer. 2015; 1(3): 1014.
Abdominoperineal Resection is Associated with a Poor Outcome Compared with Anterior Resection for Rectal Cancer: A Meta-Analysis
Yen-Chien Lee1*, Chung-Cheng Hsieh2 and Jen- Pin Chuang1
1Department of Oncology, Tainan Hospital, Ministry of Health and Welfare, Tainan, Taiwan
2Department of Cancer Biology, University of Massachusetts Medical School, Worcester, UK
*Corresponding author: Yen-Chien Lee, Department of Oncology, Tainan Hospital, Ministry of Health and Welfare, ROC.No. 125, Jhongshan Rd, Tainan, Taiwan
Received: November 16, 2015; Accepted: December 01, 2015; Published: December 03, 2015
Abstract
Background: It’s controversies whether Anterior Resection (AR) is superior to Abdominoperineal Resection (APR) for rectal cancer. To solve this question, a meta-analysis was performed.
Methods: Studies published from 1990 to May 2014 evaluating outcomes after AR and APR for rectal cancer were identified by an electronic literature search. A meta-analysis was performed to compute Hazard Ratio (HR) along with 95% Confidence Intervals (CI). We extracted HRs of Disease-Free Survival (DFS) and Overall-Survival (OS) compared these two methods using a randomeffects model.
Results: Twenty four studies met the inclusion criteria, yielding a total of 21,221 patients. Pooled adjusted HRs were 1.276 (95% CI, 1.266 -1.287) for DFS and 1.130 (95% CI, 1.126-1.133) for OS that compared APR with AR. Sensitivity analyses were performed and APR was still associated with poor prognosis.
Conclusion: APR has been associated with poor prognosis compared with AR. While possible, a more radical operation, extralevator abdominoperineal resection should be considered.
Keywords: Rectal cancer; Meta-Analysis; Abdominoperineal resection; Disease free survival
Introduction
Colorectal cancer is the third most commonly diagnosed cancer in males and second in females [1]. It is also one of the leading causes of cancer mortality worldwide, and rectal cancer accounts for 30 to 35% of these cases [1].
Miles, who introduced Abdominoperineal Resection (APR) in 1908, based his work on that the spread of tumors of the lower rectum occurred through the lymph nodes outside the levator ani muscles. APR was thought to address this problem. Anterior Resection (AR) was later introduced for proximal rectal cancers. Improvements in stapling technology over the following decades have resulted in an increase in the number of sphincter-saving operations [2]. The more important recent advance in rectal cancer surgery has been the Total Mesorectal Excision (TME). TME is defined as sharp pelvic dissection between the parietal and visceral planes of the pelvic fascia and it has been introduced since 1982 by Heald [3]. TME and precise perimesorectal plane dissection were introduced in all the major countries of Europe in 1995 [4]. Local recurrence rate can decrease to less than 10% for middle and lower rectal carcinomas with this procedure [5]. Following several workshops and operative demonstrations around the world, TME is now generally accepted as the standard procedure for rectal cancer [6].
Previously APR was thought to be able to eradicate border field than AR and achieve better outcomes in disease free survival or even overall survival. Others suggest otherwise [7-10]. It’s not clear if the worse outcome associated with APR is a result of surgical procedure or patient- and tumor-related factors. Many studies have tried to explicate these relationships. Possible reasons for high local recurrence of APR compared with AR include the higher incidence of inadequate margin [11] or lymph node involvement that may follow a different pattern in low rectal carcinomas. Very low cancers have a dual lymphatic drainage [12]. Tumor or rectal perforation are other important factors that might contribute to poorer outcomes in APR.
However, due to tumor nature and anatomic reason, further randomized-controlled trials would not be feasible to compare these two methods. This question has been further complicated by different neoadjuvant, adjuvant, and chemotherapy agents. Since prospective randomized studies comparing APR with AR are ethically unavailable, we try to answer this question from previous studies through metaanalysis. This is the first meta-analysis that attempts to answer this question.
Method
Search strategy and Selection criteria
We systematically searched Pub Med and Medlines for relevant articles published up to May12, 2014, with the following search terms, “anterior” and “rectal cancer, “abdominoperineal” and “rectal cancer” without language restriction. Additional search methods included manual review of the reference lists of relevant studies. Studies were included if the following were true: (1) they were published with extractable information on disease free survival (DFS) or overall survival (OS); (2) they were primary rectal cancer. Chemotherapy was not used in patients with rectal cancer during the late 1990s. Whether adjuvant was used or not are included as well. Studies before 1990 were excluded. Kaplan-Meier DFS or OS graph with three or fewer outcome events was considered as inadequate and was excluded. Only original articles were included; posters, abstracts, and conference reports were excluded.
Information on age and stage were extracted when available and taken into account in the analysis. Abdominoperineal excision was often involved positive circumferential resection margins [13] which has been associated with a poor prognosis [14]. Due to variable factors adjustments in each studies, if any one of stage, age or margin were included in original studies for adjustment, the HR were considered as multivariate analysis.
We assessed the methodologic quality of included studies using the Newcastle-Ottawa Scale [15] for determining the quality of individual cohort studies included in the meta-analysis.
Statistical analysis
We extracted HR by direct or indirect methods [16] based on the available information provided in the selected articles. If information for applying these methods was not available, a graph methods, which stratifies the published survival curve into nonoverlapping intervals to estimate the log HR, was used to extract the HR [16]. Summary HRs were obtained using the random-effect model. Forest plots were used to display the study-specific HRs and the summary estimates. Heretorgenetiy among the studies was tested with Q statistics. Analyses were conducted with Stata version 12.0 (Stata Corp, College Station, TX). Two-sided p values <0.05 were regarded as statistically significant.
Results
Literature search
The steps of our literature search are shown in (Figure 1). After reviewing titles and abstracts, 104 potential papers were extracted to review in full. Two papers [17,18] were from two different but overlap periods of the same hospital. Due to one paper provided information to overall survival and the other to disease-free survival without double weighting. Both of the papers were included.
Four articles were excluded due to language problem [19-22]. Four other articles were excluded due to unavailable in our setting [23-26]. Two of the four were from the same Chinese journal. As for the rest, one is excluded due to a short report [27]. One is excluded due to abdominosacral resection instead of abdominoperineal resection [28]. One is excluded due to use chi-square test for survival data [29]. Some paper with hazard ratio of local recurrence only [30]. Two paper is excluded due to less or equal to 3 events and was unable to extract hazard ratio from survival curve [31, 32]. Two were excluded due to more than 3 survival curve and unable to extract [33,34]. Others were excluded due to no extractable hazard ratio (HR) of DFS or OS. Methodological quality scores ranged from 4 to 9 on a scale of 10 (Table 1). With regard to the quality of the studies, 21 trials (87.5%) showed a high-quality score (6 points). The distribution of total scores for the 24 studies were as follows: 4 (1 study), 5 (2 studies), 6 (2 studies), 7 (4 studies), 8 (12 studies) and 9 (3 studies). Because most of the studies received a score of 6 or above and the standard criteria have not been established, we considered the studies to be of adequate quality for the analysis.
Study characteristics
We identified 24 eligible studies [7,8,17,18,35-54] published from 1990 to 2014 (Table 2a). There were 21,221 patients included in these studies (Table 2b). All were retrospective cohort studies except one matched retrospective cohort study. [18] Fifteen studies were from Europe, two studies from United States and seven studies from Asia. Patients received variable radiation and chemotherapies. The predominant chemo radiation therapy regimens and adjuvant chemotherapies were 5-fluorouracil-based.
HRs of data from one article was calculated by the direct methods, 16 by the indirect methods, and seven by the graph method. The median age of the patients was around 60 years, and the majority of the patients were men. Most studies calculated the start points from the date of primary treatment (surgery) except one [7] that started from the diagnosis date (Table 3). Eight out of the 24 studies did not provide information on HRs of disease-free survival or overall survival.
Disease free survival and overall survival
As univariate analysis (Table 2b), six out of 24 had information of disease-free survival, the pooled HR compared APR with AR was 1.311 (95% CI, 1.272-1.352). There was significant heterogeneity (p<0.001, Figure 1a). HRs from nine studies on OS was 1.264 (95% CI, 1.257-1.270), also with significant heterogeneity (p<0.001, Figure 2a).
As for multivariate HR of DFS, studies were adjusted different for stage, age and margin (Table 2b). Combining five papers HRs on DFS adjusting variable for stage, ages and margin, [39, 42, 44, 46, 54] the pooled HR comparing APR with AR was 1.276 (95% CI, 1.266-1.287), again with significant heterogeneity (p<0.001, Figure 1b). Multivariate HRs of OS [7,8,17,18,36,38,43,47-49,51] adjusted variable for stage (eight studies), age (eight studies) and margin (five studies) was 1.130 (95% CI, 1.126-1.133) (Table 2b). There was a statistically significant heterogeneity among studies (p<0.001, Figure 2b).
Sensitivity analyses
Potential sources of heterogeneity include tumor location of the rectal cancer, geographical region where the study was conducted and year of the treatment. Also, age was adjusted for with different methods. To assess if any of these factors causing heterogeneity, subgroup analysis were performed within stratum of the relevant study features. Subgroup analyses were performed for tumor located within 12cm of anal verge. Subgroups for different regions of Europe and Asia were analysis and for those received operation within 10 years (2004) as well.
Heterogeneity was equally evident in all strata except DFS in studies conducted in Asia and for tumor within 12cm anal verge (data not shown). However, the studies numbers were small. Nonetheless, APR continues to show a poor prognosis as compared with AR in different subgroups.
Discussion
Cancers of the lower rectum have a less favorable oncologic outcome compared with those situated at upper locations [8, 55- 57]. Lower rectal carcinomas had a twice chance of circumferential margin involvement compared to tumors situated over 5 cm from anal verge (26.5% v 12.6%). After chemo radiation therapy, AR might be performed as well. In lower rectal carcinoma, three times more positive margins were present in patients operated by APR than AR (30.4% v 10.7%) [58]. In the late nineteenth century, APR was the standard operation for lower rectal cancer. Due to the development of stapler technique, AR was later more widely adopted. Previously APR was thought to have better survival due to the wider dissection [37]. However, later studies showed that APR was associated with poor survival due to involvement of more positive margins [13,48] or perforation, [48] higher local recurrence rates, and poorer survival of low rectal cancer [58]. Even after adjusting for margins and perforation, APR was still associated with a poor prognosis [44]. Among the studies included in our analysis, most of the HRs for OS were adjusted for stage, age and margin and APR was still associated with a poor prognosis. The median tumor level located from anal verge also lower in the APR group than in the AR group [48]. In early 1990s, TME was not widely adopted but now it was current standard of treatment. TME cannot always be performed [9] because of the presence of a large tumor around this lower level. Visualization and access at the floor of the pelvis are limited. Nevertheless 18 out of 24 (75%) studies stated that they had performed TME on all study patients with 2 studies of variable performing TME.
In our analysis, we showed that APR was associated with poor disease free and overall survival even after adjusted for age, margin and stage. Though we found a significant heterogeneity in the pooled disease free survival or overall survival of APR compared with AR, all the analysis and most of the subgroup analyses showed the poor prognosis associated with APR while compared with AR. The heterogeneity might due to patient racial composition or difference in age adjustment. Holm T et al., [36] indicated that they had adjusted for age without a detailed description. Some studies adjusted for age with variable cut points [38] or with propensity score [8]. One study adjusted for age at cut point of 65 year-old [42] while others at 80 year-old [47] or 72 year-old [48]. Also, variable definitions of clear margin were used. The proximal, distal, and circumferential resection margins free from tumor instead of tumor involvement within 1 mm of the circumferential resection margin (CRM positive) were used by Anderin C et al., [48] while others did not provide a clear definition.[36] Radiation therapy has been a standard care for T3 rectal cancer [59]. Since the introduction of radiotherapy, local recurrence has been reduced from 11.4% to 6.1% [60]. Radiotherapy has been considered as standard therapy for stage II and III rectal cancer. However, radiation therapy has only shown a marginal effect in improvement. Due to the lack of strong evidence specifically for rectal cancer, support for the use of adjuvant chemotherapy in patients with rectal cancer is generally extrapolated from the data available for colon cancer [61].
P. How et al., [10] has published a review article of “a systematic review of cancer related patient outcomes after anterior resection and abdominoperineal excision for rectal cancer in the total mesorectal excision era” in 2011. They suggested that tumours treated by APR were lower and more locally advanced. They suggested that surgical technique itself for the tradition APR was also inadequate and resulted in poor outcomes. The results of our meta-analysis support their conclusion as well.
In recent years, a more extended approach, later called the extralevator abdominoperineal resection, has been propose by T. Holm [62]. Review article suggested that extended APR such as cylindrical resection was associated with a lower rate of radial margin involvement and improved local control rate compared to conventional APR [63]. A meta-analysis has confirmed this finding [64].
Up to 90% of patients undergo sphincter-preserving surgery will subsequently have a change in bowel habit, ranging from increased bowel frequency to fecal incontinence or evacuatory dysfunction. These have been called anterior resection syndrome [65]. An uncertain preference for one or the other surgical procedure cannot be discerned, particularly a prospective study [66] and a meta-analysis [67] on the quality of life following APR vs. AR had failed to show a superiority of AR.
Some might argue that the surgical indications for APR were different from anterior resection. Decision was based on the location of the tumor. Difference in tumor locations could also reflect a difference in tumor biology in term of spread. To answer this theory, one should compare APR vs anterior resection in upper 2/3 rectal cancer which might seem impossible due to unethical. However, as we could see that 7 out of 24 inclusions studies were from lower rectum (8cm) (Table 2A). Among them 3 papers were available for univariate OS analysis. It still showed that APR were worse than LAR (HR 1.509, 95% CI, 1.439-1.582) but non-significant after adjusted for age or margin (HR 0.954, 95% CI, 0.761-1.193) (data not shown).
Rectal cancer treatment was a rather complex issue. Surgical options including LAR or APR were performed by tumor location and the extent of tumor invasion. Despite of several trials have been done to compare the long term outcome of this two surgical options, there was still no consensus nor guideline to follow. The major reasons may be small size in each trial or dispersed distribution of rectal cancer in different patients or even each surgeon’s personal favor in certain surgical procedure. In order to solve these problems, meta-analysis could provide a more robust evidence to this important clinical issue.
Further study might be needed whether the poor prognosis is due to rupture during the operation. Due to the poor prognosis of APR compared with AR, extralevator abdominoperineal resection [64] might be another choice while APR were deem unsuitable.
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