Abstract
Introduction
Endoscopic mucosal resection (EMR) is an invaluable technique, however it is associated with significant risks. In the elderly in particular, the long-term survival benefits of polyp resection with EMR are unknown. The aim of this study was to determine the long-term outcomes in elderly patients who had undergone EMR and to identify any adverse factors.
Method
A retrospective observational study on patients of 75 years of age or greater, who underwent EMR of colorectal polyps, in a single tertiary centre, from 2005 to 2014. Demographics of the patients, including Charlson Comorbidity Index (CCI), endoscopic and histological data, were reviewed to identify potential factors predicting outcomes.
Results
The patients’ median age was 80 years. In total 239 procedures were performed in 206 unique patients. The complication rate was 1.6%. Mean overall survival was 6.7 years with only one patient dying from metastatic colorectal cancer (0.5%) and 49 dying from non-colorectal cancer conditions (24%). Age more than 79 years and CCI more than 2 were independent predictors of significantly shorter survival (p=<0.01). Gender, size of the removed polyps and total number of polyps were not statistically significantly affecting survival. Patients who had more than two colonoscopies were found to have a survival benefit (p=0.02).
Conclusion
EMR of colonic polyps is safe even for elderly patients. However, the decision to proceed to complex endoscopic therapy should be individualised considering the patients’ age and comorbidities. CCI can help to objectively assess the comorbid state of a patient prior to such decisions.
Keywords: endoscopic polypectomy, elderly, colonic polyps
Significance of this study.
What is already known on this topic
Endoscopic mucosal resection (EMR) of colorectal polyps is an invaluable technique for the removal of colorectal polyps, however continuing colonic surveillance and higher risk polypectomies in the elderly (>75 years) can be controversial.
What this study adds
We confirmed that EMR of colonic polyps remains safe in an elderly population with comparable complication risks as previously reported in younger patients. Unsurprisingly the long-term outcomes are significantly affected by the comorbidities and age of each individual patient. This study has shown that the Charlson Comorbidity Index (CCI) may be a useful tool to help in risk-benefit decision-making for elderly patients potentially undergoing this therapeutic endoscopic intervention.
How might it impact on clinical practice in the foreseeable future
The decision to undertake an EMR of a colonic polyp in an elderly patient needs to be individualised. Introducing the CCI as an assessment preprocedure can offer objective assessment of the comorbid state and lead to safer decision-making.
Introduction
Removal of adenomatous polyps can prevent advancement to malignancy1 and thus reduce morbidity and mortality from colorectal cancer (CRC).2–6 This has been demonstrated by the bowel cancer screening programme. Endoscopic mucosal resection (EMR) is an invaluable technique in removing large or complex polyps, however, it is not without risks. A recent systematic review of 50 studies outlined significant risks associated with the procedure such as perforation (1.5%), bleeding (6.5%) and even death (0.08%).7 In view of these risks, each case needs to be selected individually with a risk to benefit basis.
Age is an important factor in the pathophysiology of CRC. It has been shown that there is an increased incidence of CRC arising from sporadic adenomatous polyps associated with an increasing age.8 9 Studies have underlined the importance and benefits of screening for CRC, however, identifying an age of cessation of screening, when the benefits no longer justify its continuation, remains controversial. The patients’ age alone cannot be the only factor when considering the eligibility of screening, as pre-existing comorbidities are an important co-founder in predicted survival. Consequently, a number of scoring systems have been developed to standardise the assessment of comorbidities in various studies, for example, the Charlson Comorbidity Index (CCI).10
In the elderly, the long-term survival benefits of polyp resection with EMR are unknown given their potential life expectancy. The aim of this study was to determine the long-term outcomes in elderly patients who had undergone EMR and to identify any adverse factors.
Methods
This was a single-centre study performed at the Royal Liverpool University Hospital as part of a registered service evaluation audit with a study period between July 2005 and November 2014.
Patients selected were all patients aged 75 years and above, undergoing EMR of colonic polyps. The patients were identified through the audit tools of the endoscopy reporting software (GI Reporting Tool—UNISOFT Medical Systems).
Study design
A retrospective observational approach was adopted to complete this study. Data were collected from patients’ notes and their electronic patient record, including clinic letters, trust results system, discharge summaries and the GI Reporting Tool report of their procedure.
The CCI11 for each patient was retrospectively calculated according to relevant clinical information from the time period at which the EMR was performed. All subjects were followed until death or study censure date. Survival time was calculated as the interval from the index colonoscopy to death or study censure date; subjects with incomplete follow-up were censored at the time of their last documented follow-up. The underlying distribution of each continuous variable was assessed. These variables were modelled as continuous, but results are presented as post hoc categorised data. Size of polyps was handled as a categorical variable due to reasons of clinical interpretability.
Inclusion and exclusion criteria
Inclusion criteria
All patients of at least 75 years of age, who underwent an EMR colonic polypectomy, as reported by the performing endoscopist, from July 2005 to November 2014. EMR was defined by the performing endoscopist and chosen as a fixed set therapeutic intervention for polypectomy on UNISOFT.
Exclusion criteria
Patients younger than 75 years old were excluded from the study.
Polypectomies, which were not classified as EMR by the performing endoscopist on the endoscopy report.
Statistical analysis
Descriptive statistics were used to characterise the demographic and clinical features of the cohort. The mean survival time and associated SD are calculated using a restricted approach with upper limit of the maximum observed time.
Cox regression was used to analyse the predictors of mortality after the index colonoscopy. Backward selection via Akaike’s information criterion was used to select each variable in the multivariable model. The Kaplan-Meier method was used to estimate overall survival. All statistical analyses were performed with R V.3.2.3 software. Patients with missing values for any of the covariates were removed from the analysis. A p value <0.05 was considered to be significant.
Results
Two hundred and thirty-nine procedures were included; these were performed in 206 unique patients. Patient characteristics can be seen in table 1. The median age of the patients was 80 (range 78–83) and there was a slight male preponderance (55%).
Table 1.
Patient demographics, colonic polyp details and survival outcomes
| n | |
| Age (years), median (IQR) | 80 (78–83) |
| Charlson Index, median (IQR) | 1 (0–2) |
| Repeat colonoscopies, median (IQR) | 1 (0–2) |
| Gender | |
| Male | 114 (55%) |
| Female | 92 (45%) |
| Size of polyps (categorical) | |
| 1–9 mm | 28 (14%) |
| 10–19 mm | 61 (30%) |
| ≥20 mm | 114 (55%) |
| Missing | 3 (1%) |
| Number of polyps | |
| 1 | 121 (59%) |
| ≥2 | 85 (41%) |
| Histology | |
| Low-grade dysplasia | 146 (71%) |
| High-grade dysplasia | 38 (18%) |
| Malignancy | 14 (7%) |
| Hyperplastic | 8 (4%) |
| Mean survival, months (SE) | 80.63 (4.49) |
The median follow-up was 30 months (IQR 15, 51). The median size of the polyp resected was 20 mm (IQR 12, 30). Eighteen per cent were found to have high-grade dysplasia (HGD) with 7% having a malignant component. The vast majority was low-grade dysplasia (LGD; 71%).
Sixty-five patients (31.6%) had a single EMR procedure and had no further endoscopies. Fifty-eight patients (28.2%) had one more endoscopy after the EMR and the remaining 83 patients (40.2%) had two or more endoscopies after the EMR.
Complications
Four of the cases had reported complications (1.6%). In two cases (0.8%), bleeding was reported as an immediate complication but was managed conservatively. Another two cases (0.8%) had cardiopulmonary complications, one of which was respiratory depression related to the sedation and the other a cardiovascular compromise related to a hyoscine butylbromide-induced arrhythmia. Ten patients (4.2%) were readmitted within 7 days. None of the patients required surgery due to a complication.
Mortality
Two patients died in a relatively short period after the procedures: an 82 years old and a 78 years old who both died from cardiac causes within 1 and 2 months, respectively.
The 10 years’ mortality in our cohort was 26.4% and the 5 years’ mortality was 21.6%. The probability of survival can be seen in figure 1. One patient died as a result of CRC. Fifty-three patients died during the follow-up period of the study. The main causes of death of all patients are described in table 2. The cause of death could not be identified in eight cases, who moved out of area of our institution, and the death certificate could not be retrieved.
Figure 1.
Probability of survival curve for all patients following endoscopic mucosal resection (EMR) for colonic polyp. The solid line is the mean survival, with the dotted lines illustrating 95% CIs.
Table 2.
Causes of death
| Cause of death | n |
| Sepsis | 19 |
| Cardiac causes | 9 |
| Cancer | |
| Lung | 3 |
| Prostate | 2 |
| Cholangiocarcinoma | 1 |
| Pancreas | 1 |
| Colorectal | 1 |
| Other causes | |
| Advanced dementia | 2 |
| Pancreatitis | 1 |
| PTLD | 1 |
| Renal failure | 1 |
| Duodenal bleed | 2 |
| Respiratory failure | 1 |
| Suicide | 1 |
| Unknown | 8 |
PTLD, post transplant lymphoproliferative disorder.
Histological outcomes
From the 206 patients studied, the majority, consisting of 146 patients, were found to have only LGD. Thirty-seven patients were found to have lesions with HGD, while 14 were found to have lesions harbouring malignancy.
Patients with HGD
Of the 37 patients with HGD, three underwent a surgical resection. One of them died, 42 months later, due to sepsis. The remaining 34 patients did not undergo surgery and eight of them died by the study censure date. Six of the deaths were unrelated to CRC, one was due to unknown causes and one was due to metastatic CRC.
Patients with malignancy
Of the 14 patients with malignancy, four had a surgical resection and at the study censure date were all still alive. The remaining 10 patients were not operated on and four of them died during the study period. Two of the deaths were unrelated to CRC (postrenal transplant lymphoproliferative disease, cardiac disease) and two died due to unknown causes (one 2 years and one 9 years after the original procedure).
Predictive factors for outcomes
The results of the univariable and multivariable analyses can be seen in table 3. Univariable analysis demonstrated age, CCI, repeat colonoscopies and the presence of HGD were risk factors for mortality following polypectomy. Specifically patients aged 80 and above were as expected more likely to die than those aged <80 (p<0.01) (HR 1.39, 95% CI 1.09 to 1.77). A CCI of 3 or 4 was associated with death following polypectomy (p<0.01) (HR 1.14, 95% CI 1.04 to 1.25) as was a CCI of more than 4 (HR 1.29, 95% CI 1.09 to 1.53). Patients with at least one repeat colonoscopy were less likely to die than those with none (p<0.02, HR 0.84, 95% CI 0.73 to 0.98).
Table 3.
Univariable and multivariable analyses of risk factors of death following EMR of colonic polyp in patients >75 years of age
| Variable | P value | Univariable HR (95% CI) |
Multivariable HR (95% CI) |
|
| Age | 76–79 | <0.01 | 1 | 1 |
| ≥80 | 1.39 (1.09 to 1.77) | 1.28 (1.00 to 1.64) | ||
| Charlson Index | <3 | <0.01 | 1 | 1 |
| 3–4 | 1.14 (1.04 to 1.25) | 1.14 (1.04 to 1.25) | ||
| >4 | 1.29 (1.09 to 1.53) | 1.28 (1.07 to 1.54) | ||
| Repeat colonoscopies | 0 | 0.02 | 1 | 1 |
| 1 | 0.84 (0.73 to 0.98) | 0.85 (0.74 to 0.99) | ||
| ≥2 | 0.70 (0.52 to 0.95) | 0.72 (0.53 to 0.97) | ||
| Gender | Male | 0.28 | 1 | N/A |
| Female | 0.72 (0.39 to 1.31) | |||
| Size of polyps (mm) | 1–9 | 1 | N/A | |
| 10–19 | 0.59 | 1.36 (0.45 to 4.17) | ||
| ≥20 | 0.67 | 1.26 (0.44 to 3.61) | ||
| Number of polyps | 1 | 0.84 | 1 | N/A |
| ≥2 | 0.94 (0.53 to 1.68) | |||
| Histology | Low-grade dysplasia | 0.03 | 1 | N/A |
| High-grade dysplasia | 0.51 | 2.16 (1.07 to 4.36) | ||
| Malignancy | 0.66 | 1.33 (0.57 to 3.08) | ||
| Other | 1.57 (0.21 to 11.71) | |||
EMR, endoscopic mucosal resection; NA, not applicable.
Multivariable analysis demonstrated age, CCI and repeat colonoscopies to be significant with a hazard risk of 1.28, 1.14 and 0.85, respectively. The directions of effect were as per the univariable results. The occurrence of a complication did not predict mortality and only one of the four reported complications died, up to the censure date of this study, 1 year later from respiratory sepsis.
Interaction between age and Charlson Index, and their impact on survival after EMR, was assessed by creating patient subgroups as seen in table 4. Those patients with a score of <3, irrespective of age, had the longest survival after EMR. CCI did not predict risk of complication (p=0.5), readmission (p=0.3) or the presence of carcinoma and HGD (p=0.5). When considering those with an individual polyp greater than 20 mm, application of the CCI is a strong predictor of mortality. This can be seen in figure 2 with immediate separation in the Kaplan-Meier curve. This begins to maximise by 5 years and is greater still by 10 years (p=0.0126).
Table 4.
Patient subgrouping according to age and Charlson Index. Includes mean survival (months) for each patient subgroup
| Age | Charlson Index | Patients | Mean survival, months (SE) |
| 75–79 | <3 | 67 | 87.7 (5.1) |
| 75–79 | 3–4 | 11 | 61.6 (6.2) |
| 75–79 | >4 | 10 | 63.9 (12.1) |
| ≥80 | <3 | 87 | 84.3 (8.1) |
| ≥80 | 3–4 | 18 | 47.5 (5.3) |
| ≥80 | >4 | 12 | 68.5 (14.2) |
Figure 2.
Kaplan-Meier curve based on those with an individual polyp ≥20 mm.
Discussion
Considering outcomes of EMR for colorectal polyps in elderly patients is important due to their potential longevity, the high preponderance of polyps in this age group and the risks of the procedure. We have presented the largest dedicated cohort of elderly patients undergoing colonic polyp EMR. Our study has demonstrated that elderly patients, as defined by patients of 75 years of age or greater, who underwent EMR for colonic polyps, had low complication rates and postprocedural survival exceeding 5 years in the vast majority (78.6%). It has also highlighted the importance of CCI and advancing age as independent risk factors for predicting survival after procedure.
The Office for National Statistics commonly quotes data on individuals aged over 65, while WHO has defined an ‘older person’ as someone ‘whose age has passed the median life expectancy at birth’, which in the UK is currently 81.2 for men and women combined.12 Defining elderly at 75 years therefore falls between these two definitions.
Inclusion in this study was not based on polyp size, but instead on the recording of EMR as the mode of polyp removal from the performing endoscopist. This has led to 14% of polyps included in the study being <10 mm. However, it is important to highlight that 55% were >20 mm. The potential for a patient to have a CRC-associated death from a polyp <10 mm is low in a cohort >75 years old. Risk of advanced dysplasia and CRC increases with an increase in polyp size, particularly those >20 mm,13 and this may to a degree explain the high rates of HGD and malignancy in our study. Furthermore, the fact that this was a single-centre study based in a tertiary centre may explain the presence of higher risk polyps referred for assessment from other centres. Polyp size at EMR did not influence mortality in our study. Other studies examining outcomes following EMR have also included polyps <20 mm,14 like in our study, these studies reported outcomes whereby the majority of lesions resected were >20 mm. Other such studies only included polyps identified to be >20 mm.15 16 None of these studies were specifically examining outcomes in the elderly or subsequent mortality. All of these studies reported postprocedural outcomes, namely procedural complications and local adenoma recurrence. Finding increased polyp size, specifically those >40 mm were associated with increased complications and polypectomy site recurrence.15–17
Comorbidity is an important factor that determines the survival of patients and a number of scoring systems have been developed to standardise the assessment of comorbidities.11 In this study we used the CCI, which is a weighted index that takes into account the number and the severity of comorbid diseases. It predicts the cumulative mortality attributable to comorbid disease. The estimated increment in the relative risk of death, from an increase of 1 in CCI proved approximately equal to that from an additional decade of age.10 11 The score has been validated and shown to independently predict adverse outcomes across a broad spectrum of conditions,17–19 including CRC.20 21 Using only the endoscopy report to assess the underlying comorbidities of our patients would lead to significant underestimation of their CCI. Therefore, we used information from all available sources, including clinic letters, discharge summaries and investigations (echocardiograms (ECHOs), angiograms, cross-sectional imaging, and so on), to calculate every patient’s individual CCI. This has led to 24.7% of our patients having a CCI of 3 or more.
Histology identified that 18% of the resected polyps contained HGD. This was associated with an increased risk of postprocedural death (p=0.03). In a study assessing 40 826 patients with a total follow-up time of 334 154 person-years, HGD in the resected polyp was identified as a predictor or death in both univariate and multivariate analyses.22 HGD as a predictor of future mortality may be related to the inferred risk of future neoplasia and in particular CRC.23 In our study the presence of malignancy did infer a future risk of death but did not achieve statistical significance, in contrast to the presence of HGD. This may be due to limited numbers of patients with malignancy and the fact that 28.5% of them underwent surgery which suggests that they were in a better comorbid state and suitable for surgical resection.
Colonoscopy is considered to be a relatively safe procedure, however, EMR of larger polyps has been reported to have an overall risk of bleeding of up to 7%24 or as low as 0.44%,25 an overall risk of perforation of up to 1.5% and a risk of postpolypectomy coagulation syndrome of up to 3.7%.24–26 Studies examining the outcomes of EMR in elderly patients are retrospective and sparse within the literature. They have differing complication rates in this cohort of patients. One study of 412 adenoma resections in 343 patients included a subcohort of elderly patients defined as 74 years of age or greater (n=80).27 They demonstrated a perforation rate of 1.2% (5/412) and bleeding rates of 8% (28/412) (4.6% early bleeding and 2.2% delayed bleeding).27 Another study examined 50 patients of which 32 were 65 years or greater. They reported no perforations and a bleeding rate was 4%.28 By comparison our study was favourable with an overall complication rate of just 1.6%, with no reported perforations and a bleeding rate of 0.8%. Our other main complication was cardiopulmonary compromise, which is unsurprising in this cohort at a rate of 0.8%. Our study also included additional performance indicators including a 7-day readmission rate of 4.2% and 30-day mortality of 0.4%.
Considering that patients with multiple comorbidities are less likely to be suitable candidates for surgery or prolonged chemoradiotherapy, therefore endoscopic treatment is an appealing approach. In our cohort, patients with a higher CCI had significantly worse 5-year survival rates compared with healthier patients. The 5-year survival rate of patients with a high CCI (>3) who underwent an EMR polypectomy of a larger polyp (>20 cm) was 62%. For patients with a low CCI the 5-year survival was significantly better at 83.5%. A Danish population study revealed that after diagnosis of CRC in patients with a CCI ≥3, the 5-year survival rate was up to 28%.29 In our study, patients aged 75–79 with a high CCI had a comparable 5-year survival compared with patients aged 80+ with a small CCI. Therefore, the decision on the appropriate management of a large colonic polyp should take under careful consideration the coexistent comorbidities as they play a crucial role in the outcome. This underlines the importance of careful assessment and reporting of all known comorbidities before undertaking endoscopy in patients of these characteristics. This further emphasises that age alone should not be used as the sole determining factor for suitability for colonic polyp EMR.
Patients who had >1 colonoscopy had increased survival following their EMR. This likely represents less comorbidities and thus more suitability for the index and any subsequent colonoscopies. Moreover, repeated colonoscopies would ensure complete excision by removal residual disease at the site, detect local recurrence and reduce the risk of missed adenomatous or even malignant lesions. In our study, 44.6% of patients who underwent EMR for a larger polyp (>2 cm) underwent at least two more subsequent endoscopies for surveillance or treatment of recurrence while 22.3% underwent at least three more procedures. Only one patient subsequently died of CRC.
The retrospective nature of our study infers some limitations. Calculating the CCI score of our patients retrospectively may underestimate their actual comorbid state. To compensate for that fact, we used all resources available to us for each individual patient. Despite our efforts we may have not identified all the comorbidities of this elderly group due to under-reporting in the clinical letters.
In order to identify our group of patients we relied on the endoscopists’ report of an EMR procedure. That may explain why 14% of the polyps resected were smaller than 10 mm. However, it is important to highlight that the vast majority of the polyps resected were significantly larger and that all the procedures were reliably defined, performed and reported by senior endoscopists. Furthermore, our survival analysis (figure 2) limited in patients with a polyp larger than 20 mm replicated our findings regarding the significance of CCI in predicting survival.
Due to the nature of our service and the wide geographic catchment of the referral area cause of death could not be recorded in all cases. Follow-up time after EMR was also truncated in some cases as some of the procedures occurring within 1 year of the closure of the study.
In conclusion, EMR of colonic polyps can be safely performed in an elderly population, without excessive complication or readmission rates. When considering a patient’s suitability for the procedure their age and CCI can be independently considered as risk factors for reduced survival following the procedure. This study therefore suggests that both age and CCl are important factors for decision-making in the elderly when considering EMR in this population. The introduction of the CCI within the preprocedure patient assessment pathway for elderly patients undergoing this therapeutic endoscopic procedure could improve the risk to benefit decision-making in these patients.
Footnotes
Contributors: All of the authors have made substantial contributions to the conception and design of the study or to the data acquisition and analysis or to the article drafting and they all concur with the submission. TS, AB and SS have written the paper, AG planned the study, AG and LB did the statistical analysis, TS and MJL collected the data, TS submitted the study and SS supervised the study.
Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Competing interests: None declared.
Patient consent for publication: Not required.
Provenance and peer review: Not commissioned; externally peer reviewed.
Data availability statement: No data are available. All the data were collected as part of a registered service evaluation audit with a study period between July 2005 and November 2014. Following statistical analysis and completion of the audit the original spreadsheets have been destroyed as per protocol to maintain confidentiality.
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