Transanal Endoscopic Microsurgery Combined with Laparoscopic Colectomy for Synchronous Colorectal Tumors: A Word of Caution

Abstract

Background:

The incidence of malignant synchronous colorectal tumors (SCRT) is between 2% and 5%, and the association of synchronous adenomatous polyps in colon cancer has been reported to be 15%–50%. Surgical resection is the primary treatment option for SCRT not amendable to endoscopic resection. Lesions in adjacent segments are usually treated with more extensive resection; however, there is still some controversy on how to best treat synchronous lesions in separate segments, especially when the rectum is involved. In this study, we aimed to report the outcome of patients with SCRT treated by laparoscopic colectomy combined with Transanal Endoscopic Microsurgery.

Methods:

Data pertaining patients undergoing combined colectomy and Transanal Endoscopic Microsurgery (TEM) between 2004 and 2014 were retrospectively collected.

Results:

141 TEM performed in the study period, 9 (6.5%) with combined laparoscopic colectomy were included. Mean age was 69.1 ± 10.6 years. There were 6 (66%) right, 2 (22%) left, and one (11%) sigmoid colectomy. All rectal lesions were benign adenomas, with mean tumor size 2.5 cm, and distance from the verge 9 ± 2.5 cm. Lesions were located in lateral rectal wall in 4, posterior in 4, and anterior in one case. Seven patients had the colectomy before TEM, and 2 had the TEM first. Mean operative time was 245 minutes (range 185–313) for the combined procedures. Median time of hospitalization was 6 days (range 4–11). Six patients (66%) had prolonged postoperative diarrhea. The final rectal pathology reports were adenoma with high-grade dysplasia (HGD) in 5 patients and adenoma with low-grade dysplasia in four cases. The colon pathology was T1 N0 in 3, T2 N0 in one, T3 N1 in one, adenoma with HGD in 2, and no residual tumor in 2 patients. Two patients underwent re-TEM for recurrent adenoma of rectum at 14 and 18 months postoperatively.

Conclusion:

The combination of TEM with laparoscopic colectomy is feasible and should be kept in mind as an alternative procedure in case of SCRT. However, more strict selection criteria should be considered and the disadvantages should be discussed with the patient.

Introduction

Colorectal cancer is the most common gastrointestinal malignancy and the second most common cause of cancer-related death in Western countries.¹ While the incidence of colorectal cancer is high, the majority of tumors are resected with curative intent (70%–80%) and colorectal cancer-related deaths account for only 20%–30% of those diagnosed and treated surgically. Approximately 55% of colorectal cancers diagnosed during screening are found to present with Stage I or II disease.²

Synchronous epithelial lesions in the colon have varied incidence. Although most colorectal tumors are solitary lesions, the incidence of malignant synchronous colorectal tumors (SCRT), defined as two or more primary cancers identified in the same patient and at the same time, is observed between 2% and 5% of colon cancers.³ In addition, synchronous adenomatous polyps in association with colon cancer have been reported to occur in 15%–50% of all colon cancers.⁴ Moreover, synchronous colorectal polyps are reported to occur in 21%–29% of patients undergoing screening colonoscopy.^5,6

The standard treatment of colorectal adenomas is endoscopic polypectomy. However, when confronted with a colon malignancy with a coexisting rectal neoplasm, most synchronous colorectal polyps do not require surgical treatment.⁷

Surgical resection is the primary treatment option for malignant SCRT as well as for benign lesions that are not amenable to endoscopic resection. Patients with synchronous lesions located in adjacent segments commonly undergo more extensive colorectal resection⁸; however, controversy still exists on how to best treat synchronous lesions in separate segments. A conservative approach consisting of multiple segmental resections, which aim to retain the normal colon, has been suggested by some authors.⁹ Others have suggested that more extensive procedures such as subtotal colectomy, total colectomy, or even proctocolectomy with ileoanal anastomosis should be performed.^10,11

Nevertheless, when one of the synchronous lesions is located in the rectum, the standard treatment is guided by the principle of locoregional control of disease by Total Mesorectal Excision (TME), either by Low Anterior Resection (LAR) or Abdominoperineal Resection (APR).¹²

However, radical rectal surgery is associated with high morbidity and mortality rates.^13,14 As such, when combined with another colectomy, like in the case of synchronous colorectal lesions, such radical rectal surgery may be unwarranted for some patients with benign or early invasive rectal lesions.

In these cases, some rectal lesions can be excised by different surgical techniques through a Transanal Excision (TAE) approach. Transanal Endoscopic Microsurgery (TEM) is a minimally invasive endoscopic technique that improves the quality of the local excision by excellent access and visualization of the surgical field and precise full-thickness excision of rectal lesions.¹⁵

TEM has become an acceptable tool in the surgical armamentarium for the treatment of both benign and early invasive malignant rectal lesions.¹⁶ For rectal adenomas, TEM represents a superior approach over the traditional TAE, and for T1 rectal cancer, it is faster and safer than traditional radical surgery.¹⁷

Nevertheless, the main disadvantage of TEM remains the inaccuracy of the various preoperative diagnostic modalities in predicting the presence of invasion of the rectal wall and nodal involvement. In actual fact, radical rectal surgery following TEM is required in up to 20% of patients as a result of an unexpected invasive pathology of the TEM specimen.^18,19

Laparoscopic surgery for colorectal cancer offers several advantages in comparison to open procedures. These include reduced postoperative pain, shorter duration of postoperative paralytic ileus, shorter hospital stays, and decreased morbidity.²⁰

The aim of our study is to report the outcomes of patients with synchronous colon and rectal lesions treated by a combination of two minimally invasive techniques; laparoscopic colectomy and TEM.

Materials and Methods

We retrospectively collected data on 141 patients with rectal tumors treated by a TEM procedure at the Department of Surgery at Hasharon Hospital, Rabin Medical Center from the years 2004 to 2014. Nine of the 141 patients underwent additional colon resection combined with TEM. These patients were included in the study. In addition, data on patient demographics and comorbidities were collected. Data on the surgical procedure included the type of resection performed, the duration of the operation, tumor location, and the number of lymph nodes collected in the specimen.

The full medical records of the patients were obtained, reviewed, and recorded.

All patients underwent colonoscopy with biopsy or polypectomy and the lesion was marked with India ink. In the case of synchronous colorectal lesions with one lesion located in the rectum, patients were further evaluated according to a standard protocol, including clinical examination with digital rectal examination, rigid proctoscopy, and endorectal ultrasound (EUS). For each patient, the tumor's distance from the anal verge, the location of the tumor, and the tumor size were assessed.

TEM was proposed for patients who had benign rectal lesions or superficial adenocarcinoma arising from an adenoma, and negative lymph node. Patients with more advanced lesions or involvement of perirectal lymph nodes were offered radical surgery or preoperative chemoradiation therapy. Patients were also staged before surgery with abdominal and pelvic CT, and some patients also underwent an FDG-PET.

The TEM procedure was performed with the original Richard Wolf (Knittlingen, Germany) equipment under general anesthesia. Depending on the tumor location, the patients were placed in a prone jackknife or lithotomy position. The tumor site was removed by excising the full-thickness rectal wall with a 1-cm margin around the tumor. The underlying mesorectal fat was included with the specimen. The specimens were pinned and marked for orientation by the surgeon. The rectal defect was closed primarily in a transverse manner with absorbable sutures.

Depending on whether it was a right or left colectomy, the laparoscopic colon resection was performed with the patient in a supine or lithotomy position. In most cases, the dissection was carried out using a mediolateral approach in both the ascending and the left colon with identifying and preserving vital structures. The specimen was resected and anastomosis performed extracorporeally.

The preoperative preparation for the patients included mechanical bowel preparation (polyethylene glycol) on the day before the operation and prophylactic antibiotics (Cefamizine1 g and metronidazole 500 mg) at the induction of general anesthesia.

Postoperative pain management for all patients included parenteral narcotics (morphine or tramadol) and dipyrone or paracetamol administered orally. Patients began an oral intake of a liquid diet on postoperative day one and they were subsequently advanced to a soft diet. A specific enhanced recovery program was not implemented. Bowel function postoperatively was determined by the presence of flatus and/or stool. Patients were discharged when an oral diet was well tolerated and no complications were detected.

Results

Of the 141 patients who underwent TEM during the study period, nine (6.5%) combined laparoscopic colectomy. There were 3 female and 6 male patients. The mean age was 69.1 ± 10.6 years. All rectal lesions were benign adenomas on preoperative biopsy, and there was no rectal wall invasion or perirectal lymph node metastasis on the EUS. The mean tumor size was of 2.5 cm (1–6), and the distance from the anal verge was 9 ± 2.5 cm. Four lesions (44%) were located in the lateral rectal wall, four (44%) were posterior, and one (11%) was anterior. The locations of the colonic lesions were as follows: in the cecum one (11%), ascending three (33%), transverse two (22%), left two (22%), and the sigmoid colon one (11%). Two (22%) lesions, one in the transverse and other in the left colon, were nonresectable large benign polyps, and the other seven (77%) were malignant.

Seven patients had the colectomy before TEM and 2 patients had the TEM first. There were six (66%) right colectomies, two (22%) left colectomies, and one (11%) sigmoid colectomy.

The mean operative time was 245 minutes (with a range of 185–313 minutes) for the combined procedures. The mean operative time was 105 minutes (with a range of 65–160 minutes) for the TEM. The median time of hospitalization was 6 days (with a range of 4–11 days).Table 1 summarizes the demographic and perioperative data.

Table 1.

Patients and Perioperative Characteristics

Male/female	6/3
Age (years)	69.1 + 10.6
Rectal lesion:
Tumor distance from anal verge (cm)	9 + 2.5
Tumor diameter (cm)	2 (1–6)
Location in rectal wall (n)
Anterior	1 (11)%
Lateral	4 (44)%
Posterior	4 (55)%
Colonic lesion (n)
Cecum	1 (11%)
Ascending colon	3 (33%)
Transverse colon	2 (22%)
Left colon	2 (22%)
Sigmoid colon	1 (11%)
Right colectomy	6 (66%)
Left colectomy	2 (22%)
Sigmidectomy	1 (11%)
Mean operative time: (minute)
The combined procedures	245 (180–313)
TEM	105 (65–160)
Median time of hospitalization (days)	6 (4–11)

TEM, transanal endoscopic microsurgery.

Two patients had urinary retention, which was treated with a catheter. No cases of rectal bleeding, suture dehiscence, or other major complications were observed. Although no fecal incontinence was reported by any of the patients, six (66%) of them had prolonged postoperative diarrhea characterized by frequent passage of bowel movements (between 6 and 10 a day), mostly of very soft or watery nature, which lasted for 16 weeks (range 7–20 weeks).

The final rectal pathology reports demonstrated adenoma with high-grade dysplasia (HGD) in 5 patients and adenoma with low-grade dysplasia (LGD) in 4 patients, all of them had free margins. The colon pathology was T1 N0 in 3 (33%), T2 N0 in 3 (33%), T3 N1in 1 (11%), and adenoma with HGD in 2 (22%) patients.

In a median follow-up of 52 months (range 14–72 months), 2 patients who had developed a rectal polyp in the scar of the TEM resection underwent re-TEM for the recurrent polyp at 14 and 18 months postoperatively, and both had a final pathology of adenoma with foci of HGD. Although 2 patients had adjuvant chemotherapy for unfavorable colonic pathology, no distant metastases or colonic recurrence were detected in the follow-up period.

Discussion

Minimally invasive surgical techniques continue to evolve in an effort to treat patients more effectively with minimal morbidity. Paradigms of minimally invasive techniques that established their role in colorectal surgery are TEM and laparoscopic surgery.^21,22

Up until the 1970 s, a preoperative diagnosis of SCRT was quite rare (1.6%–4.3%). During this time, it was mostly discovered by intraoperative bowel manipulation.^23,24 With the development of early diagnostic technologies, SCRT has been increasingly diagnosed. The high incidence of colorectal tumors has led to the need for new surgical approaches.

There remains a controversy over the most appropriate surgical approach in cases of SCRT. Some authors propose radical operations such as a subtotal colectomy to remove sufficient intestinal length as well as to prevent future development of metachronous tumors.¹¹ In cases of neoplastic lesions in contiguous intestinal segments, such as the right and transverse colon or the left colon and rectum, it is necessary to perform an extended hemicolectomy or an anterior resection of the rectum.²⁵ Such procedures are associated with significant morbidity.

Others recommend a more conservative approach for older patients, while supporting radical procedures for younger patients with regionally confined nonmetastatic disease.²⁶ While some believe that morbidity is lower following large operations like a hemicolectomy for benign colonic polyps as opposed to malignant ones, this is in fact a misconception.²⁷ In addition, the inability to preoperatively rule out by biopsy whether a large endoscopically unresectable polyp harbors an invasive component provides further impetus to perform a local full-thickness colonic excision for benign colonic lesions as an alternative to major surgery.

Nevertheless, when one of the synchronous lesions is located in the rectum, sometimes it can be excised by transanal approach. TEM provides an excellent tool for full-thickness bowel wall local excision for rectal lesions. Suitable rectal lesions for TEM are benign noninvasive adenomas and early rectal cancer without lymph node involvement.

The combined approach, using both TEM and a laparoscopic colectomy, is the option we examine for cases of SCRT. Combining the two procedures has the significant advantage of reducing morbidity and preserving the length of the large bowel. While this is a considerable advantage, it is also important to note that the combined approach has disadvantages, including the need for radical rectal resection in some cases as a result of an unexpected invasive pathology of the TEM specimen, the potential development of metachronous rectal lesions, an increased prevalence of prolonged postoperative diarrhea, and is a technically demanding procedure.

The unique approach we propose of combining the two minimally invasive techniques, laparoscopy and TEM, to treat synchronous colonic neoplasms was previously described in the literature by Spizzirri et al.²⁸ They described 6 patients with rectal pathology that was either benign or malignant with a synchronous colonic neoplasm. One of the patients in their series progressed at 3 years with metastasis to the liver. Interestingly, this patient had noninvasive pathology in the rectum. The authors of this study claim that oncologic standard of care was maintained for all patients.

Our study provides additional evidence showing the major advantage of this approach for patients with SCRT: the significant reduction in morbidity.²⁹ This technique is associated with decreased morbidity because it allows for the preservation and functionality of the rectum. Unlike the rest of the colon, the rectum greatly contributes to a patient's fecal continence and incontinence can have a major effect on a patient's quality of life.³⁰

A valid alternative approach for SCRT would be a staged procedure, in which the TEM is performed as a first operation to provide the definitive rectal pathology, hence permitting a multidisciplinary approach especially in occasion of advanced rectal cancer, and subsequently a colonic resection, of various extents, as a second procedure. A staged approach would be appropriate for benign rectal adenomas that are most likely to harbor an invasive component, like in case of a large rectal lesion, or a lesion with malignant appearance at the direct proctoscopy despite benign biopsy.

Although the staged approach allows for the preservation of the rectum as in the combined approach, the avoidance of additional operation is a powerful argument in favor of the combined approach. In actual fact, TEM is identical in both the staged and combined procedure, but the possibility of increased morbidity performing two separate anesthesia and procedures outweighs the morbidity of the single combined procedure.

The need for radical rectal resection following TEM as a result of an unexpected invasive pathology is considered a real concern in both the staged and combined TEM procedure for SCRT. Therefore, performing preoperative staging of the rectal tumor by EUS is quite significant for appropriate patient selection. Unfortunately, some studies report a 20.5% discrepancy rate between preoperative EUS and histological staging of the tumors.³¹

In this study, EUS performed for all patients did not show any rectal wall invasion or pathological perirectal lymph nodes. And none of them required a radical rectal surgery after TEM since all had a benign pathology.

A main disadvantage of the combined approach is the increased prevalence of prolonged postoperative diarrhea. In our study, 6 of the 9 patients suffered a postoperative prolonged course of diarrhea. While recognizing that our study is a case series with a limited number of patients, this high rate of postoperative diarrhea warrants further discussion and analysis.

While literature about TEM combined with laparoscopic colectomy for SCRT is lacking, many studies discuss the rates of postoperative diarrhea following TEM when it is solely performed without the addition of a synchronous laparoscopic resection of a colonic mass. TEM on its own has also been associated with fecal incontinence. While TEM is less likely to lead to fecal incontinence than TME, concerns about this complication following TEM have been raised since the technique's early use.³² The subject has been well studied and several factors were identified to be significant in the causality of these complications. Postoperative sphincter injury is a possible cause of fecal incontinence following TEM and can be diagnosed by EUS.³³ Another possible cause is injury to the rectal pudendal nerve, which can be assessed by motility tests.³⁴

These studies concluded that three nonmutually exclusive risk factors for anal dysfunction exist following TEM: long operative time (>2 h), depth of excision, and preexisting anorectal dysfunction. For the third risk factor, preexisting anorectal dysfunction, it is recommended that the preoperative anal function of patients be evaluated by EUS and/or anal manometry.³⁴

Most of these studies show a zero or low rate of diarrhea and the diarrhea is transitory in nature. Tsai et al. demonstrated a 4.1% rate of fecal continence deterioration after TEM with a nearly 82% return to baseline within 4–8 months.³⁵ Middleton et al. reports no cases of diarrhea in their meta-analysis of 98 patients undergoing just TEM for rectal adenomas.³⁶ Moreover, Guerrieri et al. reported a 1% rate of stool incontinence and their patients were treated with physiotherapy and anal sphincter biofeedback. All the patients in their study reported the resolution of their symptoms within 2 months of the operation.³⁷ Han et al. reported incontinence of hard stool in 1 patient out of 44 patients treated with TEM for rectal adenoma at 6 months follow-up.³⁸

Allaix et al. conducted an in-depth analysis of postoperative fecal urgency, or diarrhea, in 93 patients following TEM for both benign and early invasive lesions. Like the above studies, he showed that only 5% of patients had prolonged postoperative diarrhea at 60 months. Interestingly, he also reported that 65% and 30% of patients had diarrhea at 3 and 12 months, respectively. In their study, postoperative manometry values at 3 months were significantly lower than at baseline (P < .050), but had returned to preoperative values at 12 months.³⁹

Unlike the other studies, Allaix et al. show the prevalence of diarrhea in both the early and late postoperative period. Even though the patients in Allaix et al.'s analysis underwent only TEM, while the patients in our case study underwent TEM and a laparoscopic colectomy, it is noteworthy that the prevalence of diarrhea in the early postoperative period is similar, 65% in Allaix et al's study and 66% in our study. However, the postoperative diarrhea experienced by most of the patients in Allaix et al's analysis was eventually resolved, unlike in our case series, where the high prevalence of postoperative diarrhea continued.

We hypothesize that the high prevalence of postoperative diarrhea in patients who underwent TEM combined with a laparoscopic colectomy is a result of the dual injury caused by the combined procedure. A laparoscopic resection of the colon results in an injury to the sympathetic innervation to the colon. As the result of a TEM procedure, the parasympathetic innervation to the rectum is injured. The dual nature of this injury, to both the sympathetic innervation to the colon and parasympathetic innervation to the rectum, may be the cause of the prolonged postoperative diarrhea. The literature fails to address this combined injury and clinical studies are currently lacking on this topic. Additional research is needed to further examine the effect of the dual nature of the injury resulting from the combined procedure on prolonged postoperative diarrhea.

In addition to prolonged postoperative diarrhea, the risk of developing metachronous lesions in the rectum constitutes a disadvantage of the combined approach. While obviously not a risk in radical resection, the potential development of metachronous lesions in the rectum is also a disadvantage when TEM is performed on its own.

Two of our patients developed metachronous lesions and they had to undergo TEM for a second time. This would have been avoided with a definitive procedure to remove the entire rectum. At the same time, the combined approach or TEM on its own allows for the procedure to be performed multiple times in the case of repetitive and multifocal resections. Also, when needed, radical surgery can still be performed without compromising oncologic outcome.⁴⁰ However, major surgery after TEM is probably more difficult given the disruption of surgical plains and scarring.

The incidence of recurrence of rectal adenomas after TEM is reported in large meta-analyses to be 4%–6%.^39,41 Our 22% rate of recurrence following TEM is somewhat high, but is likely due to the small sample of patients included in our study.

In a large single-center study with an adequate follow-up period, HGD was found to be a risk factor for local recurrence of rectal adenomas after TEM treatment in comparison to LGD.⁴²

Tumor size has repeatedly shown to be a risk factor for recurrence of rectal adenomas following TEM. McCloud et al. reported a series of 75 patients who underwent TEM for adenoma with a follow-up period of 31 months.⁴³ They found that larger polyps were incompletely excised, with 68.9% of polyps <50 mm completely excised and only 33.3%> 50 mm completely excised. Similarly, Ganai et al. reported tumor size >4 cm to be an independent prognostic factor for local recurrence in 107 patients who had TEM for benign neoplasms.⁴⁴

Our 2 patients with recurrence had the final pathology of adenoma with HGD, with a diameter of 3.2 cm in the first and 2.8 cm in the second, and both had free resectional margins.

Nonetheless, some cases of metachronous or recurrent lesions after TEM despite a complete resection, give the impression of a tendency in these patients to develop more rectal polyps. Patients who evidently have “polypogenic rectums” would likely benefit from an up-front radical resection of the rectum instead of repeat TEMs due to the increased burden of undergoing repeated surgical procedures.

An additional disadvantage of the combined approach is that it is a technically demanding procedure. Even on its own, without the addition of the laparoscopic colectomy, TEM is a difficult procedure to learn. The learning curve was studied by a group in the Netherlands who noted that the rate of conversion to radical resection increased with increasing size of the tumors. In addition to this factor, they also noted that the rate of conversion was higher early in the learning curve of a surgeon.⁴⁵ In their study, recurrence-free survival of patients operated during the 36th through 80th procedure per surgeon was significantly shorter than in patients operated during procedures 1–35 and 81 onward.

Another technical issue in the combined procedure that should be taken in consideration is the need of repositioning the patient, while passing from the laparoscopic colectomy to the TEM, which increases the overall surgery time. Also, a bothering large colon dilatation as a result to gas insufflations through the TEM can be encountered when performing laparoscopic colectomy after TEM, adding to the complexity of the combined procedures.

In our study, none of the patients had to be converted from laparoscopic to open colectomy or from TEM to LAR or APR to successfully resect the rectal lesion.

In a meta-analysis of six different case series of TEM, the median conversion rate for adenomas was 5.7%. Approximately, one-half of the immediate conversions were to LAR and other half to direct local excision.³⁶ Our large experience in TEM and a carefully preoperative patient selection might contribute to a low conversion rate in this study.

Our study had several limitations; it was a nonrandomized retrospective study and involved a small number of highly selected patients.

Conclusion

TEM currently is and prospectively will be playing an important role in the management of rectal tumors. Given the significant reduction in morbidity, the combination of TEM with laparoscopic colectomy is feasible and should be kept in mind as an alternative to the staged procedure in the case of SCRT. However, strict selection criteria should be considered and the disadvantages, including prolonged postoperative diarrhea and the risk of developing metachronous lesions, should be discussed with the patient before proceeding with the combined approach.

Footnotes

Disclosure Statement

The authors have no conflicts of interest or financial ties to disclose.

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