locally recurrent colorectal cancer: results of surgical therapy

ORIGINAL ARTICLE

Locally recurrent colorectal cancer: results of surgical therapy

M. Kruschewski & M. Ciurea & S. Lipka & S. Daum &

L. Moser & B. Meyer & J. Gröne & J. Budczies & H. J. Buhr

Received: 6 February 2012 /Accepted: 8 June 2012 /Published online: 28 June 2012# Springer-Verlag 2012

AbstractPurpose Up to 20 % of colorectal cancer patients developrecurrent disease despite standardized surgical techniquesand multimodal treatment strategies. Radical resection isthe central component of curative therapy in these cases.The aim of this study was to evaluate treatment results inpatients with locoregionally recurrent colorectal cancer.Methods From January 1995 to December 2007, surgery wasperformed for recurrent colorectal cancer in 82 patients whohad undergone curative (R0) resection of their primary tumor.Assessment included patient, tumor and treatment character-istics, postoperative complications, and time without re-

recurrence; recurrence-free and overall survival rates werecalculated according to the Kaplan–Meier method.Results Resection was performed in 60 of the 82 patients(73 %), repeat R0 resection in 52 % (31/60). Patients had apostoperative morbidity of 39 % (31/82), a relaparotomy rateof 13 % (11/82), and a lethality of 7 % (6/82). Forty-eightpercent of all surgically-treated patients received a permanentstoma. Re-recurrence was seen in 52 % (16/31). R0 resectionwas associated with a 5-year survival rate of 35 % (11/31).Conclusions Extensive reinterventions often enable repeatR0 resection. Despite relevant morbidity, the lethality appearsto be acceptable. Decisive for the prognosis is re-recurrence.

M. Kruschewski :M. Ciurea : S. Lipka : J. Gröne :H. J. BuhrDepartment of Surgery, Charité–Universitätsmedizin Berlin,Campus Benjamin Franklin,Hindenburgdamm 30,Berlin, Germany

S. DaumDepartment of Gastroenterology, Charité–UniversitätsmedizinBerlin, Campus Benjamin Franklin,Hindenburgdamm 30,Berlin, Germany

L. MoserDepartment of Radiation Oncology and Radiotherapy,Charité–Universitätsmedizin Berlin,Campus Benjamin Franklin,Hindenburgdamm 30,Berlin, Germany

B. MeyerDepartment of Diagnostic and Interventional Radiology andNuclear Medicine, Charité–Universitätsmedizin Berlin,Campus Benjamin Franklin,Hindenburgdamm 30,Berlin, Germany

J. BudcziesInstitute of Pathology,Charité–Universitätsmedizin Berlin, Campus Mitte,Hindenburgdamm 30,Berlin, Germany

M. Kruschewski (*)Chirurgische Klinik und Hochschulambulanz I, Charité–Universitätsmedizin Berlin, Campus Benjamin Franklin,Hindenburgdamm 30,12200 Berlin, Germanye-mail: [email protected]

Langenbecks Arch Surg (2012) 397:1059–1067DOI 10.1007/s00423-012-0975-z

Keywords Locally recurrent . Colorectal cancer . Morbidityand mortality . Complications . Long-term results . Surgery

Introduction

Advanced surgical techniques (total mesorectal excision(TME)) and multimodal treatment strategies have consider-ably reduced the incidence of locoregionally recurrent color-ectal cancer after curative (R0) resection, which is now 0–8 % for colon cancer and 3–20 % for rectal cancer [1–9].

Radical resection of the recurrent tumor offers the onlychance for long-term survival [10–12]. Without surgery,patients with local recurrence have a 5-year survival rateof less than 5 % and a median survival time of about8 months [5, 7, 13]. The surgical measures are flanked bymultimodal treatment strategies, though radiation therapyoften cannot be repeated due to past radiation dose [14, 15].

Since particularly locoregional recurrences of rectal can-cer are often very extensive and infiltrate adjacent struc-tures, they can require multivisceral resection and even totalpelvic exenteration. As a result, continence can only bepreserved in exceptional cases [16–19]. Such radical inter-ventions are undoubtedly associated with relevant morbid-ity. Particularly pelvic exenteration with sacral resection isassociated with high complication rates that range up to

82 % even in recent literature [2, 7, 20–22]. Despite thehigh morbidity, lethality is <10 % in experienced hands[18]. The aim of this study was to evaluate treatment resultsin patients with locoregionally recurrent colorectal cancer.

Material and methods

Study design

An analysis was done to examine colorectal cancer patientsdocumented online from 1995 to 2007. Of the total group of1,367 patients, 82 (6 %) had surgery for recurrent colorectalcancer after having previously undergone R0 resection of theirprimary tumor. Sectional imaging techniques (CT, MRT, andPET) were used to ascertain the diagnosis and assess theresectability of recurrent colorectal cancer. The indication forsurgery under curative intention was given if distant metasta-ses could be ruled out and local R0 resection seemed possible.Further, diagnostics were needed to plan the operation, e.g.,for multivisceral resections demanding interdisciplinarypatient care (Fig. 1). Whenever possible, the diagnosis wasconfirmed by CT-guided puncture (histology). This was pos-sible in 39 % of patients. Follow-up data were obtained fromquestionnaires sent to the attending physicians or from therecords of the surgical outpatient department.

Fig. 1 MRI (a) and CTexamination (b–d) of a 65-year-old male patient with presacraltumor recurrence and infiltra-tion of the sacrum after deepanterior rectal resection. Thesagittal fat-saturated MRI (a)already shows extension of thehyperintense tumor into thesacrum (arrows in a). The sag-ittal (b, c) and axial (d) refor-matted CT images with softtissue (b, d) and bone algorithmreconstructions (c) reveal thepresacral recurrence (arrows inb and d) as well as the inter-ruption of cortical continuity(arrows in c) and the impair-ment of bone microarchitectureindicative of bone infiltration

1060 Langenbecks Arch Surg (2012) 397:1059–1067

Apart from basic data, documentation comprises adetailed patient history, risk factors, preoperative diagnosticprocedures, surgical techniques, intraoperative findings, his-topathological work-up, and the postoperative course.

The detailed history also enabled the collection and anal-ysis of tumor data (tumor localization, TNM classification,grading, UICC stage), patient age, and surgical managementof the primary tumor. Thus, recurrent colorectal cancercould be subdivided into three groups according to primarytumor localization (Table 1).

Statistical analysis

Statistical analyses were performed with the StatisticalPackage for the Social Sciences, version 13.0.1. The

Kaplan–Meier method was used to calculate recurrence-free and overall survival. Differences in survival with p<0.05 were considered statistically significant.

Results

Twenty-six (32 %; male, 14; female, 12) of the 82patients surgically treated for locoregional recurrencehad undergone primary resection for colon cancer, 56(68 %; male, 35; female, 21) for rectal cancer. Themedian follow-up was 98 months. The median intervalbetween resection of primary and recurrent tumors was19 months (6–420 months) for colon and 28 (5–120 months) for rectal cancer.

Table 1 Patient, tumor, and therapy characteristics in cases of curative-intent resection for recurrence (n082)

Parameters Localization of primary tumor

Right hemicolon (n010) Left hemicolon (n016) Rectum (n056)

Median age (in years) 74 (42–79) 69 (44–82) 61 (33–91)

Urgency (n)

Elective 8 (80 %) 14 (88 %) 47 (84 %)

Urgency (n) 2 (20 %) 2 (13 %) 9 (16 %)

Tumor localization recurrence (n) Right hemicolon: 4 (40 %) Left hemicolon: 4 (25 %)

Upper third of rectum: 1 (10 %) Upper third: 2 (13 %) Upper third: 7 (13 %)

Middle third: 4 (7 %)

Lower third: 2 (13 %) Lower third: 6 (11 %)

Small pelvis: 5 (50 %) Small pelvis: 8 (50 %) Small pelvis: 39 (70 %)

Surgical procedure (n) Local re-resection: 2 (20 %) Subtotal colectomy: 5 (31 %) Neorectal resection: 9 (16 %)

Subtotal colectomy: 1 (10 %) Sigmoid resection: 1 (6 %) Neorectal extirpation: 3 (5 %)

Other resections: 2 (20 %) Rectal resection: 1 (6 %) Hartmann: 4 (7 %)

Multivisceral resection: 3 (30 %) Multivisceral resection: 4 (25 %) Multivisceral resection: 7 (13 %)

Pelvic exenteration: 1 (10 %) Pelvic exenteration: 9 (16 %)

Exploration: 1 (10 %) Exploration: 3 (19 %) Exploration: 11 (20 %)

Stoma: 1 (10 %) Stoma: 6 (11 %)

Other resections: 1 (6 %) Other resections: 7 (13 %)

Permanent stoma 5 (20 %) 6 (38 %) 28 (50 %)

Radicality(n)

R0 4 (40 %) 9 (56 %) 18 (32 %)

R1 2 (20 %) 0 (0 %) 8 (14 %)

R2 3 (30 %) 3 (19 %) 13 (23 %)

Inoperable 1 (10 %) 4 (25 %) 17 (30 %)

Neoadjuvant therapy

Chemoradiation therapy 3 (19 %) 10 (18 %)

Postoperative therapy

Chemotherapy 4 (40 %) 2 (13 %) 14 (25 %)

Chemoradiation therapy 1 (10 %) 3 (19 %) 6 (11 %)

Radiotherapy 1 (6 %) 11 (20 %)

Urgency: operation within 24 h

Multivisceral resection: resection of the recurrent colorectal cancer with en bloc resection of at least one other organ or structure

Langenbecks Arch Surg (2012) 397:1059–1067 1061

Isolated extraluminal recurrences were the most frequenttype (77 % of recurrent colon and 79 % of recurrent rectalcancer). An isolated intraluminal recurrence was observed in15 % and, respectively, 12 % of the cases, a combinedrecurrence in 8 and 9 %.

Therapy of recurrences

Resection was performed in 60 (73 %) of the 82patients surgically treated for recurrence under curativeintention and repeat R0 resection could be achieved in31 (38 %). Thus, palliative resection was carried out in

29 patients (35 %). The recurrent tumor was unresect-able in the remaining 22 patients (27 %) due to exten-sive spread (Table 1).

In two thirds of the 82 patients, recurrences—mainlyof rectal cancer (70 %)—were localized in the smallpelvis. Apart from resection of the tumor-bearing bowelsegment, 29 % of patients had en bloc resection of atleast one other organ. Twenty percent required resectionof more than one organ (Table 2). Repeat R0 resectionwas achieved by multivisceral resection or pelvic exent-eration in five patients with recurrent colon and in ninepatients with recurrent rectal cancer. In 15 cases, the

Table 2 Resected organs andlocal radicality in surgery forrecurrent disease (multipleentries possible) (n082)

Organs Recurrent colon cancer (n026) Recurrent rectal cancer (n056)

n Local R0 resection (%) n Local R0 resection (%)

Internal genitals 3 2 (67) 10 6 (67)

Bladder 2 1 (50) 6 3 (50)

Kidney, ureter 3 1 (33) 1 1 (100)

Small bowel 4 2 (50) 4 2 (50)

Abdominal wall 2 2 (100) 2 1 (50)

Omentum 1 0 (0) 1 1 (100)

Sacrum/coccyx 4 3 (75)

Psoas/iliacus m. 1 1 (100)

Total 16 9 (56) 28 17 (71)

Table 3 Morbidity and lethality of surgery for recurrence (multiple entries possible; n082)

Complication Recurrent colon cancer (n026) Recurrent rectal cancer (n056)

n (%) Relaparotomy (%) Exitus letalis n (%) Relaparotomy (%) Exitus letalis

Surgical complications

Burst abdomen – – – 1 (2) 1 (2) –

Abdominal wall abscess 2 (8) 1 (4) – 3 (5) 1 (2) –

Intraabdominal abscess 3 (12) 1 (4) – 2 (4) 1 (2) –

Ileus 3 (12) – – 9 (16) – –

Sacral cavity infection 1 (4) 1 (4) – 1 (2) 1 (2) –

Ureteral/bladder injury 1 (4) 1 (4) – 1 (2) – –

Disturbed micturition – – – 6 (11) – –

Urinary tract infection 1 (4) – – 3 (5) – –

Other (small bowel fistula, etc.) 1 (4) 1 (4) – 5 (9) 2 (4) m

Nonsurgical complications

Multiple organ failure 1 (4) – – 1 (2) m 1 (2)

Sepsis 1 (4) – 1 (4) 1 (2) – –

Pulmonary embolism 1 (4) – 1 (4) – – –

Myocardial infarction/heart failure – – m 1 (2) – –

Decompensated renal failure – – – 2 (4) – 1 (2)

Pneumonia 2 (8) – – 3 (5) – 1 (2)

Other 4 (15) – – 4 (7) – 1 (2)

Total 21 (81) 5 (19) 2 (8) 43 (77) 6 (11) 4 (7)


intervention had to be limited to exploratory laparotomy.A permanent stoma was placed in 48 % of the totalpatient population (Table 1) and in 65 % of the cura-tively resected patients (20/31).

Thirteen patients (16 %) underwent neoadjuvant che-moradiation therapy with 5-FU/folinic acid and a maxi-mum radiation dose of 50.4 Gy. Adjuvant chemoradiationtherapy could be performed in 10 patients (12 %) and 12were given only adjuvant radiation therapy. Nine patients(11 %) received 12 Gy of intraoperative radiation therapy.Combination therapy was no longer possible in 32 cases(39 %) due to previous irradiation; thus 20 patients (24 %)received only chemotherapy (5-FU/FA±oxaliplatin or iri-notecan; Table 1).

Postoperative complications

In relation to the total patient population (n082), the rate ofpostoperative complications requiring relaparotomy was6 % for recurrent colon and 7 % for recurrent rectal cancer;none of the patients died.

Nonsurgical complications eventually led to the death oftwo patients with recurrent colon (2 %) and four with

recurrent rectal cancer (5 %). The patients with recurrentcolon cancer were two women aged 44 and 53. The 44-year-old patient developed severe postoperative sepsis with puru-lent peritonitis due to perforation of a large inoperableextraluminal recurrent tumor that ultimately led to septicmultiple organ failure. The second patient, who also suf-fered from a large recurrent tumor with peritoneal carcino-matosis, died postoperatively of a pulmonary arteryembolism (Table 3).

Two of the four patients with recurrent rectal cancer diedpostoperatively of multiple organ failure or renal failuremainly due to their advanced disease. The two other patientswith recurrent rectal cancer died after developing postoper-ative respiratory failure and ileus in conjunction withadvanced disease.

Curatively resected patients with recurrent disease had apostoperative morbidity of 52 % and a lethality of 3 % (1/31). The lethality among all resected patients was 5 % (3/60)and the overall lethality was 7 % (6/82; Table 3).

Long-term results

Six of the 82 patients died in the early and 65 in the latepostoperative course (65/76, 86 %). Death was due toadvanced disease in 49 cases (64 %), to other causes (suicide,alcohol intoxication) in two (3 %) and to unknown causes in14 cases (18 %; Table 4). Overall survival related to resectionof the recurrent tumor was 106.1±11.9 months for R0 resec-tion, 72.5±12.4months for R1 resection, 37.9±4.7 months forR2 resection and 42.2±6.2 months for inoperable recurrence(p00.001, Fig. 2). Sixteen of the 31 R0-resected patients(52 %) developed re-recurrence (recurrent colon cancer,n08; recurrent rectal cancer, n08) after a mean of 82.9±16.9 months. Mean survival was 137.5±22.1 months without

Table 4 Causes of death during the postoperative course of patientswith recurrence (n076)

Cause of death Recurrent colon Recurrent rectalCancer (n024) Cancer (n052)

Tumor-related/metastatic disease 17 (71) 32 (62)

Suicide – 1 (2)

Alcohol intoxication 1 (4) –

Not specified 2 (8) 12 (23)

Total 20 (83) 45 (87)

Fig. 2 Overall survivalstratified according to R0, R1,and R2 resection andinoperability of recurrence (n082)


and 105.5±19.5 months with re-recurrence (p00.129, Fig. 3).A total of 11 patients (14 %, 11/76) had repeat R0 resectionand survived recurrent disease (recurrent colon cancer, n04;recurrent rectal cancer, n07; Fig. 4).

Discussion

The introduction of TME and the further development ofmultimodal treatment strategies have considerably reducedthe locoregional recurrence rate of R0-resected rectal cancer(3–20 %) [1–3, 13, 20, 23, 24], which is highest for lowerthird rectal cancer [25].

We are dealing here largely with extraluminal lateral orpresacral recurrences; intraluminal recurrences (anastomoticrecurrence) are the exception [5, 26]. This greatly compli-cates their treatment and curative surgery often requiresextensive multivisceral pelvic resection. In this way, R0resection of even extensive local recurrence can be achievedin about 30–50 % of the cases [27, 28].

Radical resection of the recurrent tumor flanked by multi-modal treatment strategies offers the only chance for long-term survival [10–12], although particularly locoregionalrecurrence of rectal cancer represents a surgical challenge[16–19]. This is reflected in factors such as morbidity.Complications are frequent, particularly after pelvic exent-eration with sacral resection, and range up to 82 % even inmore recent literature [2, 7, 20–22]. Despite this high mor-bidity, lethality is <10 % in experienced hands [18, 29].

The aim of this study was to evaluate treatment results inpatients with locoregionally recurrent colorectal cancer. Thisstudy included 82 patients with recurrence after curativeresection of primary colorectal cancer. The median interval

between primary R0 resection and diagnosis of recurrencewas 19 months for colon cancer and 28 months for rectalcancer. Comparable data are reported by most study groupsexamining such patient populations: 22 months in publica-tions by Saito et al., 31 months in ones by Boyle et al.,23 months as reported by Heriot et al., and 23 months accord-ing to Rahbari et al. [5, 20, 27, 29].

The present patient population had a total of 26 coloncancer and 56 rectal cancer recurrences (32 and 68 %).Most recurrences were extraluminal in both groups: 77 %in the colon cancer (n020) and 79 % in the rectal cancergroup (n044). The majority of recurrences reported inliterature are also extraluminal (55–72 %) [2, 29–31].

Fig. 3 Overall survival afterrepeat R0 resection forrecurrence stratified accordingto the development of re-recurrence (n031)

R0 resection: n=31 (38%)


Resection for recurrence: n=82 (100%)


Inoperable: n=22 (27%)

30-day survival: n=76 (93%) Early postoperative death: n=6 (7%)

Overall survival: n=11 (14%, 11/76) Late postoperative death: n=65 (86%, 65/76)

(35%, 11/31)

Tumor-related: n=49 Other cause: n=2 Unknown: n=14

Fig. 4 Overview of the patient population (n082) in the postoperativecourse


Surgical procedure

In the present study, 31 patients with local tumor recur-rence underwent repeat curative resection (38 % of all82 patients and 52 % of the 60 resected patients). Thisoften requires extensive surgery involving multivisceralresection and pelvic exenteration (n014, 45 %). Table 5lists the surgical procedures required to achieve R0resection. Authors who provide similarly detailed infor-mation on their procedure report comparable results,though the percentage of pelvic exenterations rangesup to 65 % and in part greatly exceeds the 29 % inour study [6]. However, it is 44 % in our study whenconsidering only patients who underwent curative

resection of recurrent rectal cancer. With an R0 resec-tion rate of 52 %, the results are in the middle of thereported spectrum of 37–82 % (Tables 5 and 6). Thehigh rate of R0 resections achieved by Schurr et al. andSaito et al. (82 and 75 %) may be attributable to thehigh percentage of pelvic exenterations (65 and 53 %)[6, 27].

Complications

Both multivisceral resection and pelvic exenteration havehigh rates of postoperative complications. The most com-mon complications are sacral abscesses and perineal andabdominal wound infections, followed by ileus, bleeding,

Table 5 Comparison of surgicalprocedures for R0 resection ofrecurrent colorectal cancer

PE pelvic exenteration, MVRmultivisceral resection

Surgicalprocedure

Schurret al. [6]

Palmeret al. [36]

Saitoet al. [27]

Lopez-Kostneret al. [12]

Our results

n (%) n (%) n (%) n (%) n (%)

R0 resection 37 (82) 25 (44) 43 (75) 43 (37) 31 (52)

Local resection – 5 (20) 4 (9) – 2 (6)

Anterior resection 10 (27) 2 (8) 2 (4.6) 10 (23) 7 (23)

Abdominoperinealresection

3 (8) 15 (60) 12 (28) 23 (53) 3 (10)

Subtotal colectomy – – – – 5 (16)

MVR – – – – 5 (16)

Anterior PE 10 (27) – – 3 (7) 5 (16)

Posterior PE – – 4 (9) – –

(Extended) total PE 14 (38) – 19 (44) 7 (16) 4 (13)

Other – 3 (12) 2 (4.6) – –

Table 6 Literature results of resection for local recurrence after curative resectionof the primary tumor

Author Year Numberof patientswith primary R0resection (n)

Interval betweenprimary R0 resectionand diagnosisof recurrence(median months)

Extraluminal localrecurrences of resectedrecurrences in % (n)

R0 resection ofresected localrecurrencesin % (n)

5-Yearsurvivalin %

Re-recurrencein R0-resectedpatients

Rahbari et al. [29] 2011 107 23 62 % (57/92) 59 % (54/92) 47 % 38 %

Heriot et al. [20] 2008 160 23 55 % (84/153) 64 % (98/153) 37 % n.s.

Schurr et al. [6] 2008 72 42 n.s. 82 % (37/45) 52 % n.s.

Yun et al. [37] 2008 91 n.s. 65 % (28/43) 81 % (35/43) 48 % n.s.

Palmer et al. [36] 2007 108 16 53 % (30/57) 44 % (25/57) 57 % 28 %

Boyle et al. [5] 2005 64 30.8 72 % (41/57) 37 % (21/57) n.s. 49 %

Bakx et al. [38] 2004 40 17.3 42.5 % (17/40) 40 % (16/40) 53 % 45 %

Moriya et al. [34] 2004 57 23 n.s. 84 % (48/57) 42 % n.s.

Saito et al. [27] 2003 85 22 n.s. 75 % (43/57) 39 % 50 %

Hahnloser et al. [39] 2003 394 33 66 % (201/304) 45 % (138/304) 37 % n.s.

Lopez-Kostneret al. [12]

2001 117 20 9 % (10/117) 37 % (43/117) 32 % 53 %

Our results 82 26 83 % (50/60) 52 % (31/60) 35 %(11/31)

52 % (16/31)

n.s. not specified


fistulas and intraoperative ureteral or bladder injuries, etc.,which sometimes require revision [16, 32–35]. Nonsurgicalcomplications include sepsis, renal insufficiency, heart fail-ure, thrombosis, and pneumonia.

In this study, 9 % of the patients surgically treated forrecurrence developed a sacral or intraabdominal abscess,ileus occurred in 15 %. The relaparotomy rate was 13 %.None of the patients died as a result of surgical complica-tions. Lethality was 7 % for nonsurgical complications suchas pneumonia (Table 3). On the whole, morbidity and lethal-ity are comparable to results reported in literature [29, 32,33, 35].

Oncological results

Overall survival depends decisively on whether repeat R0resection is achieved. Thus, R0 resection was associatedwith significantly longer overall survival than noncurativeresection (107.9±12.5 vs. 46.0±4.5 months, p00.001;Fig. 2).

Table 6 elucidates the basic results of this study bycomparing them with those of other studies performed overthe last 10 years. Here, only the resected locoregional recur-rences are compared and nonresecting procedures areexcluded. In our patient population, recurrences could beresected in 60 cases (73 %; Fig. 4).

The 31 patients treated with repeat curative resectionfor recurrence have a 5-year survival rate of 35 % (11/31), which is within the range of 32–57 % currentlyreported in literature (Table 6). Decisive for the prog-nosis of repeat R0 resection is re-recurrence (Fig. 3),which was seen in 16 patients (52 %). It is striking thatthis problem receives hardly any attention in the liter-ature. Re-recurrences are observed in 28–53 % of cases(Table 6). Palmer et al. found re-recurrences in only28 % and reported a 5-year survival rate of 57 %.However, they did not have to perform any multivisc-eral resections or pelvic exenterations, which suggeststhat the recurrences were not too far advanced and mayexplain the good results (Tables 5 and 6) [36].

Conclusions

1. Most recurrences are localized extraluminal lesions.2. Repeat R0 resection (potentially curative) can be

achieved in 40–80 % but often requires extensivesurgery.

3. The permanent stoma rate is high and ranges between20 and 65 % depending on the location of therecurrence.

4. The interventions have a relevant morbidity of about40 % but a lethality of only 3–7 %.

5. Decisive for the prognosis is re-recurrence, which isseen in 28–53 % of the cases.

6. The 5-year survival rate is 32–57 %.

Conflicts of interest None.

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locally recurrent colorectal cancer: results of surgical therapy

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