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Review

Comparative outcomes of rectal cancer surgery between


elderly and non-elderly patients: a systematic review
Gilles Manceau, Mehdi Karoui, Andrew Werner, Neil J Mortensen, Laurent Hannoun

Elderly people represent almost all patients diagnosed with and treated for rectal cancer, and this trend is likely to
become more apparent in the future. Surgical management and treatment decisions for this disease are becoming
increasingly complex, but only a few reports deal specically with older patients. In this systematic review, we provide
an overview of published studies of outcomes after curative surgery for rectal cancer in elderly people (>70 years). We
identied 48 studies providing information about postoperative results, survival, surgical approach, stoma formation,
functional results, and quality of life after rectal resection for cancer. We found that advanced chronological age
should not, by itself, exclude patients from curative rectal surgery or from other surgical options that are available for
younger patients. Although overall survival is lower in elderly patients than in younger patients, cancer-specic
survival does not decrease with age. However, the level of evidence for most studies was weak, emphasising the need
for high-quality clinical trials for this population.

Introduction
The incidence of rectal cancer increases with age, reaching
a peak at around the age of 80 years, with an age-specic
incidence of 135 new cases per 100 000 people per year
between 80 and 84 years of age.1 Thus, although people
older than 75 years account for only 510% of the overall
population in developed countries, 3545% of patients
with rectal cancer are in this age group.2,3 This proportion
may increase in the future because of demographics of an
ageing population, and increases in life expectancy.
Surgery is the cornerstone of curative therapy for
patients with rectal cancer. However, there is no
consensus about the optimum surgical management of
elderly people who are a heterogeneous group of patients,
ranging from very t to very frail individuals. This
population is undertreated compared with younger
patients. The percentage of patients operated upon
decreases with age,2,49 and the curative surgery rate is
substantially lower in older patients.4,7,8,1012 Additionally,
elderly people need more emergency surgery than do
younger patients.12,13 When curative surgery is planned,
neoadjuvant radiotherapy or chemoradiotherapy is less
discussed and used.2,3,6,8,9,12,1416 Usually, non-restorative
procedures such as Hartmanns procedure, abdominoperineal resection, or local excision are undertaken.
Anterior resections are done less often in elderly
patients,2,5,8,1113,15,17,18 although tumour location and stage
do not dier in elderly patients and younger patients.3,710
These disparities could be explained by patients
preferences, or by surgeons opinions about patients of
advanced age.
Elderly patients are generally recruited to clinical trials
less often than younger patients and therefore are
under-represented in publications about cancer treatment.19 They were not included in most trials that
assessed neoadjuvant therapy.20,21 Similarly, in most
colorectal cancer guidelines, routine screening is not
oered to patients older than 75 years.22 Because this
heterogeneous, fragile subset of patients with more
comorbidities and decreased reserve capacity was exwww.thelancet.com/oncology Vol 13 December 2012

cluded from major studies leading to the development


of standard practice for rectal cancer, can these
recommendations be extrapolated to the elderly population or do they need to be modied? The aim of this
systematic review is to summarise the published work on
the curative surgical management of rectal cancer in
elderly people.

Methods
Search strategy and selection criteria
Two authors (GM and MK) independently undertook
electronic literature searches with PubMed (Medline).
The search strategy applied was as follows: (elderly [Title/
Abstract] OR older [Title/Abstract] OR oldest [Title/
Abstract]) AND rectal neoplasms (MeSH).
We set an arbitrary age limit for considering a patient
as old at 70 years of age. We included only studies
published in English, in peer-reviewed journals, between
January, 1985, and April, 2012. We excluded editorials,
case reports, reviews, and letters or comments, and
studies that included both colon and rectal cancers
without a specic analysis of the results for rectal cancer.
We also excluded studies of palliative management
and neoadjuvant or adjuvant treatments. We identied
prospective and retrospective series and no study was
excluded on the basis of its type or size.
We then selected relevant articles from titles and
abstracts. The related articles function was used to
broaden the search. Further articles that were potentially
missed by the search strategy were identied by a manual
search of the references from the key articles.

Lancet Oncol 2012; 13: e52536


Assistance Publique-Hpitaux
de Paris, Department of
Digestive and HepatoPancreato-Biliary Surgery,
Piti-Salptrire Hospital,
University Institute of
Cancerology (Paris VI), Pierre
and Marie Curie University,
Paris, France (G Manceau MD,
Prof M Karoui MD,
Prof L Hannoun MD);
Department of Surgery,
Louisiana State University,
Health Science Center,
Shreveport, LA, USA
(A Werner MD); and
Department of Colorectal
Surgery, Churchill Hospital,
Oxford, UK
(Prof N J Mortensen MD)
Correspondence to:
Prof Mehdi Karoui, Assistance
Publique-Hpitaux de Paris,
Department of Digestive and
Hepato-Pancreato-Biliary
Surgery, Piti-Salptrire
Hospital, University Institute of
Cancerology (Paris VI), Pierre and
Marie Curie University,
4783 Boulevard de lHpital,
75013 Paris, France
mehdi.karoui@psl.aphp.fr

Data analysis
GM and MK independently extracted data and assessed
quality. Disagreements were resolved by discussion.
The following topics were specically considered:
postoperative morbidity and mortality, postsurgical
survival, functional results and quality of life after
surgery, risk of permanent stoma, surgical approach,
type of bowel diversion, and place of local excision.
e525

Review

Results
Description of studies
48 studies met our selection criteria (gure), including
27 comparative retrospective studies, 13 cohort studies,
six non-comparative retrospective studies, and two
casecontrol studies. We identied no studies of bowel
diversion or place of local excision.

Short-term outcomes after curative rectal surgery


Table 1 shows the short-term outcomes after rectal
surgery in elderly patients. There are no data in the
published work for the results of fast-track rehabilitation
in elderly patients after rectal cancer surgery. 17 studies
(six prospective and 11 retrospective) assessed postoperative results after curative rectal cancer resection in
elderly patients.1,3,8,9,11,13,15,17,18,2330 Even when patients are
selected for surgery, a cohort study by Law and
colleagues18 showed that patients older than 75 years
were more vulnerable, with signicantly more
comorbidities than patients aged 75 years or younger
(541% vs 365%, p<0001). The largest studies showed
a signicantly higher 30-day mortality risk for this
patient group.3,8,11,13,17 In a German multicentre study of
1115 patients,11 mortality increased from 05% in
patients 50 years of age or younger to 13% in patients
older than 80 years. Nevertheless, after a logistic
regression analysis, Barrier and colleagues reported
that age was not an independent factor for postoperative
mortality, unlike American Society of Anesthesiologists
(ASA) score and emergency surgery.12
Overall postoperative morbidity is roughly 40% in
elderly patients, but is not signicantly higher than in
younger patients.9,15,18,26 The only study that showed a
signicant dierence in morbidity with age was a
retrospective study.17 In a matched casecontrol study by
Puig-La Calle and colleagues,15 patients older than 75 years
with comorbidities had substantially more postoperative
complications than did those without comorbidity (41% vs
23%, p=002). According to Law and colleagues,18

431 records identied through database searching

283 excluded on the basis of title


and abstract

148 possibly relevant publications identied and


screened for eligibility

25 additional records identied


from the reference lists of
relevant articles

125 excluded on the basis of


full-length article

morbidity is related to concomitant diseases and patients


American Society of Anesthesiologists (ASA) score. In
2002, in a prospective multicentre study assessing
mortality and morbidity for low rectal cancer surgery in
France, Alves and colleagues25 assessed 238 patients, with
a mean age of 66 years (SD 13). In a multivariate analysis,
age was not one of the four independent risk factors for
postoperative complications: ASA score greater than 2,
intraoperative faecal contamination, operative time of 6 h
or longer, and smoking. Finally, Marusch and colleagues31
studied a total of 19 074 patients with colorectal cancer
(including 6884 with rectal cancer); 2932 of the
patients with colorectal cancer were aged 80 years or older.
The factors aecting postoperative morbidity for rectal
cancer were high ASA score, emergency surgery, advanced
tumour stage, neoadjuvant treatment, male sex, and
pulmonary and renal diseases.31
Surgical complications are similar across age groups,
especially the rate of anastomotic leakage.1,9,15,18,26,27 This
nding was conrmed in a national cohort study and a
retrospective study that specically assessed risk factors
for leaks after total mesorectal excision.28,29 In Eriksen
and colleagues study28 of 1958 patients, the four independent risk factors in a multivariate analysis were male
sex, neoadjuvant radiotherapy, and low (46 cm from the
anal verge) or ultra-low (3 cm) colorectal anastomosis.
The percentage of symptomatic anastomotic leakage was
similar between the dierent age groups (9% for patients
80 years of age vs 129% for those 59 years of age,
p=0265). However, the rate of cardiovascular complications increased signicantly with age.18 Pulmonary
complications are also twice as common.1,9,18
Postoperative complications are more severe in
elderly patients than in younger patientseg, the
occurrence of anastomotic leakage. In two studies by
Rutten and colleagues,1,17 derived from the Dutch trial,32
the anastomotic leakage rate after low colorectal
anastomosis was 10% for patients 75 years or older and
12% for those younger than 75 years (p=063). At
6 months, more than half of patients 75 years and older
died after an anastomotic leakage, which was
signicantly higher than for younger patients (571% vs
82%, relative risk [RR] 694, 95% CI 2991611).1 This
survival dierence was also noted with other postoperative complications (mainly sepsis, abscess, and
cardiac and pulmonary complications). Thus, the
occurrence of a complication was associated with a
signicantly increased risk of 6-month mortality
(229% vs 70%, RR 327, 95% CI 205521). Overall,
6-month mortality was four times higher in elderly
patients than in younger patients (140% vs 33%,
p<00001).17

Long-term outcomes
48 studies included in the analysis

Figure: Study selection

e526

Table 2 shows the long-term outcomes after surgery for


rectal cancer in elderly patients. 17 studies (four
prospective and 13 retrospective) reported survival results
www.thelancet.com/oncology Vol 13 December 2012

174
(53%)

<75
years

www.thelancet.com/oncology Vol 13 December 2012

276
(75%)

<80
years

154
(69%)

<75
years

NR

NR

626

833

61

78

77

70

741
(26%)

1383
(49%)

75
79
years

65
74
years

479
(78%)

75
years

NR

NR

244
(57%)

182
(43%)

60
69
years

64

70
years

Shahir et al6 (2006)

133
(22%)

>75
years

80

82

504
(18%)

80
84
years

Law et al18 (2006)

88

212
(8%)

85
years

Endreseth et al8 (2006)

69
(31%)

75
years

Vironen et al9 (2004)

92
(25%)

80
years

Barrier et al12 (2003)

157
(47%)

75
years

NR

NR

244

353

NR

NR

NR

NR

39

NR

NR

75

274

001

<005

NR

NR

NR

81

98

NR

NR

NR

NR

13

NR

NR

64

0482

021

NR

p
value

NR

NR

23

105

NR

NR

NR

NR

25

NR

NR

29

76

0001

NR

p
value

1
2
34

1
2
34

12
34

12
34

24

NR

NR

NR

NR

NR

NR

NR

NR

15

816 127

12

21

13

336
551
113

28

30

32

34

42

33

39

36

68

67

61

56

46

54

52

51

44

735 24

73

NR

NR

42

15

006

<0001

NR

006

NS

08

23

17

06

13

001

0178

0178

<0001

NS

026

NS

p value

Local p
(%)
value*

AR/ APR HM
LAR (%) (%)
(%)

729 143

<0001

NR

<0001

NR

p
value

30-day
mortality (%)

Surgery

75
706
218

NR

NR

NR

NR

NR

NR

84
16

67
33

NR

NR

p
value

Score %

Pulmonary

Cardiac

Neurological

ASA score

Mean Comorbidity (%)


age
(years)

Puig-La Calle et al15 (2000)

Number
of
patients
(%)

51

65

301

368

NR

NR

NR

NR

25

32

NR

NR

36

34

0007

0141

031

NS

p
value

Overall

25

75

NR

NR

NR

NR

NR

NR

CV

001

0014

NR

p
value

Postoperative morbidity (%)

12

31

NR

NR

NR

NR

NR

NR

013

0127

NR

NR

72

31

NR

NR

NR

NR

13

NR

NR

AL

0168

NR

NR

p
value

(Continues on next page)

NR

NR

p
value

Pulmonary

Review

e527

e528

29
(100%)

9737
(63%)

<75
years

125
(79%)

<75
years

1126
(83%)

<75
years

1126
(83%)

<75
years

574
(57%)

70
years

NR

NR

NR

NR

NR

NR

NR

NR

NR

NR

85

NR

NR

NR

NR

NR

NR

352

606

NR

NR

28

<005

NR

NR

NR

NR

NR

NR

24

91

NR

NR

NR

0106

NR

NR

NR

NR

NR

NR

32

NR

NR

NR

>0999

p
value

1
2
3
45

1
2
3
45

12
34

NR

NR

NR

NR

NR

NR

NR

100

100

NR

NR

66

60

81

73

NR

NR

NR

NR

19

27

691 192

NR

10

NR

NR

NR

NR

117

171 197

35

266
534
178
22

35

631

<0001

NR

NR

NR

NR

20

<0001

0292

<0001

NR

NR

NR

NR

25

78

26

91

<00001

<0001

p value

Local p
(%)
value*

AR/ APR HM
LAR (%) (%)
(%)

8
498
367
54

30
70

p
value

30-day
mortality (%)

Surgery

NR

NR

418

513

42

51

44

576

NR

NR

46

NR

0008

0165

p
value

Overall

NR

NR

31

87

NR

NR

08

61

NR

NR

NR

CV

NR

0111

p
value

Postoperative morbidity (%)

NR

NR

69

117

NR

NR

24

NR

NR

NR

NR

>0999

p
value

Pulmonary

37

75

115

101

12

10

16

NR

NR

NR

AL

0008

NR

063

0507

p
value

Table 1: Postoperative results and morbidity and mortality after rectal cancer surgery in elderly patients in dierent age groups

Except where indicated, p values are for comparisons between elderly (the oldest age group) vs non-elderly patients (other age groups) in each study. ASA=American Society of Anesthesiologists. AR=anterior resection. LAR=low anterior resection.
APR=abdominoperineal resection. HM=Hartmanns procedure. CV=cardiovascular. AL=anastomotic leakage. NR=not reported. NS=not signicant. *p values are for comparisons between dierent types of rectal surgery between elderly and non-elderly
patient groups in each study. Median. Results for curative and palliative surgery. 1-year results. Non-comparative study. ||Comparison between elderly and non-elderly patients was only done for predictive factors for AL after rectal cancer resection.

425
(43%)

>70
years

Lin et al30 (2011)||

230
(17%)

75
years

Rutten et al1 (2008)

230
(17%)

75
years

Rutten et al17 (2007)

33
(21%)

75
years

Hotta et al26 (2007)

5606
(37%)

75
years

Tan et al13 (2007)

80
years

Andereggen et al23 (2006)

p
value

p
value

Score %

Pulmonary

Cardiac

Neurological

ASA score

Mean Comorbidity (%)


age
(years)

(Continued from previous page)

Number
of
patients
(%)

Review

www.thelancet.com/oncology Vol 13 December 2012

Review

after curative surgery for rectal cancer.2,79,12,1518,23,26,3338


5-year overall survival is signicantly lower in elderly
patients than in younger patients.8,9,12,15,17,18,34,35,38 However,
most studies emphasise that 5-year relative survival does
not change with age, and the intrinsic prognosis of
elderly patients is similar to that of younger
patients.8,9,12,15,18,33,34 In the population-based study by
Dekker and colleagues35 of 2992 patients with rectal
cancer with a median age of 69 years, relative survival for
patients 75 years or older was similar to that of patients
younger than 65 years, under the condition of surviving
for 1 year after surgery (conditional relative survival),
because of the 1-year mortality rate (201% vs 51%).
Cancer-specic survival has improved in recent years.
In a retrospective study of 11 437 patients, Nedrebo and
colleagues37 showed a signicant increase in 5-year
relative survival for patients operated on for rectal cancer
between the periods 199496 and 200103 (721% vs
796%, p<0001). This increase was noted for patients
75 years of age or younger (735% vs 801%, p<0001) and
for patients older than 75 years of age (675% vs 784%,
p=0003), with a greater dierence in elderly patients
(66% vs 109%). Results were particularly signicant for
patients older than 75 years with rectal cancer and lymph
node involvement (373% vs 658%, p=0003), with an
improved relative survival of 281% in less than 10 years.

Quality of life in elderly patients after rectal cancer


surgery
Seven cohort observational studies that used validated
questionnaires have reported quality-of-life results after
rectal cancer surgery in 1597 elderly patients.3945 Four of
these studies were retrospective4042,45 and three were
prospective.39,43,44 The investigators considered nonresponse bias in these studies to be negligible. All these
studies included patients operated on by anterior
resection or abdominoperineal resection with no sign of
recurrence at the time of assessment. Two reported
results of the same cohort.43,44 One provided data for the
height of anastomoses from the anal margin,40 whereas
another assessed the patients preoperatively.44 All studies
at least used the European Organisation for Research
and Treatment of Cancer (EORTC) QLQ-30 and CR38
questionnaires.
In Engel and colleagues study39 of a population of
1038 patients, 299 were selected for nal analysis with
4 years of follow-up. 87 patients (291%) were at least
70 years old, with a signicantly higher rate of abdominoperineal resection in this group than in patients
younger than 70 years (276% vs 142%, p=002). Elderly
patients had signicantly worse sexual function, but
higher emotional function, than did patients younger
than 70 years.
The study by Sideris and colleagues41 included a
homogeneous group of 132 patients who were operated
on for rectal cancer located within 10 cm from the anal
verge, with a minimum of 1 year follow-up. After
www.thelancet.com/oncology Vol 13 December 2012

subgroup analysis, the investigators reported no


dierence between the age groups in either overall
quality of life or prevalence of psychological disorders.
However, it was again found that patients older than
70 years of age had poorer sexual function than did
younger patients.
In Hendren and colleagues study,42 the time interval
between surgery and assessment was not specied.
Of 223 patients, 180 (807%) returned questionnaires.
Unlike the two previous studies, advanced age was not
associated with a decrease in sexual function after surgery,
but rather was an independent factor of sexual inactivity.
The assessment in the rst study by Schmidt
and colleagues44 was undertaken preoperatively and at
3, 6, 12, and 24 months after surgery. Of 466 patients,
253 (543%) responded to at least three assessments. The
analysis included two groups: 168 patients younger than
70 years and 85 patients 70 years or older. The two groups
did not dier in terms of sex, type of surgery, tumour
stage, and adjuvant treatment. The EORTC QLQ-C30
score was signicantly in favour of patients younger than
70 years with respect to global health, and physical,
cognitive, and social functioning. Emotional and
psychological functioning were similar irrespective of
age. Patients at least 70 years of age had signicantly
more pain and fatigue, and patients younger than
70 years reported more nausea and vomiting. Sexual
function was more impaired after surgery in patients
younger than 70 years. Stress of treatment and stress
due to impaired sexuality were also higher in patients
younger than 70 years. A second study by the investigators
accorded with these results.43
The two-centre study by Rauch and colleagues40
included 121 patients without tumour recurrence after
more than 2 years. An age-matched and sex-matched
comparison, with representative samples of the German,
Norwegian, and French populations, showed signicantly lower physical functioning in elderly patients.
Global quality of life, fatigue, and role, social, and
emotional functioning did not change with age.
The study by Pucciarelli and colleagues45 included only
patients with rectal cancer located up to 11 cm from the
anal verge, similar to the study by Sideris and colleagues.41
Median follow-up was 68 months.45 The abdominoperineal
resection rate was low (8%). In multivariate analysis,
patients older than 70 years had signicantly worse
physical and sexual functioning than did younger
patients.
No studies have investigated quality of life in elderly
patients after abdominoperineal resection and pseudocontinent perineal colostomy using a graft of colic
muscle wrapped around the end of the colon and
requiring daily colonic irrigations.
In conclusion, the overall quality of life of elderly
patients operated on for rectal cancer does not seem to
dier from that of younger patients. However, physical,
cognitive, and social functions are aected to a greater
e529

Review

Number of
patients (%)

Mean age
(years)

Local recurrence

5-year DFS

Mollen et al (1997)

p value
012

33

75 years

48 (21%)

NR

5-year OS
p value

NS
66%
63%

90 (38%)

NR

22%

NR

49%

NR

18%

NR

53%

Damhuis et al34 (1997)

008

14%

NR

44%

75%
71%

327 (36%)

NR

18%

NR

60%

328 (36%)

NR

23%

NR

66%

Puig-La Calle et al15 (2000)

75 years

157 (47%)

78*

NR

<75 years

174 (53%)

61*

NR

Smith et al16 (2002)


17 (14%)

NR

NR

<80 years

103 (86%)

NR

NR

Barrier et al12 (2003)

NR

72 (23%)

NR

NR

<80 years

240 (77%)

NR

NR

Vironen et al9 (2004)


69 (31%)

NR

NR

<75 years

154 (69%)

NR

NR

Bouvier et al4 (2005)

71%
01

53%

NR

77%

NR

NR
0002

40%

NR

57%

59%
001

43%

69%

008
50%

04
60%

NR

NR

66%

NR

075
69%

75 years

002
51%

NR

80 years

70%

>80 years

06
60%

65%

70%

0057

NR

NR

NR

343%
396%

8589 years

79 (36%)

NR

NR

NR

NR

8084 years

103 (47%)

NR

NR

NR

NR

Lemmens et al5 (2005)


80 years

048

NR

1564 years

39 (17%)

56%
<0001

6574 years

357%
<00001

402 (16%)

NR

NR

NR

243%

NR

6579 years

1265 (50%)

NR

NR

NR

449%

NR

5064 years

865 (34%)

NR

NR

NR

578%

Endreseth et al8 (2006)

0315

85 years

212 (8%)

88

17%

<0001
24%

NR
<0001

14%

NS
36%

8084 years

504 (18%)

82

14%

39%

28%

49%

7579 years

741 (26%)

77

12%

47%

38%

53%

6574 years

1383 (49%)

70

14%

Law et al18 (2006)


>75 years

133 (22%)

80*

NR

75 years

479 (78%)

64*

NR

Shahir et al6 (2006)


244 (57%)

NR

NR

6069 years

182 (43%)

NR

NR

Andereggen et al23 (2006)

NR

85*

NR

75 years

33 (21%)

NR

NR

<75 years

125 (79%)

NR

NR

Hotta et al26 (2007)

NR

754%
<00001

44%

NR

0326

NR

NR

57%
NS

NR

67%

44%

NR

70%

25%

0061
675%

701%

Jung et al2 (2009)

63%
<0001

477%

NR

29 (100%)

51%

70 years

80 years

58%

p value
NS

42%

94 (41%)

90 years

NR

3564 years

247 (27%)

p value

8%

6574 years

75 years

5-year CSS

NR

0012
49%
71%

<005

75 years

3663 (377%)

80*

9%

NR

NR

73%

<75 years

6042 (623%)

65*

8%

NR

NR

78%

p values are for comparisons between elderly (the oldest age group) vs non-elderly patients (other age groups) in each study. DFS=disease-free survival. OS=overall survival.
CSS=cancer-specic survival. NR=not reported. NS=not signicant. *Median. Results for curative and palliative surgery. Non-comparative study.

Table 2: Long-term results after curative surgery for rectal cancer in elderly patients compared with younger patients

e530

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Review

extent. Information about the eect on sexual function is


contradictory, but the eect seems to be lower in this age
group. Nevertheless, the amount of stress caused by
sexual dysfunction is greater for younger patients. Details
about the psychological eect also dier between studies.

Preservation of sphincter function


Is sphincter-saving surgery associated with a higher risk
of failure leading to a permanent stoma in elderly
patients? When considering all surgical options, sphincter preservation in the elderly could give poor functional
results with a high risk of anal incontinence, and the
potential eect of a permanent stoma on their quality of
life should be considered.

Risk of permanent stoma in elderly patients


Four retrospective studies have examined whether elderly
patients have an increased risk of a permanent stoma
(non-reversal of diverting stoma or secondary stoma
formation that was left in place) after low anterior
resection for rectal cancer.4649
One study from the Dutch trial32 included 924 patients
who underwent low anterior resection,46 of whom
523 (57%) had a diverting stoma at the end of the procedure and 93 (10%) secondarily because of postoperative
complications. After a median follow-up of 71 years,
19% of stomas were still present. In a multivariate
analysis, age was a signicant risk factor associated with
a decreased likelihood of stoma reversal (p=0029). Other
independent factors were secondary stoma construction,
an end stoma, local or distant recurrence, and any
postoperative complication.
In a cohort study of 6581 patients who underwent
anterior resection,47 diverting ileostomy was undertaken in
146% of cases (964 patients). After a minimum follow-up
of 3 years, 233 of patients (249%) had not had their
ileostomy reversed. Advanced age and comorbidity
(Charlson score >1) were predictive factors for persistent
ileostomy (69 vs 67 years, p=0041; and 318% vs 222%,
p=0003, respectively). In patients older than 70 years, one
in three retained their protective ileostomy permanently.
Building on the multicentre randomised trial that
assessed the rate of symptomatic anastomotic leakage
after low anterior resection with the completion of a
diverting stoma or not,50 investigators of one study
focused on risk factors leading to the presence of a
permanent stoma.48 Of 233 patients, 45 (19%) had a
stoma after a median follow-up of 6 years. Patients older
than 75 years accounted for 422% of patients in this
group and 266% of patients without stoma. For this age
group, 19 of 69 patients (28%) had a permanent stoma.
The median age of patients maintaining a stoma was
signicantly higher than that of those without stoma
(73 vs 67 years, p=004). In a multivariate analysis, two
independent factors for a permanent stoma were age
greater than 75 years and the occurrence of symptomatic
anastomotic leakage.
www.thelancet.com/oncology Vol 13 December 2012

Finally, in a study of 397 patients with low colorectal


anastomosis or coloanal anastomosis, the permanent
stoma rate was 18% after a median follow-up of
735 months.49 Notably, 33 of 279 patients (118%) had their
stoma not reversed. In a multivariate analysis, three
signicant risk factors were associated with a permanent
stoma: postoperative complications, anastomosis-related
complications (stula, stenosis, or poor anorectal function),
and local recurrence. This is the only study that did not nd
a correlation between age and stoma maintenance (odds
ratio [OR] 1032, 95% CI 09921074, p=0115).

Functional results after sphincter-saving surgery in elderly patients


Three retrospective studies have reported results of anal
continence after total mesorectal excision and sphinctersaving surgery for middle or low rectal cancers in elderly
patients.5153 In a case-matched study, Dehni and colleagues51 compared long-term functional results (minimum follow-up of 3 years) after coloanal anastomosis
with colonic J-pouch between 20 patients older than
75 years and 37 younger patients. Digital examination of
preoperative sphincteric tone was normal in all patients.
The adjuvant radiotherapy rate was comparable between
both groups (35% vs 19%, p=01). For all the 14 criteria
considered, no dierence was shown. Elderly patients
had more constipation (40% vs 22%, p=02) and used
laxatives (32% vs 17%, p=03) and small enemas (35% vs
17%, p=02) more frequently than did younger patients,
but dierences were not signicant. 90% of patients
older than 75 years and 91% of patients 75 years and
younger were satised with their results (p=1).
In a non-comparative study by Phillips and colleagues,52
92 patients older than 75 years were assessed 1 year after
an anterior resection. The main criterion was the
patients own interpretation of their bowel function,
without the use of an incontinence score. No patient had
adjuvant radiotherapy. 78 patients (85%) considered
themselves to have minor or no diculties with continence. Occasional accidents occurred in 13 patients
(14%). Only one patient required a diverting stoma
because of faecal incontinence.
Hida and colleagues53 studied functional outcomes
3 years after colonic J-pouch reconstruction. Patients
were divided into three age groups: younger than 60 years,
6074 years, and 75 years and older. Criteria included:
number of bowel movements per day and night, urgency,
evacuation diculty, bowel fragmentation, laxative use,
soiling, protective pad use, gasstool discrimination,
perianal pain, dietary restrictions, social eect, and
degree of satisfaction. Results for the 54 patients, whose
anastomosis ranged from about 1 cm to 4 cm from the
anal verge, were similar for the three groups for all
categories. The degree of satisfaction with bowel function
was better for patients 75 years and older (0% dissatised)
than for those younger than 60 years (267%), and those
between 60 and 74 years of age (286%), but not
signicantly (p=00679 and p=00640, respectively).
e531

Review

A prospective study of 96 patients assessed factors


associated with anal incontinence (with a Wexner score of
16 points, 12 months after stoma closure) for the most
extreme procedure in sphincter-saving resection
(intersphincteric resection, which, unlike conventional
coloanal anastomosis, includes partial, subtotal, or total
excision of the internal sphincter).54 In univariate analysis,
only the extent of the internal sphincter excision and
preoperative chemoradiotherapy were signicant indicators of poor anal function. Age had no eect, with similar
incontinence rates between patients 70 years and older and
those younger than 70 years (17% vs 27%, p=05).
Investigators of a prospective study of 35 patients
reported postoperative outcomes after total mesorectal
excision and delayed coloanal anastomosis for adenocarcinoma of the lower third of the rectum.55 Direct
coloanal anastomosis was made on the fth postoperative
day. The major benet of this procedure is that it avoids
the need for a prophylactic covering stoma because of the
adhesions occurring in the gap between the colon
lowered to the perineum and the anal canal. In this
series, 70% of patients were considered to have a good
functional result after a follow-up of 2 years, and 75%
after 3 years. At 18 months postoperatively, age greater
than 70 years had no eect on functional results.
Furthermore, no anastomotic leakage occurred and the
pelvic abscess rate was only 28%.

Eect of permanent stoma on quality of life in elderly patients


Two studies provided information about the health-related
quality of life of elderly patients with permanent stoma
through the use of validated questionnaires (EORTC
QLQ-C30/CR38, Short Form-36, and the modied City of
Hope Quality of Life Ostomy).41,56 In the study by Sideris
and colleagues,41 42 (32%) of 132 patients underwent
abdominoperineal resection. Groups with stoma and nonstoma patients (after low anterior resection with colorectal
anastomosis or coloanal anastomosis, or pseudocontinent
perineal colostomy) were similar, except for preoperative
or postoperative radiotherapy, which was most frequently
undertaken in patients with colostomy (98% vs 80%,
p=001). In a subgroup analysis, irrespective of patient
age, denitive colostomy had no negative eect on all
quality-of-life scores, with the exception of body image,
which was signicantly worse after a follow-up of more
than 5 years. In the cross-sectional casecontrol study by
Krouse and colleagues,56 246 patients with permanent
stoma were compared with 245 patients with anastomosis.
Women younger than 75 years of age with stoma had a
signicant decrease in physical wellbeing, whereas
women 75 years and older did not.
Thus, in the long term, elderly patients with permanent
stoma seem to have a deterioration of their body image.

Surgical approach: laparoscopy or laparotomy?


Table 3 lists comparative studies of laparoscopic rectal
surgery in elderly and younger patients. No randomised
e532

controlled trials have assessed the benets of laparoscopic surgery for rectal cancer in elderly people, in
terms of both short-term and long-term results, quality
of surgery, functional outcomes, and quality of life. The
mean age of patients in published randomised trials that
included those with rectal cancer has never been greater
than 69 years.60
Only one comparative single-centre prospective study
specically reported the feasibility and short-term results
of laparoscopy in patients older than 75 years operated on
for rectal cancer between 2001 and 2008.59 It included
three groups: two groups operated by laparoscopy (group
A of 44 patients 75 years and group B of 228 patients
<75 years) and one group operated by laparotomy
(group C of 43 patients 75 years). In groups A and B, the
conversion rate into laparotomy and operating time were
similar. Blood loss was very low in both groups.
Oncological criteria (distal margin, circumferential
margin, and number of nodes harvested) did not dier
between the groups. Postoperative mortality and morbidity rates did not dier, although patients in group A
had a signicantly higher ASA score than did those in
group B. Similarly, time to atus and length of hospital
stay were similar. Between groups A and C, operative
time was signicantly longer for laparoscopy (256 min vs
202 min, p=00003). Blood loss was lower (25 mL vs
250 mL, p<00001) but the investigators did not undertake
an assessment of transfusion requirement. Postoperative
morbidity and mortality were identical, but resumption of
gastrointestinal function and length of stay were better
for patients in the laparoscopy group than for those in the
laparotomy group (13 days vs 37 days, p<00001; and
19 days vs 22 days, p=0002, respectively).
Two studies (one prospective comparison and one casecontrol study)57,58 analysed the laparoscopic approach for
colorectal surgery, and compared outcomes for elderly
patients and younger patients. In the multicentre study
by Scheidbach and colleagues,57 701 (15%) of 4823 patients
were operated on for rectal cancer (193 patients >75 years
and 508 <75 years). Postoperative mortality was higher in
elderly than in younger patients, but not signicantly so.
However, overall morbidity was higher in elderly patients
than in younger patients, mainly because of cardiopulmonary complications (93% vs 30%, p=0022) and
lung infections (72% vs 13%, p=0008), but not surgical
complications (haemorrhage 41% vs 25%, p=0485;
prolonged ileus 72% vs 38%, p=0257; anastomotic
leakage 134% vs 119%, p=0715). In Chauttard and
colleagues study, 75 patients aged 70 years and older
(including 27 undergoing rectal resection and 22 with
rectal cancer) were matched to 103 patients younger
than 70 years (including 34 undergoing rectal resection
and 24 with rectal cancer), according to body-mass
index, sex, ASA score, pathology and procedure
undertaken.58 For rectal resections, no signicant
intraoperative or postoperative dierence was detected
between the two groups.
www.thelancet.com/oncology Vol 13 December 2012

Review

Number
of
patients
(%)

ASA score

%
Scheidbach et al57 (2005)
>75 years

Number
of rectal
resections
(%)

Number Conversion
of rectal
cancers
(%)

p
value

p
value

Mean
operative time

Blood loss

Transfusion

Mortality

Morbidity

min

mL p
value

NS

p
value

p
value

p
value
NS

Mean hospital stay

p
value

Days p
(SD) value

0007

909
(19%)

NR

NR

193
(212%)

58
(64%)

NR

NR

NR

5
(52%)

43
(443%)*

NR

<75 years 3914


(81%)

NR

NR

508
(13%)

226
(58%)

NR

NR

NR

0 (0%)

67
(284%)*

NR

Chautard et al58 (2008)

NS

NS

NS

NS

NS

70
years

75
(42%)

NR

27
(36%)

22
(29%)

3
(11%)*

266
81*

NR

3
(11%)*

0*

9
(33%)*

15
(11)*

<70
years

103
(58%)

NR

34
(33%)

24
(23%)

7
(20%)*

294
91*

NR

5
(13%)*

0*

15
(44%)*

15
(12)*

Akiyoshi et al59 (2009)

<00001

06066

0627

08006

00829

44
75 years
(16%)
(mean:
79 years)

1: 45%;
2: 818%;
3: 136%;
4: 0%

44
(100%)

44
(100%)

0
(0%)*

256*

25*

NR

0*

6
(136%)*

19*

<75 years 228


(84%)
(mean:
59 years)

1: 526%;
2: 461%;
3: 13%;
4: 0%

228
(100%)

228
(100%)

1
(04%)*

248*

33*

NR

0*

27
(118%)*

15*

p values are for comparisons between the elderly and non-elderly patient groups in each study. ASA=American Society of Anesthesiologists. NR=not reported. NS=not signicant. *Results for rectal surgery only.

Table 3: Postoperative results, morbidity, and mortality after laparoscopic rectal surgery for elderly and younger patients

Discussion
This systematic review has not addressed the global care
management of elderly patients with rectal cancer or the
indications for palliative surgery in this population. We
agree that multidisciplinary cooperation, involving
oncologists, gastroenterologists, radiotherapists, anaesthetists, radiologists, pathologists, and surgeons, is
essential in elderly patients. Furthermore, a comprehensive geriatric assessment is a major consideration in
assessment of operative risk, treatment decision making,
and adapting perioperative care if surgery is undertaken.
It will aim to identify any disability, undernutrition,
depression, polypharmacy, social or familial isolation, or
cognitive or functional disorder.61 In addition to biological
markers, this assessment needs to use validated scoring
systems. The Preoperative Assessment of Cancer in the
Elderly, which incorporates several questionnaires, could
be useful to identify suitable candidates for rectal
surgery.62,63 Added to this is a model integrating ve
variables (age, ASA score, operative urgency, cancer
resection, and metastatic disease) with a score of 045,
developed by the Association of Coloproctology of Great
Britain and Ireland for patients older than 80 years with
colorectal cancer, which could assist in patient selection
by predicting 30-day postoperative mortality, notably
after anterior resection or Hartmanns procedure.64
What emerges from this review is the scarcity of
evidence-based data for surgical rectal cancer management in elderly patients. The quality of most selected
www.thelancet.com/oncology Vol 13 December 2012

studies was poor. Most of them were single-centre series


from specialised surgical centres, with inherent selection
biases. They included mainly elderly people experiencing
successful ageing with no serious comorbidity, or with
intermediate functioning. Most vulnerable and frail
elderly patients with rectal cancer are not referred to
surgeons or are spontaneously excluded from some
surgical indications.
Nevertheless, several ndings and suggestions can be
emphasised. Advanced age should not, by itself, rule out
patients from undergoing curative rectal resection. In the
included studies, elderly patients had signicantly more
comorbidities than did younger patients. Thus, it was not
surprising to record a signicantly higher risk of
postoperative mortality. However, despite higher postoperative mortality and reduced overall survival, selected
elderly patients benet from radical surgery for rectal
cancer. We noted that comorbidity, rather than age,
increases mortality and the occurrence of complications
after curative surgery for rectal cancer in elderly patients.
Their survival is aected more by their comorbidities
than by their malignant disease. In these patients, after
oncogeriatric assessment taking into account physiological age, presence of geriatric syndromes, comorbidities, the patients general condition, and estimated life
expectancy, major curative rectal cancer surgery similar
to that undertaken in younger patients can be done. This
assessment is crucial because other studies have shown
that diminishing physiological reserves leads to an
e533

Review

increase in mortality and that progressive loss of stress


tolerance with ageing exacerbates the consequences in
case of postoperative complications.1,65 That age does not
aect cancer-specic survival was also reported for other
gastrointestinal cancers, such as oesophageal and gastric
cancers.66,67
Age alone should not be a contraindication to
restorative rectal resection. Older adults are known to
have a deterioration of the pelvic diaphragm muscles and
external anal sphincter, leading to a greater incidence of
continence and defecation disorders. The prevalence of
anal incontinence, which is dicult to quantify because
there is no standardised denition, is about 8% in the
general population, 25% for individuals between 20 and
30 years of age, more than 15% in those older than
70 years, and higher in institutionalised patients.68
Similarly, use of laxatives and the incidence of constipation increase with age.69 Nevertheless, the impact of
cancer surgery on quality of life is very important in
elderly people.70 This aspect should be considered
carefully and could greatly aect the proposed type of
rectal surgery (sphincter-saving surgery or permanent
colostomy after Hartmanns procedure or abdominoperineal resection). However, to undertake a randomised
study comparing quality of life after these two surgical
options is ethically impossible. Two meta-analyses and
one study have shown that the quality of life of patients
after abdominoperineal resection was not as poor as
expected and that their overall quality of life was similar
to that of patients who kept their intestinal continuity.71-73
Sphincter function, assessed clinically and if necessary
after manometry, is an essential element to consider in
the preoperative assessment and the decision-making
procedure.51 In the case of poor preoperative sphincter
function with faecal incontinence (not secondary to rectal
tumour), restorative surgery should be excluded.
Hartmanns procedure or abdominoperineal resection
(according to oncological requirements) is preferable. If
sphincter function assessment is found to be acceptable,
low colorectal anastomosis and intersphincteric resection are possible in selected elderly patients and are
associated with good functional results and quality of
life.53,54 For patients with signicant comorbidities, and
after giving clear information about the dierent surgical
options, delayed coloanal anastomosis could be an
alternative to low colorectal anastomosis.55 Indeed, the
occurrence of postoperative pelvic sepsis has a major
eect on survival for this patient population. Anastomotic
leakage and deep abscess rates seem to be low with this
procedure. This low rate of surgical complication was
conrmed in a retrospective study of 100 patients with a
median age of 64 years (range 2783 years) operated on
for middle or low rectal cancer with delayed coloanal
anastomosis, with a gradual improvement of functional
results during the rst 2 years after the operation.74 Furthermore, elderly patients have a signicant risk of
permanent stoma, and this surgical technique avoids
e534

the need for a diverting stoma. However, the published


work on delayed coloanal anastomosis is scarce, and no
studies have shown an advantage of this technique
compared with low colorectal anastomosis in terms of
surgical morbidity. Further high-level studies are also
needed to clarify the functional outcomes before
validation of this intervention in the various surgical
options available, because it is a direct coloanal
anastomosis with no colonic reservoir.
Finally, rectal cancer surgery by laparoscopy seems to
be feasible in elderly patients.5759 Some concerns were
initially raised about the use of the laparoscopic
approach in colorectal surgery (and especially in rectal
surgery) for this patient population, who can be
medically fragile with high comorbidities and a reduced
cardiopulmonary capacity. These concerns are partly a
result of the respiratory and haemodynamic eect of the
pneumoperitoneum, the length of the procedures, and
the extreme positions needed for exposure and
dissection. Conversely, results of studies of rectal
surgery by laparotomy in the elderly have drawn
attention to the increased risk of cardiac and pulmonary
postoperative complications.1,9,18 Thus, this minimally
invasive approach, which is known to preserve lung
function better, would be expected to improve shortterm outcomes in this population.75,76 Several randomised
trials for colon cancer have shown the technical
feasibility, improved postoperative results (including
analgesic consumption, overall morbidity, return of
bowel function, and duration of hospital stay), and
oncological eciency (quality of surgical resection, and
disease-free and overall survival) of the laparoscopic
approach.7780 Although the laparoscopic approach has
not yet been recommended, several high-quality studies
and meta-analyses tend to reach the same conclusions
with respect to the use of laparoscopy for rectal
cancer.60,7981 After rectal resection, elderly patients seem
to benet more from a laparoscopic approach than do
younger patients in terms of cardiac and pulmonary
postoperative complications.59

Conclusion
No randomised trial of curative rectal cancer surgery in
elderly patients has been done. This systematic review
summarises the results of the few studies published so far
to assess applicability of established standard practices for
elderly people. Most standard practices and recommendations for rectal cancer can be extrapolated to elderly
patients. Rather than age itself, the frailty of patients and
preoperative anal sphincter function determine the
operative indication and type of surgery. To further
optimise surgical management, more studies are needed.
In particular, these studies should raise the question of the
most suitable type of diverting stoma for this population,
and the extension of indications for local excision (with or
without neoadjuvant or adjuvant chemoradiotherapy) for
patients with signicant comorbidities.
www.thelancet.com/oncology Vol 13 December 2012

Review

Contributors
MK contributed to study design, literature search, data analysis and
interpretation, and writing. GM contributed to literature search, data
analysis and interpretation, and writing. AW contributed to data analysis
and interpretation, and writing. NJM contributed to study design, data
analysis and interpretation, and writing. LH contributed to data analysis
and interpretation, and writing. All listed authors contributed equally to
the paper.

19

Conicts of interest
We declare no conicts of interest.

22

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