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Abdominoperineal Excision Evolution of a

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DATASET NOVEMBER 2012

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HISTORICAL PERSPECTIVES

Abdominoperineal Excision: Evolution

of a Centenary Operation
Fbio Guilherme Campos, M.D., Ph.D.1 Angelita Habr-Gama, M.D.2,3
Sergio Carlos Nahas, M.D., Ph.D.1 Rodrigo Oliva Perez, M.D., Ph.D.1,2
1 Colorectal Surgery Division, Gastroenterology Department, University of So Paulo Medical School, So Paulo, Brazil
2 Angelita & Joaquim Gama Institute, So Paulo, Brazil
3 University of So Paulo Medical School, So Paulo, Brazil

During the last century, great improvements have been

made in rectal cancer management regarding preoperative
staging, pathologic assessment, surgical technique, and
multimodal therapies. Surgically, there was a move from
a strategy characterized by simple perineal excision to
complex procedures performed by means of a laparoscopic
approach, and more recently with the aid of robotic
systems. Perhaps the most important advance is that rectal
cancer is no longer a fatal disease as it was at the beginning
of the 20th century. This achievement is definitely due in
part to Ernest Miles contribution regarding lymphatic
spread of tumor cells, which helped clarify the natural
history of the disease and the proper treatment alternatives.
He advocated a combined approach with the rationale to
clear the zone of upward spread. The aim of the present
paper is to present a brief review concerning the evolution
of rectal cancer surgery, focusing attention on Miles
abdominoperineal excision of the rectum (APR) and its
controversies and refinements over time. Although APR has
currently been restricted to a small proportion of patients
with low rectal cancer, recent propositions to excise the
rectum performing a wider perineal and a proper pelvic
oor resection have renewed interest on this procedure,
confirming that Ernest Miles original ideas still influence
rectal cancer management after more than 100 years.
KEY WORDS: Rectal cancer; Ernest Miles;
Abdominoperineal resection; Abdominoperineal excision.
Financial Disclosure: None reported.
Correspondence: Fbio Guilherme Campos, Rua Padre Joo Manoel,
222 Cj 120/129 - So Paulo (SP), Brazil 01411-001. E-mail: fgmcampos@
terra.com.br
Dis Colon Rectum 2012; 55: 844853
DOI: 10.1097/DCR.0b013e31825ab0f7
The ASCRS 2012

844

t the beginning of the 19th century, rectal cancer

was managed with defunctioning colostomy, which
had been described by Jean Zulema Amussat in
1776.1 The first successful resection for rectal cancer is
credited to Jacques Lisfranc in 1826 (published in 1833),
who removed only a few centimeters of the distal rectum.2
At that time, management of rectal cancer in Europe was
essentially performed by means of perineal dissection, and
peritonitis induced by disruption of the peritoneal cavity
was the main cause of complications. Simple patient discharge from the hospital was then considered a successful
operative outcome. The first resection through an abdominal approach was performed by Carl Gaussenbauer
in 1879, but this approach was not widely adopted until
after a publication by Henri Hartmann on the treatment
of high rectal cancers.3,4
Historically, the surgical treatment of rectal cancer has
made significant advances and innovations, evolving from
simple operations to complex surgical procedures such
as laparoscopic and even robotic surgery. Along this long
pathway, one of the most important steps was the establishment of abdominoperineal resection (APR) described
by Sir Ernest Miles (Fig. 1), which represented the first attempt to develop a radical operation that could actually
cure rectal cancer. Miles published his seminal contribution, A method of performing abdomino-perineal excision for carcinoma of the rectum and of the terminal
portion of the pelvic colon,5 in 1908.
During the 20th century, many surgical refinements,
along with the addition of chemoradiation, were combined to improve outcome of treatment of rectal cancer.
The present article aims to provide a brief historical perspective on the developments leading to the introduction
of APR, and to discuss the technical innovations that
have been introduced since then in attempts to improve
oncological results of the surgical treatment of rectal
cancer, in particular a new proposal regarding extralevator APR.
DISEASES OF THE COLON & RECTUM VOLUME 55: 8 (2012)

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DISEASES OF THE COLON & RECTUM VOLUME 55: 8 (2012)

FIGURE 1. William Ernest Miles (18681947) [Courtesy of the Library

of the Royal College of Surgeons, England].

A HISTORICAL PERSPECTIVE: THE YEARS BEFORE APR

During his medical training at St. Bartholomews Hospital
in London, Ernest Miles was a pupil of Harrison Cripps, a
surgeon renowned for his studies on rectal cancer and for
the introduction of perineal excision in England.6 At that
time, the etiology of cancer was poorly understood. Contrary to the common belief that metastasis represented de
novo manifestations of cancer, Cripps thought metastasis
developed through blood and lymphatic spread from the
primary tumor.7 These ideas certainly influenced Miles
thinking some years later.
By the second half of the 19th century, most rectal
tumors were excised through the perineum (perineal approach) for symptomatic patients, despite high morbidity
rates. At St. Marks Hospital, William Herbert Allingham
would perform an initial colostomy followed several
weeks later by rectal excision guided by his finger inside
the rectum. According to Lockhart-Mummery,8 Allingham removed the growth by splitting up the rectum and
dissecting out the growth. Perineal healing was established by granulation.
Subsequently, developments in anesthesia and infection care allowed others such as Theodor Billroth, Aristide
Verneuil, Emil Kocher, and Paul Kraske to introduce modifications, including removal of the coccyx, sacrectomy,
and other procedures for facilitating access and excision
of the rectum. Kraske suggested a posterior approach in
which the rectum could be reached from behind to remove the segment containing the growth and then sew the
2 ends of the bowel together.9 A transsphincteric approach

proposed by Arthur Bevan in the United States10 (later

attributed to A. York Mason)11 resulted in prolongation of
recovery due to sphincter dysfunction and/or fistulas.
These methods yielded poor functional results, early
recurrence, and high postoperative mortality due to sepsis.
At that time, many surgeons, including Kraske, felt that
more radical operations were necessary to treat rectal cancer, even suggesting a combination of sacral or perineal
methods with an abdominal operation to accomplish this
goal.12
In an interesting review of 1500 rectal resections
performed before 1900, Graney and colleagues13 showed
a 21% mortality rate and an almost inevitable 80% recurrence rate. It is clear that tumor recurrence was already a
great challenge at that time. Still, the majority of s urgeons
continued to prefer 2-stage perineal resection to treat
rectal cancer until 1930.8 With this approach, resectability was assessed and a loop sigmoidostomy was created
during the first step. Two weeks later, the distal limb of
the colostomy was irrigated, and the rectum was excised
through the perineum with the help of coccygectomy
and lateral excision of the levator ani muscles. Although
most specimens comprised only 7 to 8 cm, this technique
allowed the resection of almost 25 cm of the distal rectum
and sigmoid, with vascular control limited to the superior
hemorrhoidal vessels.
Because of technical difficulties in removing the
growth from below, most surgeons thought it was necessary to extend the operation from the perineum into the
abdomen. Consequently, the next period of rectal cancer
surgery was marked by the introduction of abdominoperineal resection (APR). Removal of the rectum by a combined abdominal and perineal operation had already been
performed in 1884 by Vincent Czerny (Fig. 2), who was
forced to open the abdomen during sacral resection of a
proximal tumor.7,13 Thus, Ernest Miles was not the first to
use the combined abdominoperineal approach. However,
this synchronous procedure has been historically associated with his name since his description of it at the beginning of the 20th century.5

THE BASIS OF APR

After Miles was appointed assistant surgeon at the Royal
Cancer Hospital in 1899, he began developing technical modifications of rectal posterior excision procedures,
operating on 57 patients through 1906.5,14 Overall, 54 of
the 57 patients (95%) had recurrence within 6 months
to 3 years after surgery. Postmortem anatomic dissection
showed neoplastic disease in the pelvic peritoneum, mesocolon, and pelvic lymph nodes of patients who had died of
unresectable disease. Miles thought that assessment only
through perineal excision was a waste of time, because he
believed recurrence was inevitable.15,16 His dissatisfaction

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CAMPOS ET AL: ABDOMINOPERINEAL EXCISION

FIGURE 2. Vincenz Czerny (18421916), who performed the first

combined abdominoperineal resection in Heidelberg, Germany, in
1883 [Photograph courtesy of the National Library of Medicine].

with these results forced him to abandon exclusively perineal excision and look for alternative procedures to avoid
disease recurrence.12
Miles then focused on ideas regarding lymphatic
drainage of the rectum, where he distinguished 3 spread
zonesupward, lateral and downward (Table 1)and
stated that spread occurred in all directions (cylindrical concept).5,15,16 He suggested that recurrence could be
prevented by removing the pelvic colon, its mesentery, the
rectum, and as much of the lymphatic drainage as possible
(Fig. 3), similarly to the principle of Wertheim surgery
employed for uterine cervix cancer. In his original article, Miles wrote: removal [of the zone of the upward
spread] is just as imperative as is the thorough clearance
TABLE 1. Zones of rectal cancer spreada
Zone

Cancerous regions

Downward
spread
Lateral spread

Perianal skin, ischiorectal fat, and external

sphincter muscle
Levator ani muscles, retro-rectal lymph nodes,
internal iliac lymph channels, prostate gland,
base of bladder, posterior wall of vagina,
cervix, and base of broad ligament
Peritoneum of the oor of the pelvis, pelvic
mesocolon, paracolic lymph nodes, and lymph
nodes at the bifurcation of the left common
iliac artery

Upward spread

See also Figure 3.

FIGURE 3. Extent of Miles resection to remove zones of spread

[from Miles WE. Cancer of the rectum (Lettsomian Lectures).
Trans Med Soc Lond. 1923;46:127. Courtesy of the Royal Society of
Medicine].17

of the axilla in cases of cancer of the breast.5 Later on,

he concluded that of the 3 zones of possible extramural
spread, the upward zone is the most important because
secondary deposits are always present, visible to the naked
eye or discernible by the microscope.17
These ideas formed the basis for efforts to solve the
almost inevitable problem of recurrence. Miles conceived
the idea of adding a laparotomy to the perineal approach
to enable resection of the zone of upward spread, with resection of proximal lymph nodes and high-lying tumors.18
This combined approach also provided an opportunity to
explore the abdomen, allowing more accurate assessment
of disease stage.
Miles continued observations from 1899 through
1906 helped him understand that any attempt to restore
bowel continuity would preclude removal of tissues from
the lateral and downward spread. Therefore, a permanent
colostomy would be necessary. Furthermore, he emphasized that the perineal phase should be performed with a
wide dissection to remove these zones.5 Miles performed
the first operation based on these ideas in January 1907.14
Early results from 12 patients were published in his seminal paper in December 1908, in which he called his procedure abdomino-perineal excision to describe an en
bloc resection of rectal cancer together with lymph nodes
through a combined approach (Fig. 4). He postulated that

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DISEASES OF THE COLON & RECTUM VOLUME 55: 8 (2012)

rectum depends not upon the limited extent and mobility

of the growth in the rectum, but upon the absence of visible metastases in the zone of upward spread.17 After all,
the reason for developing the APR procedure was to avoid
the exceedingly high recurrence rates associated with exclusively perineal resections. Miles reported a recurrence
rate of 29.5%,17 a highly successful achievement when
compared to the greater than 90% recurrence rates associated with standard perineal procedures at the time.
Over time, Miles initial concept regarding distal
spread was proven wrong. The introduction of anterior
resection and pull-through techniques, together with
the development of stapling devices, created the path to
sphincter-saving procedures by the anterior approach
without oncological compromise.20,21

THE PROFESSIONAL RIVAL

FIGURE 4. Specimen after Miles abdominoperineal resection

[Courtesy of the Royal Society of Medicine].7,17

this operation should be used to treat all rectal tumors

regardless of location and local spread.
The proposed procedure included 5 basic principles:
(1) creation of a permanent abdominal anus (colostomy),
which was much more manageable than a sacral articial
anus; (2) removal of the whole pelvic colon (with the exception of the part from which the colostomy is made), because its blood-supply is contained in the zone of upward
spread; (3) resection of the whole of the pelvic mesocolon
below the point where it crosses the common iliac artery,
together with a strip of peritoneum at least an inch wide
on either side; (4) removal of the group of lymph nodes
situated over the bifurcation of the common iliac artery;
(5) and wide perineal resection including the levator ani
muscle (to extirpate the lateral and downward zones of
spread).5,15 The original technique involved a 1-team approach in which the coccyx was removed, the rectum was
pulled from below to complete the anterior dissection, and
the perineal wound was left open.
Goligher19 described this radical operation as a most
impressive display of operative technique, with its abdominal phase rarely taking more than 35 to 40 minutes.
Then, after the patient was moved from the Trendelenburg to a right lateral position, the perineal resection was
completed in less than 10 minutes.5,19 In his 1923 lecture
series, Miles stated that the operability of cancer of the

At the beginning, the first series of patients treated with

APR had a higher mortality rate (31%) when compared
with perineal excision alone, mostly because of blood loss
and infection,7 as blood transfusion and antibiotic therapy
were not yet available. For this reason, APR did not immediately become the preferred operative choice for most
surgeons after Miles report. In fact, John Goligher once
stated that it could be plausibly argued that its outstanding merit of great radicality might be largely dissipated if
a significant number of patients...failed to survive the immediate postoperative period.19
In this regard, Miles disagreed with his great professional rival, John Percy Lockhart-Mummery (18751957;
Fig. 5), who advocated a perineal excision preceded by a
laparotomy with colostomy. Working as an assistant surgeon at St. Marks Hospital, Lockhart-Mummery gained
broad respect within the Royal College of Surgeons for his
extensive contributions to the literature during his career
and many books focusing on colorectal surgery and heredity. After his arrival in 1903, the hospital increased the
number of cancer operations performed with techniques
such as simple colostomy, rectal excision by transsacral rectorrhaphy or transsacral perineal excision, abdominal excision, and perineal excision.22 The first mention of perineal
excision was made in an annual report in 1907, but he did
not publish a description until 1920, when he felt he had
sufficiently perfected the technique. He wrote, I have for
some years been trying to find a technique which would enable me to remove the rectum for cancer with a reasonable
degree of safety and without the serious mortality which
has hitherto accompanied rectal excision, and which would
be applicable to all cases where the growth had not already
invaded vital organs or set-up metastatic deposits.22
Lockhart-Mummery tried many modifications of the
operation that Miles had described in 1908, but the associated high mortality (13%35%) made him persist with

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CAMPOS ET AL: ABDOMINOPERINEAL EXCISION

In this setting, a historical debate was established between the need to conquer the disease (under Miles vision)
or to save the patient (under Lockhart-Mummerys vision).
Lockhart-Mummerys efforts resulted in a better chance
for survival at a time when operative mortality was a true
and significant concern for surgeons. According to Basil
Morson, a pathologist at St. Marks, anyone can confirm
from the records of St. Marks Hospital that Percy Lockhart-Mummery had a postoperative mortality rate of only
3.5% and a 5-year survival rate of about 40 to 50% of his
patients.22 Interestingly, Morson reported that the professional rivalry between Miles and Lockhart-Mummery did
not affect their personal relationship, which he described
as friendly.22

MILES OPERATION: TECHNICAL MODIFICATIONS,

CONTROVERSIES, AND IMPROVEMENTS

FIGURE 5. John Percy Lockhart-Mummery (18751957), assistant

surgeon and rival of Ernest Miles at St Marks Hospital [Photograph
courtesy of St. Marks Hospital].8

perineal excision. Because of this technique, he became

greatly admired and attracted many visitors to St. Marks
Hospital for a number of years. In 1926, he reported an
operative mortality rate of 3% and a 5-year survival rate of
approximately 50% in 200 patients.8 In that report, he also
presented a classification scheme for rectal cancer, before
the seminal publication by Dukes.23
Lockhart-Mummery emphasized the need for a rapid
operation with minimal peritoneal incursion (to lessen
surgical shock) and no attention to the zone of upward
spread, believing that the involvement of mesocolic nodes
indicated incurability. With this approach, he could treat
only low rectal tumors, and he reserved abdominoperineal
operations for cases otherwise inoperable or for growths
too high up to allow of removal by the perineal route.8
Even though he considered the reduction of recurrence to
be a great achievement of the Miles operation, LockhartMummery argued that the procedure was associated with
a great operative risk. He wrote, While the operation APR
is a great improvement upon its predecessors, it has certain
serious drawbacks as a routine method of removing rectal
cancer. The mortality of the operation, even in the hands
of experienced operators, is very highin any large series
of cases it is 30% or over, and it cannot be performed on
people over 60 years of age, or where there are complicating
conditionsin fact, the mortality can only be kept down to
at all a reasonable level by a very careful selection of cases.8

Thus, although Miles gave us the idea of the first radical

surgery for rectal cancer, it came at the price of a high
mortality rate when compared with the results of Lockhart-Mummerys alternative approach. This spurred Miles
and others to progressively fine-tune the technical steps
to shorten the operative time and achieve acceptable outcomes. By the beginning World War II, it was possible to
observe a significant reduction in mortality rates (10%
15%), mainly due to advances in anesthesia and blood
transfusion.7,24,25
Abdomino-Perineal or Perineo-Abdominal Approach?

Although APR eventually became a standard procedure

in the treatment of rectal cancer, the 1-stage procedure
proposed by Miles was not universally accepted at once.
Beginning in 1912, other leading surgeons such as William Mayo tried to reduce the operative mortality of APR
secondary to infection and hemorrhage by performing
the procedure in 2 stages.26,27 The first stage consisted of a
colostomy and mobilization of the rectum. In the second
stage some weeks later, the rectum was excised through
the perineum. In England, Lockhart-Mummery and other
surgeons also did the same.
Following Miles description of APR, his colleague
William Bashall Gabriel (18931975; Fig. 6), developed a
significant experience at St. Marks Hospital with a variant
1-stage procedure he called perineo-abdominal excision
of the rectum.28 The first step consisted of rectal excision
with the patient in a left lateral position; the patient was
then turned to a supine position to access the abdomen.
Because of the risks, he was against conservative resection
with restoration of intestinal continuity. In 1957, Gabriel
summarized his results with perineo-abdominal excision
performed since 1932, reporting a mortality rate of 9.2%
(112 deaths in 1,223 patients) for his total series at all
hospitals and clinics, and a rate of 2.6% (11 deaths in 422

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DISEASES OF THE COLON & RECTUM VOLUME 55: 8 (2012)

FIGURE 6. William Bashall Gabriel (18931975), house surgeon at

St Marks Hospital, London, where he advocated perineoabdominal excision [Photograph courtesy of Mr. Ian P. Todd,
St. Marks Hospital, London, UK].28

patients) for operations performed at St. Marks from 1947

through 1956.29 The overall 5-year survival rate for the total
series operated on from 1932 through 1951 was 50.5%.29
In 1934, Martin Kirschner from Heidelberg proposed
a combined lithotomy-Trendelenburg position to allow 2
surgical teams to work concurrently.19 Subsequently, the
development of adjustable leg supports allowed Oswald
Vaughan Lloyd-Davies (19051987)30 to perform the first
synchronous combined radical APR in the lithotomyTrendelenburg position in 1939, increasing popularity
and acceptance of the idea. This device provided simultaneous access to the abdomen and perineum by 2 surgeons,
making the procedure faster, facilitating the resection of
advanced tumors, and eliminating the cumbersome and
dangerous need to reposition the patient under anesthesia.25,26 Since then, the lithotomy-Trendelenburg position
has been associated with Lloyd-Davies name.31
At that time, Gabriel emphasized the need to address the upward zone because of the presence of positive
lymph nodes in 56% of the cases.28 He advocated proximal ligation of the inferior mesenteric artery. Indeed, the
discussion regarding vascular control had already been
initiated in 1908 by Miles5 (who originally proposed ligation below the left colic artery) and Lord Moynihan from
Leeds (Fig. 8), who proposed high ligation close to the
aorta.32 The issue of the level for arterial ligation in surgery for rectal cancer remains controversial today.

FIGURE 7. Oswald Lloyd-Davies (19051987) designed leg supports

to provide simultaneous access to the abdomen and perineum. For
that, the lithotomy-Trendelenbug position is associated with his
name [Photograph courtesy of Dr. Basil Morson, St. Marks Hospital,
London, United Kingdom].30

Possibility of Sphincter Preservation

Miles article in The Lancet5 maintained an impact on surgeons minds for decades, and APR became the standard
procedure for rectal cancer surgery. Despite its widespread
use, this operation was considered radical and was associated with high morbidity rates and significant changes
in body image. In contrast to the common belief that the
rectum always had to be entirely removed, the impressions
and results from the works from Donald Balfour, who described a technique of anterior resection with anastomosis
in 191033; Henri Hartmann, who removed the tumor and
performed a colostomy4; and Claude Dixon, (who propagated anterior resection with anastomosis) gave support
to the idea of sparing part of the rectum without compromising oncological outcome.34
By the early 1930s, pathologic studies had contradicted
Miles belief that spread occurred in 3 different directions,
finding most lymph nodes to be either parallel to or proximal to the level of the primary rectal tumor.7,35 Cuthbert
Dukes showed that downward and lateral spread from rectal cancer had been overestimated by Miles, as he demonstrated that lymphatic spread from rectal cancer occurred
mostly cephalad, generally proximal to the tumor level.36
As the concept of always removing the entire rectum
changed over time, anterior resection techniques became
the preferred choice for patients with upper or mid rectal
tumors.34,37,38 Subsequently, technical improvements, such

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CAMPOS ET AL: ABDOMINOPERINEAL EXCISION

supporting the use of laparoscopic resection for rectal

cancer to date.44
The laparoscopic Miles operation represents a truly
laparoscopic operation that does not require an auxiliary
abdominal incision for specimen extraction.45 The magnified view of the pelvis facilitates identification of surgical
planes, nerves, and the pelvic floor, particularly in a narrow pelvis (frequent among male patients), in which open
surgery may be quite challenging. In addition, patients
undergoing a laparoscopic Miles operation may benet
from the recognized advantages of laparoscopic surgery
regarding early postoperative outcomeearly return to
activities, less postoperative pain, reduced blood loss, and
improved cosmesis and hospitalizationwithout compromising oncologic principles.46
Miles Operation Revisited: The Extralevator APR
FIGURE 8. Lord Berkeley George Andrew Moynihan (18651936),
the first Professor of Clinical Surgery in Leeds University. President
of the Royal College of Surgeons of England in 1931 [Photograph
courtesy of the University of Leeds].

as restorative techniques, coloanal anastomosis, stapling

instruments, and better knowledge of tumor spread revolutionized rectal surgery.
The widespread use of circular staplers from the late
1970s and early 1980s significantly reduced the need for
APR, even for low rectal cancers.39 Moreover, the rule requiring a 5-cm distal margin40 was challenged. Results of
sphincter-preserving procedures demonstrated shorter
transmural invasion and oncologic equivalence regarding
cancer survival and local recurrence, shortening the safe
distal margin to 2 cm.4143 Since then, margins of 1 cm or
less have been considered appropriate in the setting of total
mesorectal excision and multimodality therapy, leading to
the development of intersphincteric resection techniques
and the ultimate challenge to this surgical dogma. Subtotal or total resection of the internal sphincter has been
performed with a combined abdominal and perineal approach to resect low rectal tumors within 5 cm of the anal
verge in the absence of direct sphincter invasion.
Miles Operation in the Era of Minimally Invasive Surgery

Since their introduction in clinical practice, minimally

invasive techniques (either laparoscopic or robotic) have
been increasingly used to treat colorectal diseases. The oncologic outcome and safety of laparoscopic surgery have
been a real concern, but numerous comparative studies
and randomized controlled trials have shown that the
laparoscopic approach for cancer patients is associated
with disease-free and overall survival rates comparable
to those obtained with open procedures.42 In this respect,
the CLASICC trial offers the highest level of evidence

Even though the Miles operation gained widespread acceptance, treatment of rectal cancer, and particularly local disease control, remained a challenge. Chances of cure
were significantly improved after the introduction of total
mesorectal excision using sharp dissection, as described by
Heald47 in 1982. Shortly thereafter, the importance of achieving a free radial or circumferential margin was emphasized
by the works of Quirke et al48 in 1986. Subsequent studies
clearly established that a positive (<1 mm) circumferential
resection margin was an independent predictor of local
recurrence and survival.49 Finally, prospective randomized
trials were able to demonstrate the benefits of preoperative
radiation therapy in local disease control even after proper
surgical resection including total mesorectal excision.50
However, local failures were still a problem. In fact,
even in the setting of total mesorectal excision and preoperative radiation therapy, APR was associated with significantly worse results than anterior resection in regard
to positivity of the circumferential resection margin and
local recurrences.51 This difference has been attributed
to both anatomic aspects (lymph node involvement may
follow a different pattern in low rectal carcinomas) and
technical difficulties associated with standard APR (higher
incidence of inadequate excision in APR).5153
In a call for a change of approach, Nagtegaal et al52
ascribed the poor prognosis of patients who had undergone
APR to the resection plane of the operation leading to a
high frequency of margin involvement by tumor and perforation with this current surgical technique. During standard APR, the reduced volume of mesorectum in the lower
rectum increased the chance of easily reaching the sphincter
at the circumferential margin, leaving a waist easily recognized in the specimens. For these reasons, an alternative
approach using a wide perineal resection has been proposed
to solve these problems. Various labels, such as extended
APR, extralevator abdominoperineal excision (ELAPE),
cylindrical APR, or Holm cylindrical abdominoperineal

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DISEASES OF THE COLON & RECTUM VOLUME 55: 8 (2012)

excision, have been used to describe such an approach.5456

The alternative procedure basically differs from standard
APR regarding the lateral extension of rectal resection. According to Holm et al,54,57 the extralevator APR is optimally
performed in the prone jackknife position and closely mirrors the extensive perineal dissection proposed by Miles,
which had been forgotten. In Miles original description,
rectal mobilization was performed posteriorly down to the
sacrococcygeal articulation, anteriorly to the prostate or
vagina, and laterally to the level of levators muscles.5 After
that, the abdominal procedure was ended with a terminal
colostomy. The perineal excision started with the patient in
the right lateral position, removing the coccyx and dividing the levators far from the white line to include the lateral
zone of spread.5
It is now recommended that the rectum should be
mobilized from the abdomen until the seminal vesicles in
men and upper vagina in women. At this point, one forms
the stoma and closes the abdomen. The patient is turned to
a ventral position on the operating table, and an extended
rectal excision is performed under direct vision. The posterior limit includes coccyx excision to facilitate visualization of the posterior pelvis previously dissected through
the abdomen. Lateral limits are extended to the origin
of the levator muscles at the pelvic sidewall, differently
from the dissection performed in the lithotomy position,
when the levator division occurs close to the external anal
sphincter. By leaving the levators attached to the specimen,
the proponents of this technique aim to remove more tissue around the tumor and thus decrease perforations and
rates of circumferential resection margin involvement.
Furthermore, better and direct visualization enhances local dissection through the correct anatomic planes and
could reduce intraoperative tumor perforation.54
More recently, West et al53 confirmed that extralevator
APE in the prone position removes more tissue around the
tumor and leads to a reduction in circumferential resection margin involvement and intraoperative perforations.
Although others have provided pathologic evidence that
conventional APR is oncologically comparable to the extralevator approach and that a change in surgical practice is
not justified,58 results seem to favor extralevator APR, even
in the setting of neoadjuvant multimodal therapy, in regard
to both circumferential resection margin involvement and
tumor perforation.56 Thus, it seems that a detailed knowledge of pelvic anatomy56 and the observation of the surgical
principles described by Miles may contribute to obtaining
appropriate surgical specimens, minimizing circumferential resection margin involvement and tumor perforation
regardless of intraoperative patient positioning.
Legacy of Ernest Miles (18691947)

William Ernest Miles was recognized as a technically

skilled surgeon. Descriptions of his manual ambidexterity
and technical skills attracted surgeons such as the Mayo

brothers and Lord Moynihan to watch his operations at

the Gordon Hospital in London.19,59,60 Many of his efforts
were devoted to standardizing and refining the operative
treatment of a highly fatal disease, considering the previous results and the poor conditions of anesthesia and perioperative care at that time. Even though the concept of
evidence-based medicine did not yet exist, he put together
observations derived from postmortem studies, and anatomic and pathologic knowledge to formulate a pioneer
radical procedure that effectively changed the outcome of
rectal cancer treatment.
By focusing attention on the local tumor spread and
lymphatic dissemination, Miles established principles that
helped surgeons understand the natural evolution of the
disease and the ways to control it. He prophetically emphasized the importance of the pelvic mesocolon and
wide soft-tissue perineal excisions to reduce tumor recurrence, and recent modifications of the APR technique
attempt to increase the volume of tissue removed below
the levators. Most of his principles and ideas still influence rectal cancer surgery as much as they did in 1908,39
although improved surgical techniques and new technology have decreased the need for APR in patients with rectal cancer. Moreover, the widespread use of neoadjuvant
therapy has improved local disease control, and significant
tumor downstaging and downsizing have even spared
a subset of patients from the morbidity associated with
radical surgery.61 Miles thought perhaps that this would
never happen. At the beginning of 1947, he told his friend
Colin Cromar that American surgeons who were trying to
perform sphincter-saving operations were wrong, saying
that there is no place for conservatism in the treatment of
malignant disease.62
On his last birthday, Miles received a gift and a letter
from the staff at St. Marks Hospital, in which they referred
to him as a great friend and trusted leader in proctology.12 Ernest Miles died on September 24, 1947, in London.
One of his colleagues, Lawrence Abel wrote, So long as
cancer of the rectum can only be cured by the surgeon,
Miles name will be honored for the pioneer work he did
and for the firm foundation of pathology and splendid superstructure of finished technique he has bequeathed....63
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