9
Single-incision transumbilical levels 1 and 2 axillary lymph node dissection using a flexible endoscope in human cadaveric models James Clark Daniel Richard Leff Mikael Sodergren Richard Newton David Noonan Robert Goldin Ara Darzi Guang-Zhong Yang Received: 7 February 2012 / Accepted: 12 June 2012 / Published online: 31 August 2012 Ó Springer Science+Business Media, LLC 2012 Abstract Background The use of the flexible endoscope as a sur- gical platform potentially exposes a range of new surgical approaches and benefits yet to be fully defined. A new method using the flexible endoscope to undertake axillary dissection for breast cancer treatment is explored together with an investigation into its acceptability to the general public. Methods Endoscopic axillary dissection via a transum- bilical approach using the flexible endoscope passed sub- cutaneously from the umbilicus is described for four human cadaveric axillas. A questionnaire, validated by clinicians, explored the general public’s reaction to the approach and how it might be influenced by potentially serious morbidity such as an increased rate of cancer recurrence. Results All axillas were accessed successfully via the transumbilical approach. Levels 1 and 2 axillary dissection was attempted on four axillas. Scarring from previous axillary surgery prevented dissection in one case. In the remaining three cases, respectively 12, 11, and 14 lymph nodes were harvested. The operative times improved with each case, from 1080 to 390 min. A total of 127 people responded to the questionnaire, with 73 % preferring the described approach over the open and periareolar alterna- tives when morbidities were considered equivalent. When a hypothetical elevated risk of cancer recurrence was included with the transumbilical approach, one-fifth of the public still accepted the approach due to the likelihood of a superior cosmesis. Conclusion The use of the flexible endoscope for onco- logically safe levels 1 and 2 axillary dissection is possible and would be acceptable to the general public if it were clinically approved. However, significant challenges with the current endoscopic equipment and relevant instrumen- tation limit the potential of the technique. Technical inno- vation in terms of new instrument design with improved ergonomics will reduce long operating times and fatigue, thus ensuring surgical acceptance of the flexible endoscope. Keywords Axillary lymph node dissection Á Flexible endoscopic surgery Á Single incision surgery Á Flexible access surgery Á Transumbilical Breast cancer remains the leading form of cancer among women. Internationally, an estimated 1.4 million people are affected, 32 % of whom [age-standardized ratio (women)] die as a direct result of the cancer [1]. However, this suggests that nearly two-thirds of all patients survive the disease, a figure that has increased over the past two decades [1]. In the United Kingdom alone, the relative 20-year sur- vival rate has increased from 44 % in the 1990s to 64 % currently [2], a figure reflected globally [1]. With the number of breast cancer survivors growing steadily, future surgical oncology needs to focus on improving the complications associated with the surgical approach that have an impact on quality of life while at the same time maintaining the oncologic outcomes. This includes exploring innovative techniques to maximize the cosmetic result and minimize visibility of the scarring J. Clark (&) Á D. R. Leff Á M. Sodergren Á R. Newton Á D. Noonan Á A. Darzi Á G.-Z. Yang Hamlyn Centre for Robotic Surgery, Institute of Global Health Innovation, Imperial College London, 3rd Floor Patterson Centre, South Warf Road, Paddington, London W2 1NY, UK e-mail: [email protected] R. Goldin Centre for Pathology, Imperial College London, London, UK 123 Surg Endosc (2013) 27:478–486 DOI 10.1007/s00464-012-2461-7 and Other Interventional Techniques

Single-incision transumbilical levels 1 and 2 axillary lymph node dissection using a flexible endoscope in human cadaveric models

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Page 1: Single-incision transumbilical levels 1 and 2 axillary lymph node dissection using a flexible endoscope in human cadaveric models

Single-incision transumbilical levels 1 and 2 axillary lymph nodedissection using a flexible endoscope in human cadaveric models

James Clark • Daniel Richard Leff • Mikael Sodergren •

Richard Newton • David Noonan • Robert Goldin •

Ara Darzi • Guang-Zhong Yang

Received: 7 February 2012 / Accepted: 12 June 2012 / Published online: 31 August 2012

� Springer Science+Business Media, LLC 2012

Abstract

Background The use of the flexible endoscope as a sur-

gical platform potentially exposes a range of new surgical

approaches and benefits yet to be fully defined. A new

method using the flexible endoscope to undertake axillary

dissection for breast cancer treatment is explored together

with an investigation into its acceptability to the general

public.

Methods Endoscopic axillary dissection via a transum-

bilical approach using the flexible endoscope passed sub-

cutaneously from the umbilicus is described for four human

cadaveric axillas. A questionnaire, validated by clinicians,

explored the general public’s reaction to the approach and

how it might be influenced by potentially serious morbidity

such as an increased rate of cancer recurrence.

Results All axillas were accessed successfully via the

transumbilical approach. Levels 1 and 2 axillary dissection

was attempted on four axillas. Scarring from previous

axillary surgery prevented dissection in one case. In the

remaining three cases, respectively 12, 11, and 14 lymph

nodes were harvested. The operative times improved with

each case, from 1080 to 390 min. A total of 127 people

responded to the questionnaire, with 73 % preferring the

described approach over the open and periareolar alterna-

tives when morbidities were considered equivalent. When a

hypothetical elevated risk of cancer recurrence was

included with the transumbilical approach, one-fifth of the

public still accepted the approach due to the likelihood of a

superior cosmesis.

Conclusion The use of the flexible endoscope for onco-

logically safe levels 1 and 2 axillary dissection is possible

and would be acceptable to the general public if it were

clinically approved. However, significant challenges with

the current endoscopic equipment and relevant instrumen-

tation limit the potential of the technique. Technical inno-

vation in terms of new instrument design with improved

ergonomics will reduce long operating times and fatigue,

thus ensuring surgical acceptance of the flexible endoscope.

Keywords Axillary lymph node dissection �Flexible endoscopic surgery � Single incision surgery �Flexible access surgery � Transumbilical

Breast cancer remains the leading form of cancer among

women. Internationally, an estimated 1.4 million people

are affected, 32 % of whom [age-standardized ratio

(women)] die as a direct result of the cancer [1]. However,

this suggests that nearly two-thirds of all patients survive

the disease, a figure that has increased over the past two

decades [1].

In the United Kingdom alone, the relative 20-year sur-

vival rate has increased from 44 % in the 1990s to 64 %

currently [2], a figure reflected globally [1].

With the number of breast cancer survivors growing

steadily, future surgical oncology needs to focus on

improving the complications associated with the surgical

approach that have an impact on quality of life while at the

same time maintaining the oncologic outcomes. This

includes exploring innovative techniques to maximize the

cosmetic result and minimize visibility of the scarring

J. Clark (&) � D. R. Leff � M. Sodergren � R. Newton �D. Noonan � A. Darzi � G.-Z. Yang

Hamlyn Centre for Robotic Surgery, Institute of Global Health

Innovation, Imperial College London, 3rd Floor Patterson

Centre, South Warf Road, Paddington, London W2 1NY, UK

e-mail: [email protected]

R. Goldin

Centre for Pathology, Imperial College London, London, UK

123

Surg Endosc (2013) 27:478–486

DOI 10.1007/s00464-012-2461-7

and Other Interventional Techniques

Page 2: Single-incision transumbilical levels 1 and 2 axillary lymph node dissection using a flexible endoscope in human cadaveric models

associated with breast cancer surgery, which has not only

physical consequences but also significant emotional and

psychological effects [3].

Lymph node sampling remains important for accurate

staging of the axillary disease burden and for planning

subsequent treatment of patients with breast cancer, the

outcomes of which guide medical management and deter-

mine the requirement for further axillary lymphadenectomy.

Currently, axillary dissection is undertaken through an

open approach using a 3- to 4-in. incision in the axilla,

although recent reports describe transaxillary and periare-

olar approaches that use conventional laparoscopic instru-

mentation [4]. With a laparoscopic approach, two small

incisions at the inferior border of the axilla accommodate

instruments, and the camera visualizes the axilla through a

periareolar incision. The resulting elimination of a linear

scar under the axilla may be the reason for reduced, but still

existent [5], risks of nerve injury, sensory disturbances,

shoulder stiffness, and mobility restrictions [4].

The consideration of moving the scar further from the

site of dissection and using smaller single incisions at sites

possibly considered less conspicuous may improve shoul-

der function and reduce the psychological burden of breast

cancer surgery. For novel surgical techniques such as nat-

ural orifice translumenal endoscopic surgery (NOTES), the

potential of the flexible endoscope as a means of under-

taking surgical procedures within the abdomen is being

explored. Currently, a wide range of surgical procedures

using the technique are described [6].

The unique benefit of the flexible endoscope is its

capability of being navigated from an access site to a dis-

tant target organ. Consequently, instruments can be

deployed through the biopsy channels to execute minor

interventions at that target site, a property clearly demon-

strated from its use in endoluminal interventions.

Subcutaneous tunneling is a technique that has been

used extensively for many years across a number of dif-

ferent surgical specialties, including vascular surgery, for

the placement of prosthetic vascular grafts in patients with

peripheral vascular disease. It also has been used in cardiac

surgery for minimally invasive long saphenous vein har-

vesting [7].

More recently, breast surgeons have successfully begun

to harness these subcutaneous avascular planes to under-

take transumbilical breast augmentation [8]. However, to

date, no reports have described the use of a flexible

endoscope tunneled from a site remote to the axilla to

facilitate axillary dissection. To this end and to document

the feasibility of such an approach, we describe the first use

of a transumbilical endoscopic levels 1 and 2 axillary

lymph node dissection in human cadaveric models with

pathologic confirmation of lymph node yields equivalent to

those of the current conventional approaches.

Methods

The transumbilical flexible endoscopic technique

Four axillary lymph node dissections were attempted in

three soft preserved human female cadavers. Alcohol,

phenol, glycerine soft preservation allows for greater tissue

manipulation than formalin fixation, although some color

differentiation of the tissues does tend to be lost, and pli-

ability is less than with living tissue.

One of the cadaver models had a breast cancer lesion for

which the woman had undergone palliative treatment with

no breast excision. However, unilateral axillary lymph

node dissection had been performed. Within this trial set-

ting, bilateral axillary dissection was performed on this

cadaver using the transumbilical approach both to explore

the feasibility of the technique on the contralateral side and

to investigate whether the same technique can be used to

approach an axilla when the associated breast has advanced

cancer. In light of the previous axillary dissection on this

axilla, a complete levels 1 and 2 axillary lymph node dis-

section was performed only on the remaining three axillas.

Access followed that described for the transumbilical

breast augmentation (TUBA) technique [8] (Figs. 1, 2). A

supraumbilical incision was made, with dissection continued

to the prefascial plane. A long tapered introducer and hollow

overtube (custom made in-house Fig. 3) was introduced

through the premade incision. The tube had an internal

diameter of 13.5 mm and an external diameter of 15 mm. A

15-mm bariatric trocar (Applied Medical, Rancho Santa

Margarita, CA, USA) was attached to the end of the tube,

which was sealed airtight. The introducer and overtube were

used to create a subcutaneous tunnel to the submammary

space aimed for the lateral edge of the inferior mammary fold.

Once at the fold, the introducer was removed, and the

trocar valve was replaced. Controlled air insufflation

through the tube exposed the submammary space, aided

initially by a long blunt dissector instrument (custom made

in-house), which enabled insertion of a 12-mm dual-

channel flexible endoscope (Karl Storz, Tuttlingen, Ger-

many) through the overtube for further dissection of the

space to expose the axillary borders. Dissection with con-

trolled air insufflation enhanced this avascular space, which

enabled further blunt dissection of the areolar tissue using

the endoscope tip under vision.

With the relative redundancy of the pectoralis major

muscles and a more lateral angulation of the overtube, the

interpectoral space could be found with relative ease. The

primary anatomic landmark for the axilla with this

approach was the lateral border of the pectoralis minor

muscle (Fig. 4).

With the arm abducted, dissection of the axilla was

undertaken using existing flexible endoscopic instruments,

Surg Endosc (2013) 27:478–486 479

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which included endoscopic graspers (Olympus Keymed,

Southend-on-Sea, Essex, UK), an electrocautery insulated-

tip knife (Olympus Keymed, Southend-on-Sea, Essex,

UK), and endoscopic diathermy scissors (LSVP Medical

Supplies, Los Altos, CA, USA). Using electrocautery, an

incision was made down the lateral border of the pectoralis

minor muscle, keeping close to the muscle itself dividing a

thin fascial layer overlying the anterior aspect of the axilla

and attaching to the pectoralis minor muscle. Once divided,

the axillary fat was freed but remained attached to the chest

wall, and the focus could be turned to exposure of the

axillary vein using cephalad-directed dissection.

Dissection was continued using a combination of blunt

and sharp dissection. In all cases an anterior cephalic vein

was noted before the axillary vessels became visible. These

were followed medially under the pectoralis muscle

(Fig. 5). Controlled air insufflation and blunt dissection

exposed the subpectoral space, enabling completion of a

level 2 dissection using endoscopic graspers coupled with

air insufflation and blunt dissection.

The posterior border of the fat was approached from the

inferior angle of the axilla. Caudal extension of the incision

along the lateral border of the pectoralis minor was

required. Blunt dissection enabled this inferior aspect of the

axilla to be teased away from the latissimus dorsi muscle at

the posterior border. Electrocautery was not used until the

thoracodorsal pedicle could be positively identified. Once

defined, the lateral border and the attachment to the

underlying subcutaneous fat of the skin were divided using

diathermy scissors as far cranially as the axillary vein. The

Fig. 1 External setup for the trials. Note the right arm of the cadaver is flexed and abducted at the shoulder

Fig. 2 Procedural steps undertaken to gain access to the axilla from

the umbilicus. A A supraumbilical incision to the prefascial plane is

made. B The introducer with an overtube is guided to the

inframammary fold. C The submammary space is dissected. D,

E The dissection creates access for the endoscope. F The cosmetic

outcome from the surgery is evident

480 Surg Endosc (2013) 27:478–486

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intercostobrachial nerve, which crosses within the axillary

fat, was identified but in all cases was not spared.

Division of the fat from the inferior border of the

axillary vessels marked the completion of the excision.

For the last two cases, a 2.3-mm minilaparoscopic

instrument (Stryker, Kalamazoo, Michigan, USA) was

inserted into the axilla via a needle incision on the upper

lateral border of the pectoralis major muscle. The axillary

fat was grasped and placed under tension to enable the

final portion of the dissection to be completed more

efficiently.

The specimen was removed en bloc through the sub-

cutaneous tunnel and exteriorized at the umbilical incision

(Fig. 6). Current endoscopic tissue retrieval techniques

were trialed including a dorma basket (Olympus Keymed,

Southend-on-Sea, Essex, UK), but the size of the specimen

far exceeded current basket sizes. The tunnel and axilla

were reexamined for any remaining tissue before the

overtube was removed and the wound closed.

All the specimens were sent for histopathologic analysis

to assess lymph node yield. In each case, the axilla was

opened and examined for neurovascular injury. Any injury

Fig. 3 Custom-made tools that include an introducer with a 14-mm-diameter overtube. A bariatric 15 9 150-mm trocar is secured to the

overtube and a hockey-stick blunt dissector

Fig. 4 The anterior border of the axilla as it appears once exposed by

the endoscope. The inset shows the images of the submammary space

when initially viewed by the endoscope. Note the loose avascular

tissue

Fig. 5 The internal anatomy of the axilla as viewed from the

endoscope, with the subpectoral space visible on the right. The insetshows the corresponding anatomy after completion of the surgery

Surg Endosc (2013) 27:478–486 481

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or residual tissue left within the axilla was verified by a

second examiner.

Patient motivation and acceptance

A questionnaire was created to assess whether such an

approach would be acceptable within the general popula-

tion when presented against the current conventional open

and periareolar laparoscopic techniques. The level of

complication risk that patients were willing to accept

should they choose the transumbilical technique also was

assessed through a series of questions that targeted their

operative preference when presented with various state-

ments of increasing risk severity for the techniques both in

isolation and together. Questions addressed the risk of

infection from the bellybutton to the armpit, the risk of

shoulder stiffness and sensory discomfort at or around the

armpit, and the hypothetical risk of cancer recurrence

compared with other approaches.

Because the complications of the technique can only be

assumed, incremental risk stratification was adopted in the

questionnaire to assess the point at which a given population

would be willing to accept the technique and the point at

which observers would revert to an alternative hypotheti-

cally safer technique. By this method, the answers given

would provide a level at which the technique must reliably

perform before it could be accepted by the general public.

The questionnaire was validated using three independent

general and breast surgeons whose comments were incor-

porated into the questionnaire before further review and

reevaluation. The questionnaire also was trialed with 10

members of the general public, whose comments and sug-

gestions were incorporated to ensure that the language used

was not technical and that the instructions were clear enough

for the questions to be completed without assistance.

The focus population for the questionnaire was women,

although not exclusively, from the age of 18 years and

upward. The general population was targeted, with ques-

tionnaires left in the jury suite of a Crown Court, at hair-

dressers, and at schools. Verbal permission was granted at

all sites for the questionnaires to be left. Members of the

public could pick up the questionnaire on their own voli-

tion. The questionnaire was anonymous, but a request was

made for the front page to be initialed and dated to confirm

that the individual agreed to be involved in the survey.

Internal validation of the questionnaire was undertaken

with the addition of a duplex question presented in a format

different from that of the original.

Questionnaires were excluded if the subject had not

initialed the agreement to participate on the front page or

when answers to the internal validation question did not

agree. The questionnaire presented the general public with

three techniques for approaching the axilla to perform

axillary dissection. These were shown as images of the

scars associated with the transumbilical, open, and peri-

areolar laparoscopic techniques.

Results

Questionnaire outcomes

Of the 127 questionnaires returned, 32 were excluded, 8

due to disagreement with the answers to the validation

questions. Consequently, 95 questionnaires were accepted

for analysis. The respondents were 87 women and 8 men

with a combined mean age of 41.6 ± 12.3 years. Three of

the women in the population surveyed had previously been

treated for breast cancer, one of whom had required axil-

lary surgery. Seven of the women had experienced some

Fig. 6 The axillary specimen excised from the cadaver (A) and the image of the axilla opened to expose the neurovascular bundles intact (B)

482 Surg Endosc (2013) 27:478–486

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form of breast surgery for benign disease. The full demo-

graphics of the surveyed population are shown in Table 1.

When given no information regarding risk or compli-

cations related to the three scar-site options, 73 % of the

population group questioned preferred the transumbilical

approach over the transaxillary or periareolar technique.

When presented with the potential complication of a

‘‘treatable infection under the skin from the bellybutton to

the armpit’’ with the transumbilical approach and no

complications disclosed for the other techniques, 19 %

changed to prefer the transaxillary approach, although

54 % still maintained their preference for the transumbil-

ical technique. Once again, when this was presented in

conjunction with complications related to the other

approaches (shoulder stiffness and wound discomfort), the

preference for the technique increased to 82 %. However,

when the transumbilical approach was presented with a

potential risk of cancer recurrence, preference fell to 15 %.

But when this was quantified as a risk of 1 in 500 for cancer

recurrence and presented with a reduction in the risk of

shoulder stiffness and wound discomfort, 20 % preferred

the transumbilical approach, suggesting that the improve-

ment in shoulder stiffness and wound discomfort may have

influenced their decision.

When the risk was further quantified, with an even

higher cancer recurrence risk of 1 %, 11 % of the public

still preferred the transumbilical technique over the alter-

native open axillary approach, which was presented with a

theoretical no risk of cancer recurrence (summarized in

Fig. 7). This suggests that cosmesis plays an extremely

important role in any operative decision made for the

subgroup evaluated in this survey.

Operative outcomes

Transumbilical levels 1 and 2 axillary dissection was

successfully undertaken in three soft preservation human

female cadavers. The transumbilical axillary approach

performed on the cadaver with a fixed breast lesion was

successfully carried out. The submammary space was

opened using pulsed air insufflation and blunt dissection.

The presence of the advanced breast lesion did not restrict

access to the axilla, as confirmed with the anatomic

demonstration of the pectoralis minor muscle. However,

scar tissue and distortion of the axillary anatomy restric-

ted further endoscopic dissection, suggesting that the

technique would not be suitable for recurrent axilla

disease.

The contralateral axillary levels 1 and 2 dissection in the

same cadaver and in the remaining two cases was suc-

cessfully managed. In the second cadaver, electrocautery

was only intermittent, thought to be due to the age and

therefore the decomposition of the cadaveric specimen,

which in turn reduced the electrical conductivity of the

tissue. Because such sharp dissection was used, the oper-

ative time for this procedure on this cadaver was consid-

erably lengthened.

The operative times for the endoscopic levels 1 and 2

axillary dissection in each of the cadavers were 1080, 840,

and 390 min (in sequential order), with clear improvement

in the times noted from the first to the last attempt. In each

case, the whole of the specimen was submitted for histo-

logic examination by a pathologist (R.D.G.).

Although the lymph nodes were autolytic as expected,

they were clearly identifiable. The lymph node harvests

were respectively 12, 11, and 14. In the case that involved

extraction of the specimen from the cadaver with a con-

tralateral breast lesion, four lymph nodes were identified as

positive for cancer (Fig. 8).

Open examination of the axillas showed that in all three

cases, the intercostobrachial nerve was sacrificed, but the

axillary vessels, thoracodorsal pedicle, and long thoracic

nerves all were identified in each case as undamaged.

Table 1 Demographics of the population who met the inclusion

criteria for the questionnaire

Sex Marital status

Female 87 Married 52

Male 8 Single 32

Divorced 4

Age (years) Widowed 1

18–30 20 Not answered 6

31–40 30

41–50 20

51–60 17 Ethnicity

61–80? 8 Caucasian 70

Mean age 41.6 African 10

Asian 5

Surgical history Oriental 3

Previous surgery 61 Middle Eastern 2

Previous laparoscopy 17 South American 1

Previous endoscopy 20 Not answered 4

Previous cancer 3

Previous breast cancer 3

Previous breast benign 7 Religion

Previous axillary surgery 1 Christian 62

No religion 24

Education Muslim 2

Secondary school 11 Buddhist 2

Sixth-form college 12 Other 2

Undergraduate 28 Sikh 1

Postgraduate 42 Not answered 2

Not answered 2

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Discussion

The introduction of the flexible endoscope into surgical

practice exposes the potential for a range of novel surgical

approaches to be developed. The unique flexibility of the

platform coupled with the delivery of interventional tools

to the tip (e.g., scissors, graspers, and dissectors) enables

the position of the incision to be distant from the target

organ. This advantage may provide significant benefits in

terms of reduced scarring in and around the operative area,

with a positive impact on the associated morbidities such as

shoulder stiffness or sensory discomfort at the wound site.

Fig. 7 Graphic representation of the outcomes from the questionnaire. The questions presented to the general public in the questionnaire are

summarized under each of the respective responses

Fig. 8 A Low-power histology of one of the excised lymph nodes. B High-power magnification demonstrating evidence of tumor deposits.

The largest is arrowed

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The advantage of the ability to make the incision distant

from the target organ has been exploited by the NOTES

community for the cosmetic benefits it provides [9].

However, the major obstacle to NOTES deployment is

closure of the unavoidable translumenal breach, with

leakage and contamination possibly proving disastrous.

Hence, the limited indications for NOTES clinicians have

applied to date. Nevertheless, this challenge should not

result in the abolishment of the flexible endoscope for

surgical applications. The potential opportunity raised

through NOTES, reiterated by the questionnaire described

earlier, points to the value that the population places on the

cosmetic outcomes from surgery. Furthermore, the impor-

tance placed by each individual on these outcomes and

even the differences of opinions as to what may be con-

sidered cosmetically appropriate also are evident, poten-

tially relating to the individual’s own preferences for his or

her body.

The question as to whether surgery should be targeted

more to the individual than to a generic approach needs to

be considered. The possibilities of personalized surgery

have the potential to be realized with the wider introduc-

tion of flexible operative platforms such as the endoscope

into the operating theatre. This would enable scars to be

placed at any location on the body and targets to be

approached using the subcutaneous techniques described.

This has been shown in other operative scenarios such as

thyroidectomy, which has shown a successful approach

from either the axilla or the mouth [10, 11].

As a flexible surgical platform, the diagnostic flexible

endoscope has had some problems related to its design,

intended to enable navigation within the confines of the

bowel lumen. The uncontrollable flexibility essential

within this environment confounds not only accurate and

effective target navigation but also the stability of the

endoscope when flexed, which is essential for instrumen-

tation precision when the platform is taken into the spatial

environment of the peritoneal or axillary space.

Within the setting of the transumbilical axillary

approach, the rigid overtube and subcutaneous tunnel

provide some of the support required for navigation and, to

some extent, stability during intervention but not enough

for an effective and reliable procedure to be completed

within an acceptable time frame. The ergonomics are fur-

ther impeded by no instrument triangulation at the endo-

scope tip.

The lack of both interventional control and triangulation

were very evident when the operative times for the tran-

sumbilical axillary dissection were considered but even

more evident in comparison with the last trial. This trial

demonstrated a markedly shorter operative time than the

initial two trials. Although, this may have been due to the

proficiency curve associated with the technique itself, it is

more likely that the introduction of a needlescopic grasper

to provide the tension on the specimen for dissection was

more significant.

Overcoming instrument triangulation is vital for a totally

transumbilical procedure. This coupled with the introduc-

tion of more specifically designed instrumentation for

flexible endoscopic operations not only would further

reduce the operative time, making it more clinically

acceptable, but also may promote greater nerve sparing and

contribute to reducing the overall morbidity further. This

may be particularly pertinent when the intercostobrachial

nerve is considered. Although the nerve was clearly visible

from the endoscope as it crossed the axilla in all three

cadavers, it could not be preserved almost entirely due to

the lack of instrument tip triangulation.

The final hurdle to overcome is the challenge of the

endoscope ergonomics itself. The learning curve associated

with intraluminal endoscopy to obtain proficiency is signif-

icant. With the challenges of navigating the endoscope

within a spatial environment such as the axilla, it is likely that

the learning curve will be even greater, having an impact not

only on the introduction of this approach but also on future

procedures involving the use of the flexible endoscope.

Only through innovation will these challenges be over-

come. Novel platform designs have already been developed

to explore these problems, but many have been based on

the flexible endoscope with devices that deal with either the

uncontrollable flexibility (e.g., Shapelock; USGI Medical,

San Clemente, CA, USA) or the triangulation (e.g., Anubis;

Karl Storz) but not both.

It is likely that the answer may eventually lie within the

field of robotics. Articulating robots that provide both

stability and control with interventional capabilities are

under development [12], but the additional requirement to

overcome the triangulation still remains a significant

research and engineering challenge.

Finally, no contemporary discussion regarding the role of

axillary lymph node dissection would be complete without

consideration of the recent results from the Z11 study. In this

study, Giuliano et al. [13] randomized women with positive

nodal disease detected by sentinel lymph node biopsy

(SLNB) to axillary lymph node dissection (ALND)

(n = 445) or no ALND (n = 446). These authors observed

similar rates of local and regional recurrence rates and no

significant difference in 5-year survival. Despite the

importance of this study in asking an important question

regarding the role of ALND and improving oncologic out-

comes, axillary dissection remains the current standard of

care for patients with SLNB-positive macro metastases [13].

Considering SLNB in isolation, the theoretical benefits

of a small transumbilical incision are no longer valid,

particularly considering the size of the incision required

for SLNB (usually only about 2.5 cm). Furthermore,

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additional challenges are likely regarding the ease of

identifying the sentinel node using this approach and

indeed regarding the time required to identify the node with

a dual technique. More specifically this is true when con-

sidering agents such as patent V blue dye, which may

adversely influence the endoscopic view, or gamma probe

detection of radioisotope, which also would be problematic

unless it could be made to fit down the working channel of

the endoscope.

Conclusion

The transumbilical approach to the axilla using the flexible

endoscope is feasible, and axillary dissection can be per-

formed safely, with node yields equivalent to those realized

with the open approach. Furthermore, it appears that the

transumbilical approach would be acceptable to the

majority of the general female public if it could demon-

strate a reduced risk of shoulder stiffness and sensory

discomfort at the wound site and also prove to be as on-

cologically safe as open surgery. Nevertheless, it is

apparent that a subgroup of the population places cosmesis

above all other factors, although under the circumstances of

a known breast cancer, it truly is unknown how many

would in reality succumb to the need for an excellent

cosmesis despite the risk of cancer recurrence. However,

only with formal clinical trials can the true benefits of this

approach be realized.

Acknowledgments We acknowledge Karl Storz, Tuttlingen, Ger-

many, for the kind loan of the endoscopic equipment used in this

study, and the Charing Cross Hospital Human Anatomy Unit, Divi-

sion of Surgery, Imperial College London, for the use of its staff and

facilities.

Disclosures James Clark, Daniel Richard Leff, Mikael Sodergren,

Richard Newton, David Noonan, Robert Goldin, Ara Darzi, and

Guang-Zhong Yang have no conflicts of interest or financial ties to

declare.

References

1. World Health Organization (2011) Global cancer database.

WHO, New York

2. UK CR (2011) Cancer statistics for breast cancer

3. Lam WW, Li WW, Bonanno GA, Mancini AD, Chan M, Or A

et al (2011) Trajectories of body image and sexuality during the

first year following diagnosis of breast cancer and their rela-

tionship to 6 years psychosocial outcomes. Breast Cancer Res

Treat 131:957–967

4. Lim SM, Lam FL (2005) Laparoscopic-assisted axillary dissec-

tion in breast cancer surgery. Am J Surg 190:641–643

5. Aponte-Rueda ME, Saade Cardenas RA, Saade Aure MJ (2009)

Endoscopic axillary dissection: a systematic review of the liter-

ature. Breast 18:150–158

6. Sodergren MH, Clark J, Athanasiou T, Teare J, Yang GZ, Darzi

A (2009) Natural orifice translumenal endoscopic surgery: critical

appraisal of applications in clinical practice. Surg Endosc 23:

680–687

7. Athanasiou T, Aziz O, Skapinakis P, Perunovic B, Hart J,

Crossman MC et al (2003) Leg wound infection after coronary

artery bypass grafting: a meta-analysis comparing minimally

invasive versus conventional vein harvesting. Ann Thorac Surg

76:2141–2146

8. Dowden RV (2008) Transumbilical breast augmentation is safe

and effective. Semin Plast Surg 22:51–59

9. Marescaux J, Dallemagne B, Perretta S, Wattiez A, Mutter D,

Coumaros D (2007) Surgery without scars: report of transluminal

cholecystectomy in a human being. Arch Surg 142:823–826

discussion 826–827

10. Karakas E, Steinfeldt T, Gockel A, Schlosshauer T, Dietz C,

Jager J et al (2011) Transoral thyroid and parathyroid surgery:

development of a new transoral technique. Surgery 150:108–115

11. Fan Y, Wu SD, Kong J (2011) Single-port access transaxillary

totally endoscopic thyroidectomy: a new approach for minimally

invasive thyroid operation. J Laparoendosc Adv Surg Technol A

21:243–247

12. Shang J, Noonan DP, Payne C, Clark J, Sodergren M, Darzi A,

Yang GZ (2011) An articulated universal joint based flexible

access robot for minimally invasive surgery. In: 2011 IEEE

international conference on robotics and automation, Shanghai,

China, pp 1147–1152

13. Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth

PW, Blumencranz PW et al (2011) Axillary dissection vs no

axillary dissection in women with invasive breast cancer and

sentinel node metastasis: a randomized clinical trial. JAMA

305:569–575

486 Surg Endosc (2013) 27:478–486

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