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 A Practical Guide to
Peritoneal Malignancy
The PMI Manual
 A Practical Guide to
Peritoneal Malignancy
The PMI Manual

Edited by
Tom Cecil
Clinical Director, Peritoneal Malignancy Institute Basingstoke
Hampshire Hospitals NHS Foundation Trust
Honorary Transplant Surgeon
Oxford University Hospitals, Oxford, UK

John Bunni
Consultant Colorectal and General Surgeon
Royal United Hospital Bath, Bath, UK
Honorary Lecturer, Cardiff University, Cardiff, Wales
Visiting Lecturer, University of Bath, Bath, UK

Akash Mehta
Consultant Colorectal Surgeon, St Mark’s Hospital and
Academic Institute, London, UK
CRC Press
Taylor & Francis Group
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© 2020 by Taylor & Francis Group, LLC

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No claim to original U.S. Government works

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Library of Congress Cataloging-in-Publication Data

Names: Cecil, Tom (Colorectal surgeon), editor. | Bunni, John, editor. | Mehta, Akash, editor.
Title: A practical guide to peritoneal malignancy : the PMI manual /
edited by Tom Cecil, John Bunni, Akash Mehta.
Description: Boca Raton, FL : CRC Press, 2019. | Includes bibliographical references and index.
Identifiers: LCCN 2019024858 (print) | ISBN 9781138495111 (paperback ; alk. paper) | ISBN 9781138495050
(hardback ; alk. paper) | ISBN 9781351024860 (ebook) Subjects: MESH: Peritoneal Neoplasms | Peritoneal
Diseases | Cytoreduction Surgical Procedures | Perioperative Care
Classification: LCC RC867 (print) | LCC RC867 (ebook) | NLM WI 575 | DDC 616.3/8--dc23
LC record available at https://lccn.loc.gov/2019024858
LC ebook record available at https://lccn.loc.gov/2019024859

Visit the Taylor & Francis Web site at

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This book is dedicated to all our patients who have trusted us and
given us the privilege of treating and ­caring for them.
Contents

List of Abbreviations ix
Foreword xi
Preface xv
Acknowledgements xix
Contributors xxi

Part I Set: Understanding and assessment of peritoneal disease 1

1 Appendix tumours and pseudomyxoma peritonei: A ‘paradigm’ for peritoneal disease 3

Akash Mehta and Tom Cecil
2 Colorectal peritoneal metastases 17
John Bunni and Brendan Moran
3 Peritoneal mesothelioma 35
Faraz Khan and Faheez Mohamed
4 Miscellaneous peritoneal malignancies 43
Andreas Brandl and Akash Mehta
5 Quantitative assessment of peritoneal disease 51
John Bunni and Sanjeev Dayal
6 Imaging in peritoneal malignancy 59
Anuradha Chandramohan and Andrew Thrower

Part II Dialogue: Intraperitoneal chemotherapy and cytoreductive surgery 75

7 Intraperitoneal chemotherapy 77
Akash Mehta and Faheez Mohamed
8 Perioperative and anaesthetic care 89
Nina Ashraf-Kashani and John Bell
9 Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy 97
John Bunni and Tom Cecil
10 Postoperative care 113
Nina Ashraf-Kashani and James Coakes
11 Postoperative complications 119
Kim Govaerts and Brendan Moran

vii
viii Contents

Part III Closure: Ongoing care and future management options 127

12 Histopathological aspects of peritoneal malignancy 129

Babatunde Rowaiye and Norman Carr
13 Follow-up protocols in peritoneal malignancy 147
Anuradha Chandramohan, Sourav Panda and Nehal Shah
14 Recurrence of pseudomyxoma peritonei 157
Jamish Gandhi and Alexios Tzivanakis
15 Future perspectives in peritoneal malignancy 163
Ioanna Panagiotopoulou, Alexios Tzivanakis and Tom Cecil

Index 183
List of Abbreviations

5FU 5-Fluorouracil ICAM-1 Intercellular adhesion molecule 1

AUC Area under the curve IL-1β Interleukin-1 beta
BSO Bilateral salpingo-oophorectomy IP Intraperitoneal
Cb Concentration in the systemic IPFC Intraperitoneal free cancer cells
circulation IV Intravenous
CMS Consensus molecular subtypes LAMN Low-grade appendiceal mucinous
Cp Concentration in the peritoneal cavity neoplasm
circulation LV Leucovorin
CPM Colorectal peritoneal metastases MMC Mitomycin C
CRLM Colorectal liver metastases MRI Magnetic resonance imaging
CRS Cytoreductive surgery Ox Oxaliplatin
CT Computed tomography PCI Peritoneal Cancer Index
DMPM Diffuse malignant peritoneal PIPAC Pressurized intraperitoneal aerosol
mesothelioma chemotherapy
DW-WB Whole-body diffusion-weighted MRI PMP Pseudomyxoma peritonei
EPIC Early postoperative intraperitoneal PSOGI Peritoneal Surface Oncology Group
chemotherapy International
ESSO European Society of Surgical Oncology Rd Pharmacokinetic advantage
GPM Gastric peritoneal metastases TME Total mesorectal excision
HAMN High-grade appendiceal mucinous TNF-α Tumour necrosis factor-alpha
neoplasm VCAM-1 Vascular cell adhesion molecule 1
HIPEC Hyperthermic intraperitoneal WDPM Well-differentiated papillary
chemotherapy mesothelioma

ix
Foreword

1987. The presentation concerned 14 patients with

BASINGSTOKE a rare disease referred to as pseudomyxoma peri-
tonei. We combined surgical removal of this large
I have been fascinated by the natural history of volume but minimally aggressive malignancy that
gastrointestinal and gynecologic malignancy arose from an appendiceal adenoma with a chemo-
throughout my surgical career. Why do surgeons therapy washing of the peritoneal space with the
so often fail in their efforts to cure the primary drugs available at that point in time. These drugs
malignancy when all the disease is removed that were mitomycin C and 5-fluorouracil. Amazingly
is visible to the naked eye? Liver metastases take about half of these patients are still alive today, and
the lives of many of our patients. Of course, cancer several of them lived over a decade prior to their
cells that cause liver metastases travel through the death from local progression of disease within the
portal blood where these cells are trapped within peritoneal space. This early report was published in
the sinusoids of the liver, implant and then grow. the Disease of the Colon and Rectum in the October
Although rejected early on, successful treatment of 1987 issue [2].
liver metastases from colon and rectal cancer was A second success story with appendiceal
eventually established [1]. malignancy was published in 1993. This report
Perhaps the dissemination of cancer to the peri- concerned 69 patients we accumulated over a
toneal surfaces is considerably more complex. The 10-year interval appendiceal peritoneal metasta-
spread can occur prior to, but often at the time of a ses. This report showed that a low-grade histol-
cancer resection. Definitely, the surgical procedure ogy, presence of extensive abdominal mucinous
is part of the natural history of gastrointestinal and ascites, complete resection and absence of lymph
gynecologic malignancy. How much does the sur- node metastases were associated with long-term
geon’s dissection contribute to the high incidence survival. There was a 35% serious complication
of peritoneal metastases documented in follow-up rate in this group of patients and a single post-
in patients with gastric cancer, pancreatic cancer, operative death from central venous line catheter
and colorectal cancer? sepsis [3].
The presence of peritoneal metastases, liver It is my assumption that Professor Bill Heald,
metastases or lung metastases in the 1980s was with his great compassion for the optimal man-
considered as a terminal condition with no reason- agement of patients and his innate intellectual
able treatments available. Of course, resection of curiosity, associated this publication in Diseases
liver metastases has become a standard of care. The of the Colon and Rectum with a patient that he
story of peritoneal metastases did not move quite had heard about in Scotland. Brian was a young
so briskly. Perhaps the first report of success in the and otherwise healthy Scotsman in his mid-30s
management of peritoneal metastases was reported who had an expanding abdomen. He had been
at the American Society of Colon and Rectal given the diagnosis of pseudomyxoma peritonei.
Surgery meeting in Washington, DC, in April of Although not the responsible physician, Professor

xi
xii Foreword

Heald wondered if these new, recently described to Waterloo Station in London. There we met with
treatments were applicable to this individual. Mr. an Officer of the National Health Service, Dr.
Heald called my office in Washington, DC, and Peter Doyle. We discussed the problem of pseu-
talked with my wife, Ilse. I then called him back domyxoma peritonei and the mucinous appendi-
from Vienna, Austria where I was participating in ceal malignancies within the UK. It was quite an
a continuing medical education course devoted to extensive discussion and required a pile of scones
peritoneal metastases. I flew to London on Sunday, and several cups of tea. Surprisingly enough, this
March 20, 1994, and visited with the patient. On enthusiastic NHS administrator seemed interested
Tuesday, March 22, 1994, Bill Heald, his Senior in this problem despite the lack of firm evidence
Registrar, Brendan Moran, and I performed a that this was a valid treatment option and that the
13-hour surgical procedure on Brian. experience at Basingstoke was limited. An initial
We had almost all of the equipment necessary application for NHS support for peritoneal malig-
for an optimal cytoreductive surgical event. We nancy was rejected, but a subsequent application
had the Thompson fixed/self-retaining retractor, by Brendan Moran for ‘Pseudomyxoma Peritonei
we had a Birtcher 5000 electrosurgical generator, of Appendiceal Origin’ was approved based on his
and we had lots of enthusiasm towards trying to now underestimated calculation that this rare dis-
help out in what was considered an impossible ease had an incidence of one per million per year.
clinical situation. We lacked a smoke evacuation Basingstoke was approved as a National Treatment
apparatus. There was a slight inconvenience for Centre in April 2000.
the fire brigade in North Hampshire. The exces- Additional cases of pseudomyxoma peritonei
sive electrosurgical smoke set off the fire alarm on were referred to Basingstoke. These all came as a
three different occasions causing the fire brigade to result of word-of-mouth contact among physi-
repeatedly come to the hospital, peer into the oper- cians around the UK and surgeons at the North
ating room and then leave with a smile on their Hampshire Hospital. In order to move this along,
faces but somewhat disgusted in that they came Mr. Heald and Mr. Moran organized the first ever
such a distance with all of their equipment to view peritoneal metastases meeting within the UK.
a surgical procedure performed by ball-tip electro- It was courageous of the group in Basingstoke to
surgical dissection. go ahead with a meeting at the North Hampshire
We placed all the tubes and drains required for Hospital on October 9 and 10, 1998. Although the
early postoperative intraperitoneal chemotherapy. attendance was limited to approximately 30 peo-
I tried to make sure that the early postoperative ple, lots of ideas regarding expansion of this con-
intraperitoneal chemotherapy would happen with- cept of cytoreductive surgery and perioperative
out incident and left to perform a liver resection in chemotherapy to other countries in Europe and
Italy. I remember that at a meeting in Venice, the around the world were formulated. It is amazing
Italian professor rebuked this concept of a surgical to me the foresight that Bill Heald and the group
treatment of peritoneal metastases as an unrealis- at Basingstoke had regarding the management of
tic surgical exercise in futility. peritoneal metastases!
Due to the expert care given Brian at the North In late 1999, a particularly problematic patient
Hampshire Hospital, he recovered from his five who had had extensive prior surgery came up on the
peritonectomy procedures, two colon resections, operative schedule at North Hampshire Hospital.
and early postoperative chemotherapy without Mr. Brendan Moran and I operated together on
incident. He lived after this for nine years, passing September 28, 1999. John was a mid-50-year-old
on August 26, 2003 of recurrent disease intimately Irishman with a recurrent pseudomyxoma perito-
associated with the small bowel and its mesentery. nei post-debulking in Dublin, having had 7 prior
He was not thought to be a candidate for a reopera- operations in Dublin. The surgery and his periop-
tive surgical event. erative chemotherapy went well. John remained
My next trip to Basingstoke was on June 11, 1997. cured from his pseudomyxoma and sadly died
Bill Heald and I took the train from Basingstoke from an unrelated pneumonia two years ago.
 Foreword xiii

The Millennial Masterclass on peritoneal Table 1. Time Line for Pseudomyxoma Institute
metastases organized by Professor Heald was held
• Sugarbaker et al., 69 appendiceal cancer
at the Royal College of Surgeons on June 1 and
patients treated by cytoreductive surgery and
2, 2000. The attendance was limited to approxi-
intraperitoneal chemotherapy, April 1993,
mately 50 people, but some very important persons
Diseases of the Colon & Rectum. Read and
were there and took these concepts back to their
appreciated by Bill Heald.
home institutions. I remember well having some
extended discussions with Professor Dominique • Brian operated on at North Hampshire
Elias, the new professor at Villejuif, France. He was Hospital on March 22, 1994, by Sugarbaker,
very interested in an exhibit of the open method for Heald and Moran. 9-year survival.
hyperthermic intraoperative intraperitoneal che- • Heald and Sugarbaker meet at Waterloo
motherapy administration. Apparently, Dr. Elias Station in London on June 11, 1997, with
was impressed because he started his own pro- NHS Administrator, Peter Doyle.
gram in Villejuif, which has been one of the most • First PSM meeting in Basingstoke, October
successful in terms of new information regarding 9–11, 1998.
peritoneal metastases. • John operated on at North Hampshire
A final meeting that helped firmly establish Hospital on September 28, 1999, by
Basingstoke as the centre for peritoneal metastases Sugarbaker and Moran. 13-hour surgery, 20
work in the UK was a meeting at the newly orga- years and no evidence of disease.
nized Pelican Centre. To my knowledge this was the • Millennial Masterclass, June 1–2, 2000, and
first time a live surgery was transmitted to a large Royal College of Surgeons.
audience. We performed a pseudomyxoma peri- • North Hampshire Hospital, Basingstoke
tonei surgery on December 5, 2002, and then had commissioned by NSCAG in 2000 to treat
a series of didactic sessions on December 6, 2002. pseudomyxoma peritonei.
The pictures from this event are still available. • Pelican Centre live surgery and didactic
It is abundantly clear to me that the centraliza- presentations, December 6, 2002.
tion of the complex treatment of a rare disease has • Christie Cancer Centre, Manchester
been of great success both in terms of high quality commissioned by NSCAG in 2002 to treat
patient care and academic productivity. The struc- appendiceal neoplasms.
tured approach with proper funding provided by • Good Hope Hospital, Birmingham
the National Specialist Advisory Commissioning commissioned by NHS England in 2014 to
group with Basingstoke as a National Treatment treat colorectal peritoneal metastases.
Centre has been a great success. This foresight
has allowed the unit to grow into one of the larg- Clinical Director, and the manual that Tom Cecil
est centres for peritoneal malignancy in the world put together with John Bunni and Akash Mehta
and allowed the development of a second National is a contribution to the continued development
Pseudomyxoma Unit at the Christie Cancer Centre of the peritoneal malignancy treatment centre.
in Manchester in 2002. In 2013, NHS England The manual aims to provide a practical informa-
commissioned the treatment of colorectal peri- tion for the understanding, assessment and treat-
toneal metastases making this treatment eas- ment of peritoneal disease for both the generalist
ily accessible for patients with a third centre for and the specialist. It is broken into three sections
Colorectal Peritoneal Metastases at Good Hope based on the UK Lapco National Train the Trainer
Hospital in Birmingham, established by Haney learning structure—the ‘Set’ focusing on under-
Youssef (Table 1). standing and assessment of peritoneal disease,
It has been my great pleasure to be associated the ‘Dialogue’ looking at the technical and prac-
with the Peritoneal Malignancy Institute at North tical aspects of delivering cytoreductive surgery
Hampshire Hospital. They have accomplished and HIPEC with special focus on the management
an incredible amount over these last 35 years. of complications, and finally ‘Closure’ exploring
The program is now headed by Tom Cecil, the ongoing care and future developments. The experts
xiv Foreword

from the Peritoneal Malignancy Institute have all the liver for colorectal carcinoma metasta-
contributed to the manual, and I hope that you find ses: A multi institutional study of indications
it interesting and useful in the future safe manage- for resection. Surgery 1987; 103: 278–288.
ment of your patients. 2. Sugarbaker PH, Kern K, Lack E. Malignant
Respectfully submitted, pseudomyxoma of colonic origin. Natural
history and presentation of a curative
Paul H. Sugarbaker, MD approach to treatment. Dis Colon Rectum
MedStar Washington Cancer Institute 1987; 30: 772–779.
Washington, DC, USA 3. Sugarbaker PH, Zhu B, Banez Sese G,
Shmookler B. Peritoneal carcinomatosis from
REFERENCES appendiceal cancer: Results in 69 patients
treated by cytoreductive surgery and intra-
1. Hughes KS, Simon RM, Songhorabodi S, peritoneal chemotherapy. Dis Colon Rectum
Sugarbaker PH, other members of the 1993; 36(4): 323–329.
Hepatic Metastases Registry: Resection of
Preface

It is an honour to be editor of the A Practical Guide the biological host response, and probably less so
to Peritoneal Malignancy: The PMI Manual. It is than previously thought as ‘the highways of metas-
especially humbling to see this book materialise tases’ and certainly clinically less significant than
from what started off as an idea and discussion vascular invasion, which would more often than
in the ‘Ark’ in Basingstoke to the culmination of not result in liver metastases.
a vast array of doyens putting their expertise and But the next part of the story, the deeper under-
wisdom into print. standing of the transcoelomic spread of exfoli-
Despite all of the surgical advances and readily ated tumour cells through the redistribution
accessible information in today’s digital era, peri- phenomenon, was of immense importance to me.
toneal malignancy still seems to be a mystery to It highlighted that cases of peritoneal metastases
many surgeons. The pathophysiology, clinical sub- represented, biologically speaking, regional dis-
types and management are much less familiar to ease and not necessarily systemic disease as most
cancer clinicians than the assessment and manage- oncologists and physicians believe. This was of
ment of liver metastases, for example. immense and fundamental importance to my
I was originally attracted to Basingstoke for its intellectual grasp of cancer surgery.
foundation as the ‘home of total mesorectal exci- Peritoneal metastasis, treated with good sur-
sion (TME)’. A beautiful surgical concept, rooted gery in the right patients, is not a terminal process
in embryology, which highlights the primacy of anymore. Management of this challenging condi-
precise, ontogenetic surgery, whereby the cure of tion highlights more than ever that the foundation
the patient is found in the surgeon’s hands faith- of effective surgery is truly in the decision making,
fully dissecting along ‘Holy Planes’ in correctly reinforcing the mantra that ‘decisions are more
selected patients. This concept alone has changed important than incisions’.
the outcome for rectal cancer patients worldwide The model for understanding peritoneal disease
and is one to which all colorectal surgeons remain all began with appendiceal mucinous tumours,
wedded. I, for one, have spent many, many hours now known as low-grade appendiceal mucinous
mesmerised watching Bill and Brendan’s open neoplasms (LAMN). These tumours, whilst not
TME videos from years ago, which were the mech- spreading via the blood vessels (and lymph nodes)
anism for spreading this vital idea. as traditional malignancy does, spread transcoe-
During my time at PMI Basingstoke, another lomically throughout the abdomen, continuously
chapter of surgical understanding descended onto dividing and eventually resulting in the clinical
me. This was somewhat unexpected as my main syndrome of pseudomyxoma peritonei. Without
passion was rectal cancer. As a result of PMI, I had intervention, this condition will cause nutritional
developed a fuller comprehension of peritoneal dis- failure, obstruction, sepsis and death. Here one
ease: the mechanisms of metastases, their clinical has a tumour traditionally considered ‘benign’
manifestation, management and prognosis. When but with deleterious consequences for the patient
considering systemic disease, I had always believed due to a different but equally dangerous mode of
that lymph node metastases were more a marker of spread, of all albeit, ‘low-grade’ disease.

xv
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