TRANSPLANTATION

Small bowel
transplantation e the latest
developments

Whats new?
C
C

Alan Wiles
Simon Gabe

Stephen Middleton
C

Abstract

Intestinal transplantation has become a routine clinical procedure for

selected patients. Over the last 10 years patient survival figures have
improved considerably and are now approaching those receiving organs
such as liver, lung and heart. Patient selection has improved and immunosuppression has been enhanced by the introduction of lymphocyte modulating
antibody therapy combined with less potent maintenance immunosuppression. The indications for intestinal transplantation remain conservative at
present and largely reserve this procedure for patients who have life threatening complications of parenteral nutrition or require surgical procedures
that make simultaneous or subsequent transplantation advantageous.
However, as survival figures improve the indications are beginning to
broaden to include consideration of quality of life. Survival after transplantation is approaching that associated with uncomplicated parenteral nutrition
and if this trend continues it may replace parenteral nutrition as the treatment of choice for patients with irreversible intestinal failure. This article
describes the current indications for intestinal transplantation and the
current results of the procedure. Guidelines for referring patients for transplantation assessment and for the management of the sick transplant patient
are given. The need to consider referral of patients at an early stage to allow
timely assessment for transplantation is also discussed.

progress but following the introduction of a series of powerful antirejection agents in the late 1980s,4,5 a cluster of reports appeared
describing transplantation of part or all the intestine both in
combination with other organs and as isolated grafts.6e9
However, long-term survival remained modest at best10 until
the introduction of lymphocyte-depleting induction therapy with
agents such as alemtuzumab (Campath-1H) in the 1990s,11,12 and
the appreciation that thorough preoperative preparation, patient
selection and scrupulous postoperative management are of critical
importance (Figure 1).13 Now, intestinal transplantation can be
considered as a routine component of the management of adult
and paediatric patients with intestinal failure, and is beginning to
replace parenteral nutrition in the long-term management strategy
for many of these patients. Currently, children tend to have better
survival than adults after 5 years (Figure 2).

The current role of transplantation in the management of

intestinal failure

Keywords infections; intestinal; multivisceral; NASIT; nutrition;

transplantation

The survival rates of patients requiring home parenteral nutrition

(HPN) range between 86e97% at 1 year, 57e83% at 5 years and
43e71% at 10 years.14e16 Survival following intestinal transplantation (any combination of organs including small intestine),
as reported by the international registry,10 (which receives
details of >90% of all cases world wide) is lower (Table 1) but
this survival gap is continuing to close. In the better performing
centres,17,18 survival figures approximate to those on HPN,
particularly for patients given lymphocyte-depleting induction
therapy, whose survival at 1 and 5 years has been reported to be
as high as 90% and 70% respectively.17 Patient survival at the
largest UK adult transplantation centre in Cambridge has also
improved, with 2-year non-oncological survival pre- and post2007 of 50% and 100% respectively, associated with a 10-fold
increase in procedures undertaken per year. The larger of the UK
paediatric transplantation centres, in Birmingham, also has
improved results, reporting 69% 3-year survival since 1998 and
31% before this.19 If these improved survival rates are reproduced in other centres and prove a match for those of HPN at
10 years, intestinal transplantation may become the preferred
primary treatment for irreversible intestinal failure, rather than
being largely reserved for those who respond poorly to HPN. It

A brief history of intestinal transplantation

The earliest significant innovations in the technical aspects of
intestinal transplantation are considered to be the canine models
developed by Richard Lillehei in the 1950s1 and 60s,2 and the
vascular anastomotic techniques of Carrel.3 Graft rejection impeded

Alan Wiles BA DPhil BMBCh MRCP is a Senior Transplantation Fellow at

Addenbrookes Hospital, Cambridge University NHS Trust and has
recently been appointed as a Consultant Gastroenterologist at Queen
Elizabeth Hospital, Kings Lynn, UK. Competing interests: none declared.
Simon Gabe BSc MD MSc FRCP is a Consultant Gastroenterologist at St
Marks Hospital in Harrow, UK. Competing interests: none declared.
Stephen Middleton MA MD FRCP FAHE is a Consultant Physician and
Gastroenterologist at Addenbrookes NHS Trust, Cambridge University
Teaching Hospital, UK. Competing interests: none declared.

MEDICINE 39:3

Improved survival figures: 1 year 85%; 5 years 70%

Survival gap between home parenteral nutrition (HPN) and
transplantation is closing
Quality of life on home parenteral nutrition HPN can be
improved by transplantation
National Adult Intestinal Transplantation (NASIT) Forum e UK
forum to discuss all patients before transplantation
CaMi (Cambridge-Miami) score: first preoperative scoring
system to estimate postoperative survival following intestinal
transplantation
It is now a requirement that all suitable patients should be
referred (or discussed) for assessment at an appropriate stage
before they lose the opportunity of transplantation

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TRANSPLANTATION

Patient survival following intestinal transplantation in different eras

between 1985 and 2009
Logrank p < 0.001

1.0

1: 19851989
2: 19901994
3: 19952000
4: 20002004
5: 20052009

Survival probability

0.8

0.6

0.4

0.2

0.0
1
2
3
4
5

23
131
409
757
856

4
39
146
196
0

1
25
68
0

1
10
0

0
0

10

15

20

Years
Figure 1

Patient survival following intestinal transplantation according to age

of patient
Logrank p < 0.584

1.0

1: 02
2: 36
3: 717
4: 18-50
5: 51+

Survival probability

0.8

0.6

0.4

0.2

0.0
1
2
3
4
5

100
39
35
100
34

360
123
116
392
125

0
0
0
0
0

21
14
8
18
4

Years
Figure 2

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TRANSPLANTATION

Patient survival following intestinal transplantation

compared with HPN
HPN14e16
Intestinal
Transplantation (data from
international registry10)
Intestinal transplantation
(best reported large
cohort survival17)
C
All patients
C
Subgroup receiving
lymphocyte depletion

1 year
86e97%
75%

5 years
57e83%
58%

10 years
43e71%
40%

85%
91%

61%
70%

42%

Summary of main indications for intestinal transplantation in the UK

1. Life-threatening complications of PN
(a) Progressive liver disease (IFALD or non-IFALD)
C
Severe liver disease or progressive disease despite all remedial actions.
(b) Recurrent septic episodes
C
IF patients who have severe septic complications (i.e. lifethreatening line infection needing admission to ITU, or
recurrent yeast or candidal infections).
(c) Lack of central venous access
C
For isolated intestine: venous access limited to three major
sites.
C
For intestine as part of a cluster graft: venous access limited to
four major sites.
2. Very poor quality of life thought to be correctable by
transplantation.
3. Patients with indications for extensive surgery involving partial
or complete evisceration:

Table 1

should also be remembered that the comparison of survival on

HPN to that after transplantation is not equitable, as those
patients currently transplanted are often selected because they
have complications of HPN, and so are at greater risk of
complications even before transplantation.
As the survival gap between HPN and transplantation
decreases, the importance of improved quality of life increases.
Where there is little to choose between the two regarding
survival, patients whose quality of life can be enhanced by
transplantation should logically be given this opportunity. The
limited quality of life data published so far suggests that there can
be considerable improvements after transplantation.20e22
The current indications for intestinal transplantation11,23 are
constructed around the premise that survival is better on HPN,
quality of life can be improved by transplantation, and transplantation should be considered before patients lose the opportunity owing to progressive co-morbidity, in particular loss of
adequate venous access. These indications are being revised and
will be largely in line with those given in Table 2.

Adults
(a) Surgery to remove a large proportion of the abdominal viscera
that is considered untenable without associated multi-visceral
transplantation (e.g. extensive desmoid disease, extensive
severe mesenteric arterial disease requiring intervention).
(b) Localized malignancy considered to be amenable to curative
resection that would necessitate extensive evisceration (e.g.
localized neuroendocrine tumours and cholangiocarcinoma e
particular caution should be exercised with this group).
Children
(a) Surgery that will lead to:
C
Terminal gastrostomy
C
Terminal duodenostomy
C
Ultra short bowel: In children <10 cm, with or without ICV
C
Recurrent fluid and electrolyte management problems needing
frequent hospital admissions
4. Patients requiring transplantation of other abdominal organs
(a) Where the transplantation procedure is expected to preclude
the possibility of future intestinal transplantation (loss of
vulnerable and limited venous access, further HLA
sensitization).
(b) Where the risk is increased by excluding the intestine from the
graft (predictable problems related to administering immunosuppression (e.g. line sepsis), ongoing severe intestinal
disease such as diabetic visceral neuropathy, or ultra-short
bowel syndrome, causing fluid, electrolyte and acid-base
balance problems (damage to renal graft), and where the need
for subsequent intestinal transplantation is considered likely.

What does intestinal transplantation involve?

Patients referred for consideration who appear to be good candidates are formally assessed at one of the intestinal transplantation
centres. Currently, there are four centrally funded centres in the UK:
two adult centres, in Cambridge, (Addenbrookes Hospital, Cambridge University) and Oxford (Churchill Hospital, Oxford University); and two paediatric centres, in Birmingham (Birmingham
Childrens Hospital) and London (Kings College Hospital, London).
Assessment is usually conducted during an inpatient stay when
a comprehensive review of the patients physical and psychological
status is conducted. Co-morbidity, when discovered, is investigated
and resolved as far as possible. After formal assessment, adult
patients in the UK are presented to a national forum (national adult
intestinal transplantation forum e NASIT)24 at which their details
are considered by a multi-disciplinary group, including specialists
who are not from transplant centres. Expert opinion from the two
national intestinal failure centres (St Marks Hospital, Harrow,
London and the Royal Salford Hospital, Manchester) is available.
This forum is designed to provide a balanced view of the potential
benefit or otherwise of transplantation for each patient. If NASIT

MEDICINE 39:3

Table 2

approval is given, patients are listed and wait for around 6e12
months or longer if they have been sensitized to HLA-antigens.
The surgical procedure is often protracted and the recipient
procedure may extend over 16 h or more. The intestine is transplanted as an isolated graft or in combination with other organs as
a so-called cluster graft, but the majority fall into four categories:

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TRANSPLANTATION

 isolated intestine
 liver and intestine
 multivisceral (liver, intestine, stomach, pancreas)
 modified multi-visceral (intestine, stomach, pancreas).
In addition, patients may undergo renal transplantation and some
centres favour splenic transplantation for immunological reasons.
Patients invariably have an ileostomy, at least initially, to provide
access for ileoscopic surveillance biopsies to detect rejection. A
few centres transplant the large intestine and abdominal wall.
Following surgery it is usual for an ITU stay of 2 or 3 days,
then HDU for 2 or 3 weeks, and finally a less intensive ward stay
for a further 4e6 weeks to establish full enteral nutrition, satisfactory immunosuppression and resolution of any postoperative
problems such as infection.
Infection is the commonest postoperative complication (Table
3). Rejection is now less of a problem since the introduction of

lymphocyte-depleting agents, but early detection and treatment

remain a pivotal part of the process and surveillance biopsies via
the stoma are undertaken at least three times a week in the first
month. Fluid and electrolyte balance are also frequently challenging but of critical importance, to prevent the downward
spiral triggered by a confluence of salt and water imbalance,
impaired renal function and sepsis, which may result in multiorgan failure. At this point, other pre-existing co-morbidities and
the lack of venous access for treatments such as dialysis can
result in inexorable deterioration. The postoperative management of these patients is complex and requires a fully integrated
team of consultants from a broad range of specialties who are
well motivated and able to provide prompt consultant-led
expertise. The combination of inducing profound immunosuppression and transplanting an organ with very high antigenicity
that also contains a host of potential pathogens produces

Common infections following intestinal transplantation (in the UK)

Location
Bacterial Central line related
Superficial
surgical site:
Pneumonia
Abdominal collection/
peritonitis

Likely pathogens
Staphylococcus aureus
(incl. MRSA)
Escherichia coli
Klebsiella,
Pseudomonas.
Coagulase-negative
Staphylococci:
(IV line infections only)

Fungal

Aspergillus fumigatus

Aspergillosis:
Wound, pulmonary,
disseminated,
cerebral

Candidal Candidiasis:
oropharyngeal,
genitourinary,
wound related,
line infections.
Viral
CMV looks for colitis,
hepatitis and retinitis.
EBV PTLD late:
>1 year

Candida albicans

Influenza virus
Respiratory syncytial
virus (RSV) or
parainfluenza
virus 3
Cytomegalovirus (CMV)
Varicella-zoster virus
(VZV)
Herpes simplex virus 1
or 2 (HSV-1/2)
EpsteinBarr virus (EBV)
Human herpes virus 6
(HHV-6)
Adenovirus

Clinica l features
Brisk deterioration/septic
shock/and organ-specific
features
(respiratory, urinary,
intra-abdominal)
Lower-grade sepsis with
coagulase-negative
Staphylococci
Cause of death in 18%
Antibiotic-resistant
pneumonia
Aspergillosis is serious,
particularly disseminated,
and intra-cerebral
is usually fatal
Antibiotic-resistant
sepsis

Diagnosis
Blood cultures/pneumococcal/
Legionella urinary antigens
Organ-specific: bronchoalveolar lavage (BAL);
sputum, urine culture, etc.
Intra-abdominal scans

Treatment
Initially broad-spectrum
antibiotics then adjust
to include sensitivities
of known organisms.
Need to cover, MRSA
and other potential
hospital-acquired
infections

Chest CT scan
BAL and trans-bronchial
biopsy PCR

Aspergillosis with
amphotericin/
AmBisome, voriconazole
or caspofungin

Blood and urine culture,

line tip culture.

Flu-like illness
Pneumonia

Nose and throat swabs,

nasopharyngeal aspirate,
broncho-pulmonary
lavage PCR

AmBisome/
caspofungin
Fluconazole if
mild/known to be
sensitive.
Antivirals, depending
on circulating strains
Nebulized ribavirin

Organ disease
Severe chicken pox or
zoster, pneumonitis
Systemic infection,
organ disease
From glandular fever
to PTLD
Systemic infection,
fever
Systemic infection,
organ disease

Ganciclovir
Acyclovir
Acyclovir
Discuss with virologist
and haematologist
Discuss with virologist
Cidofovir (discuss with
virologist)

Table 3

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a unique clinical setting, where patients often respond in an

unusual way to infections and treatments.

a high enough volume of these complex patients to build up a high

level of corporate experience. This system is very efficient as it
allows appropriate escalation and concentrates experience of the
less frequent, highly complex patients, who require a very
rounded team of clinicians to manage them effectively. In most
cases, patients fulfilling the criteria for transplantation (Table 2) or
who are approaching this situation (Table 4) should be referred.
Particular attention should be given to those who are likely to miss
the window of opportunity. These patients often have progressive
disease, which may advance to a point that contraindicates
transplantation or results in death whilst they are on the waiting
list. Examples of this include patients who are rapidly losing
venous access points and those bleeding from portal hypertension.
Special consideration should also be given to PN-dependent
patients who require transplantation of other organs. They may
benefit from a cluster graft including intestine rather than have
a subsequent intestinal transplantation in the setting of an existing
graft and consequent immunosuppression.

Which patients should be referred to a transplant centre for

consideration?
The management of all patients with intestinal failure should now
include consideration of the potential role of transplantation. It is
important to make every attempt to treat reversible disease and
thorough intestinal rehabilitation can often restore adequate
enteral nutrition. In the UK, this process is undertaken in regional
or national intestinal failure (IF) centres. The regional (mediumvolume) centres have a nutrition team and clinical staff with
subspecialty interests in the management of intestinal failure
patients. For the more complex patients, especially where multiple
surgical procedures are thought necessary, the UK has two
national IF centres. These centres have specialist medical and
surgical staff that are dedicated to intestinal failure work and have

Red-flag indicators for referral for transplant assessment

[In addition to the standard indications for transplantation e Table 2]
Patients with intestinal failure and one or more of the following:
C
Abnormal LFTs
Persistent elevation of hepatic enzymes may
indicate PN-associated hepatic fibrosis or
cirrhosis
C

Frequent line sepsis

Patients with three or more episodes of line

sepsis in a year or one episode of lifethreatening sepsis may be candidates for
transplantation particularly if there are other
relative indications

Refer to/discuss with national IF centre

Ultra-short bowel syndrome

Less than 40 cm of jejunum to a stoma is

associated with rapid-onset liver disease

Refer to/discuss with a National IF or

transplant centre

Co-existing diabetes mellitus with

complication

Diabetic complications are often indications

for pancreatic transplantation and if advanced
increase the risk associated with intestinal
transplantation. Patients may benefit from
early combined transplantation

Refer to transplantation centre for

consideration of combined pancreas and small
bowel transplantation

Pseudo-obstruction. Complicated by
severe abdominal pain

Patients with intractable abdominal pain from

distended small and large intestine may
benefit from transplantation rather than
colectomy and enterectomy and PN. They are
a relatively high-risk group for PN and removal
of intestines reduces intra-peritoneal space for
subsequent transplantation

Refer patient to transplant centre

Extensive disease threatening or damaging

other important structures. Early surgical
intervention may be preferable

Refer to transplantation centre for assessment

or to the national desmoid centrea

Extensive mesenteric arterial or venous

disease involving intestine and other essential
intra-abdominal organs

Refer to transplantation centre for assessment

or to the national desmoid centre

Patients without intestinal failure

C
Desmoid disease

Assessment of liver including biopsy, optimize

HPN and exclude other causes. Refer to or
discuss with national IF or transplant centre

Mesenteric vascular disease

The UK National Desmoid Centre is at St Marks hospital, Harrow, London.

Table 4

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What is the likely future demand for intestinal transplantation?

Advice for management of sick intestinal transplantation patient admitted to a non-transplantation

hospital

The ongoing improvement in postoperative survival brings with it

broadening of the indications for transplantation to include larger
numbers of patients. The point prevalences of adult patients
receiving HPN in the UK in 2007 and 2008 were 867 and 856
respectively, with estimated paediatric prevalences of 28 and 128
respectively. In the corresponding years, the incidences of adult
HPN patients were 138 and 157 respectively and for paediatrics,
nine and eight respectively. The majority of adult patients are aged
<60 years and approximately 35% are <40 years.25 Many of these
patients will be candidates for transplantation once the indications
become less stringent. Another factor that will eventually affect
demand significantly is the unmet requirement for salvage surgery
after catastrophic intestinal events, such as acute ischaemia.26 For
many patients the required expertise for salvage procedures is not
available. Improvements in this service will undoubtedly increase
the number of potential candidates for transplantation. Another
important factor is the relative costs of HPN versus transplantation. Although the one-off cost of the transplant procedure is
high, subsequent cost of immunosuppression are modest in
comparison with the year-on-year costs of HPN. The break-even
point, after which savings can be expected from transplantation
compared to HPN, can be approximated as 3 years.

1. Contact the appropriate transplant centre without delay for

advice and possible transfer.
2. Undertake a full infection screen, including culture (and
microscopy) of blood, urine, sputum stoma effluent/stool,
CMVePCR, CXR, AXR (CT scan abdomen and chest as required).
3. If infection is suspected (usual) commence broad-spectrum
antimicrobial therapy without delay. This usually includes:
meropenem, vancomycin, AmBisome, ganciclovir. If there is
evidence of pulmonary infection, consider high-dose
co-trimoxazole, which is active against Pneumocystis jirovecii.
Advice should be sought from the transplant centre.
4. Be aware of the possibility of tacrolimus nephrotoxicity and
neutropenia associated with valgancyclovir and co-trimoxazole
(patients may already be taking these).
5. Fluid balance: patients will be prone to salt and water depletion. They should be aware of their normal body weight, assess
sodium and water balance with spot urinary sodium and
osmolarity respectively (urine dip stick for specific gravity is
a helpful initial guide).
6. Graft rejection is difficult to diagnose so patients should be
transferred to an appropriate transplantation centre as soon as
possible.

Why do gastroenterologists need to know about intestinal

transplantation?
Transplantation will become an increasing part of gastroenterological practice as more patients are transplanted and require
follow-up at a local level in collaboration with the main centres.
Within the next 10 years, it is likely that intestinal transplantation
will become an integral part of most GI speciality registrar training,
in a similar manner to liver transplantation in hepatological
training today. At present, the most likely interaction with a local
centre will be an urgent admission of a sick transplant patient
(Table 5). It should be remembered that these patients are often
heavily immunosuppressed. They will often have had recent
corticosteroid treatment as part of initial immunosuppression
induction therapy and will usually have been given lymphocytedepleting antibodies i.e. alemtuzumab (Campath-1H), antilymphocyte globulin (Orthoclone OK-T3) or lymphocyte-blocking
(anti-interleukin 2 receptor) monoclonal antibodies (i.e. daclizumab). Following induction therapy, patients are given maintenance therapy, most commonly tacrolimus or sirolimus, either
alone or in combination with mycophenolate mofetil.
Gastroenterologists also need to consider the potential role of
transplantation in the future management of patients. This not
only applies to those with intestinal failure but also with other
morbidities that may require extensive evisceration and necessitate multi-visceral transplantation, such as abdominal desmoid
disease. In both cases, it is critical to refer patients at a stage
when the option of transplantation has not slipped away. It
should be appreciated that patients need to be physically and
mentally robust to withstand transplantation. Leaving referral
until there are few or no large venous access sites, or until
patients are bleeding as a result of portal hypertension, will often
mean that it is too late to offer them a reasonable chance of
surviving transplantation and many will die before organs
become available. As patients become more aware of the option

MEDICINE 39:3

Table 5

of transplantation, there will be an expectation from them to be

given this opportunity at an appropriate stage.
There are certain red flag indicators for referral to a main
centre (Table 4) in addition to the standard indications for transplantation (Table 2). This is not an exhaustive list of high-risk
factors but provides a guide to the type of situation that should
prompt the gastroenterologist to consider referral, to either
a national IF centre or a transplant centre, for further consideration.

Conclusion
Considerable advances over the last 20 years have taken intestinal transplantation from the first procedures that provided only
short-term success to its current status as a routine therapeutic
option for selected patients. Although HPN remains the primary
treatment for most patients with intestinal failure, we approach
the threshold of a new era when intestinal transplantation will be
considered to be the primary treatment for most patients. This
promises to be cost effective and bring with it better quality of life
for patients without reducing their longevity. A key element of
success is appropriate timing of referral to a national IF or
transplantation centre. All gastroenterologists should be aware of
when and how to refer patients, and seek advice early in the
management of the more complex patients.
A

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MEDICINE 39:3

19 Gupte GL, Beath SV, Protheroe S, et al. Improved outcome of referrals

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Practice points
C

189

The possibility of future intestinal transplantation should be

considered in the management of all intestinal failure (IF)
patients and those with extensive benign intra-abdominal
disease.
IF patients with significant complications of PN should be
referred for transplantation assessment (National IF or transplantation centre) or at least discussed with a centre.
Care should be taken not to allow IF patients to deteriorate
past the point when transplantation is possible.
Sick transplant patients must be treated without delay and
advice should be sought from their transplantation centre
immediately on presentation.
The early use of appropriate broad-spectrum antimicrobial
agents in sick transplantation patients is essential as they are
most likely to have infection.

2010 Elsevier Ltd. All rights reserved.