Copyright 2012 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.

Intestinal Rehabilitation and Bowel

Reconstructive Surgery: Improved

Outcomes in Children With Short

Bowel Syndrome?

T

o the Editor:

Few readers are likely to disagree with the main

conclusions drawn by Khalil et al (1) that ‘‘with a multi-

disciplinary approach, combining both medical and surgical
expertise, patients with short bowel syndrome can achieve enteral
autonomy,’’ and ‘‘patients with short bowel syndrome should be
treated in specialist units.’’ Their claim of improved outcomes, with
78% of patients achieving enteral autonomy, also may be true
given the previously reported 45% survival (2); however, crucial
unanswered questions include ‘‘what are the indications for longi-
tudinal intestinal lengthening?’’ (can it be justified, for example, in
the patient cited with 140 cm of small bowel presurgery?) and
‘‘does the initial ‘bowel expansion’ described actually produce
an increase in absorptive surface area over and above that known to
occur as part of the adaptive process?’’ (3).

The widely recognised immense heterogeneity of patients

with short bowel syndrome (eg, gut length, type of gut remaining,
presence of an ileocaecal valve, gut dilatation/dysmotility, primary
pathology, small numbers, different surgeons) is one set of reasons
why these patients will never be studied in randomised trials.
The other important confounding variable, and one that is key in
the context of the article by Khalil et al, is the natural history of
short bowel syndrome, which is one of the spontaneous improve-
ment in gut function on the basis of intestinal adaptation.
Consequently, the majority of patients with short bowel syndrome
will come off parenteral nutrition and will not need any recon-
structive surgery. Against this background, it becomes extremely
difficult to assess with confidence whether a reconstructive surgical
intervention has helped; most patients are getting better anyway.

One reasonable way around this problem is to carry out

before-and-after studies of feed tolerance, with surgery taking
place at a time when each patient’s adaptive process has clearly
come to an end. This can be judged by an inability to advance
enteral feeds of any description without producing intolerance as
diarrhoea and/or vomiting, notwithstanding intensive medical and
dietetic input often involving the use of modular feeds. The
publication by Khalil et al (1) is notably devoid of relevant details
in these respects, and the absence of a gastroenterologist among the
authors is surprising given their endorsement of multidisciplinary
management.

Such before-and-after studies clearly lack the rigour of

a randomised trial but have been useful in providing some evidence
of the effectiveness of interventions in this patient group (4,5).
Unfortunately, this publication, in common with all those from
the same group, fails to provide even this degree of evidence of
effectiveness and cannot be considered as being supportive of
the uncritical widespread use of reconstructive surgery, even in
specialist centres. A retrospective case note review describing how
one team manages a particular clinical problem may, even in these
days of evidence-based medicine, hold some interest and stimulate
discussion, but the study as it stands simply cannot answer such
questions as ‘‘is one approach better than another?’’ or serve as the
basis for a change in service provision.

John Puntis and

y

Ian Booth

General Infirmary at Leeds, Leeds, UK

y

Birmingham Children’s Hospital, Birmingham, UK

REFERENCES

1. Khalil BA, Ba’ath ME, Aziz A, et al. Intestinal rehabilitation and bowel

reconstructive surgery: improved outcomes in children with short bowel
syndrome. J Pediatr Gastroenterol Nutr 2012;54:505–10.

2. Bianchi A. Experience with longitudinal lengthening and tailoring. Eur J

Pediatr Surg 1999;9:256–9.

3. Weale AR, Edwards AG, Bailey M, et al. Intestinal adaptation after

massive intestinal resection. Postgrad Med J 2005;81:178–84.

4. Duggan C, Piper H, Javid PJ, et al. Growth and nutritional status in

infants with short-bowel syndrome after the serial transverse enteroplasty
procedure. Clin Gastroenterol Hepatol 2006;4:1237–41.

5. Simkiss D, Adams I, Myrdal U, et al. Erythromycin in severe

post-operative intestinal dysmotility in the neonate. Arch Dis Child
1994;71:F128–9.

Authors’ Response

T

o the Editor

: Our results show an overall survival of 92%,

with 91% achieving enteral autonomy off total parenteral

nutrition in patients under follow-up. Drs Puntis and Booth rightly
pointed out the child with 140 cm of bowel and questioned the
justification of lengthening. As our article clearly showed, this child
had a longitudinal intestinal lengthening and tailoring. This child
had a distended bowel, which was dysmotile, and the procedure
was done mainly to achieve tailoring and improve motility (which
it did). This child was operated on early in the series. Again as
mentioned in our article, we used the STEP procedure as a tailoring
procedure. If we were to be faced with a similar child now,
we would use the STEP procedure to achieve tailoring because
it is easier and faster and length is not the issue. It is important to
note that many cases of ‘‘irreversible intestinal failure’’ caused by
short bowel are really dilated dysmotile bowel, which improves
when the correct surgical technique is used. Unfortunately, some
of these children end up on transplant units. As for the bowel
expansion procedure, we published an article on our experience
with this technique and we encourage Drs Puntis and Booth to
read it (1). We completely agree with them that under the present
circumstances, a randomised controlled trial is inappropriate;
however, we believe that success in short bowel syndrome
should not be confined to survival alone. Our article shows a
relatively fast weaning off parenteral nutrition in children who
have undergone reconstructive surgery in the context of an intestinal
rehabilitation programme. This is extremely important in assessing
the outcomes of management strategies. We are unaware of results
comparing similar groups of patients managed solely via the medical
route. Children should not be allowed to deteriorate to the stage where
bowel reconstructive surgery is ‘‘a last resort,’’ especially when
the critical window of maximal adaptation has elapsed. It is the policy
of our unit that patients are carefully assessed on an individual basis
with the key principles discussed in the article in mind. Patients
should not be left to ‘‘mere chance’’ as to whether they adapt fully,
but every form of expertise (both medical and surgical) should be
used in a timely fashion and in units with considerable experience and
good outcomes. Thus, this is another reason to refer these patients
to such units. When it comes to assessment of the child before
and after, we agree with the authors that such information is vital.
This should not only be with regard to bowel habits but indeed to
the whole care of the child. As such, we were the first team to produce
a caregiver evaluation of our management strategy. We refer the
authors to our report on this subject (2). Overall, we believe that these

L

ETTERS TO THE

E

DITOR

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Volume 54, Number 4, April 2012

Copyright 2012 by ESPGHAN and NASPGHAN. Unauthorized reproduction of this article is prohibited.

patients are complex and heterogeneous and are happy that the
authors agree that a multidisciplinary approach should be used. This
approach should include both medical and surgical expertise.

Basem A. Khalil

Antonino Morabito

Department of Paediatric Surgery, Royal Manchester Children’s

Hospital, Manchester, UK.

REFERENCES

1. Murphy F, Khalil BA, Gozzini S, et al. Controlled tissue expansion in

the initial management of the short bowel state. World J Surg 2011;
35:1142–5.

2. Edge H, Hurrell R, Bianchi A, et al. Caregiver evaluation and satisfaction

with autologous bowel reconstruction in children with short bowel
syndrome. J Pediatr Gastroenterol Nutr 2011 [e-pub ahead of print].

E

RRATA

Nutritional Strategy for Adolescents Undergoing Bariatric Surgery: Report of a

Working Group of the Nutrition Committee of NASPGHAN/NACHRI: Erratum

I

n the article that appeared on 125 of the January 2011 issue, the article type was given as ‘‘Clinical Guideline.’’ The article type is
‘‘Clinical Report.’’

REFERENCE

1.

Fullmer MA, Abrams SH, Hrovat K, et al. Nutritional Strategy for Adolescents Undergoing Bariatric Surgery: Report of a Working Group of the Nutrition
Committee of NASPGHAN/NACHRI. J Pediatr Gastroenterol Nutr 2011;52:125–35.

Skeletal Health of Children and Adolescents With Inflammatory Bowel

Disease: Erratum

I

n the article that appeared on page 11 of the July 2011 issue, the article type was given as ‘‘Clinical Guideline.’’ The article type is
‘‘Clinical Report.’’

REFERENCE

1. Pappa H, Thayu M, Sylvester F, et al. Skeletal Health of Children and Adolescents With Inflammatory Bowel Disease. J Pediatr Gastroenterol Nutr

2011;53:11–25.

Human Milk Probiotic Lactobacillus fermentum CECT5716 Reduces

the Incidence of Gastrointestinal and Upper Respiratory Tract Infections in

Infants: Erratum

I

n the article that appeared on page 55 of the January 2012 issue, the clinical trial registration number was provided as NCT012156156. The
correct number is NCT01215656.

REFERENCE

1. Maldonado J, Can˜abate F, Sempere L, et al. Human Milk Probiotic Lactobacillus fermentum CECT5716 Reduces the Incidence of Gastrointestinal and

Upper Respiratory Tract Infections in Infants. J Pediatr Gastroenterol Nutr 2012;54:55–61.

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European Society for Pediatric Gastroenterology, Hepatology, and Nutrition

Guidelines for the Diagnosis of Coeliac Disease: Erratum

I

n the article that appeared on page 136 of the January 2012 issue, a number of errors are noted, as follows:



Page 138, paragraph 4, the sentence should read: When duodenal biopsies, taken during routine diagnostic workup for gastrointestinal
symptoms, disclose a histological pattern indicative of CD (Marsh 1–3 lesions), antibody determinations and HLA typing should
be performed.



Page 139, last paragraph, the sentence should read: In 2008, the UK National Institute for Health and Clinical Evidence (NICE)
published guidelines for the diagnosis and management of CD in general practice (78a).



Page 140, under ‘‘Symptoms and Signs,’’ the sentence should read: Gastrointestinal symptoms frequently appear in clinically
diagnosed childhood CD, including diarrhoea in about 50% of patients (15,16).



Page 144, Table 3, the second sentence in the footnote should read: Data also from Richtlijn Coeliakie en Dermatitis Herpetiformis.
Kwaliteitsinstituut voor de Gesondheidszorg CBO (33a).



Page 144, line 10, the sentence should read:The sensitivity of HLA-DQ2 is high (median 91%; p25 – p7586.3%– 94.0%), and if
combined with HLA-DQ8 (at least 1 is positive), it is even higher (median 96.2%; p25 – p75 94.6%–99.8%), making extremely small
the chance of an individual who is negative for DQ2 and DQ8 to have CD; even though the small percentage of HLA-DQ2-negative and
HLA-DQ8-negative patients is well documented (33–35).



Page 144, Table 4, the second sentence in the footnote should read: Data also from Richtlijn Coeliakie en Dermatitis Herpetiformis.
Kwaliteitsinstituut voor de Gesondheidszorg CBO (33a).



Page 146, paragraph 6, the penultimate line should read: Anti-TG2 antibodies also can be detected in saliva. Sufficient sensitivity and
specificity was not achieved with conventional commercially available immunoassays (63), although the use of radiobinding assays
appeared to be more favourable (64).



Page 146, paragraph 8, the first sentence should read: The positivity for anti-TG2 and/or EMA is associated with a high probability for
CD in children and adolescents (10,52); however, low levels of anti-TG2 have been described in a number of conditions unrelated to
CD, such as other autoimmune diseases, infections, tumours, myocardial damage, liver disorders, and psoriasis (62,68 – 70).



Page 147, statement 3.3.5, the second sentence should read: For other tests, values considered to be high antibody positivity should be
established by comparison with a panel of tests, which are listed in Appendix I.



Page 147, statement 3.3.8, the first sentence should read: High concentrations of anti-TG2 antibodies in blood (as defined in statement
3.3.5) predict villous atrophy better than low positive or borderline values.



Page 149, statement 3.4.10, the voting results should read: Total number of votes: 13, Agree: 12, Disagree: 1, Abstentions: 0



Page 159, reference 78a should read: National Institute for Health and Clinical Excellence. CG86 coeliac disease: full guideline. NICE
guidelines. http://guidance.nice.org.uk/CG86/NICEGuidance/pdf/English. Accessed August 31, 2011.

Figures 1 and 2 are replaced as follows:

Child/Adolescent with symptoms suggestive of CD

Anti-TG2 & total IgA*

Anti-TG2
positive

Not CD

Transfer to paediatric gastroenterologist
paed. GI discusses with family the 2 diagnostic pathways and
consequences considering patient’s history & anti-TG2 titers

Consider further diagnostic testing if:
IgA deficient
Age: < 2 years
History: - low gluten intake
- drug pretreatment
- severe symptoms
- associated diseases

Positive Anti-TG2

>10 x normal

EMA & HLA testing for DQ2/DQ8

EMA pos.
HLA pos.

Not

available

OEGD & biopsies

1 x bulbus & 4 x pars descendens

Anti-TG2
negative

EMA pos.

HLA neg.

EMA neg.
HLA neg.

EMA neg.

HLA pos.

Marsh 0-1

Marsh 2 or 3

Consider false
neg. HLA test
Consider biopsies

Unclear case

Consider:

false pos. serology

false neg. biopsy or

potential CD

Extended evaluation of

HLA/serology/biopsies

Consider false
pos. Anti-TG2

CD+

GFD

& F/u

CD+

GFD
& F/u

*or specific IgG based tests

Positive Anti-TG2

<10 x normal

FIGURE 1. Symptomatic patient. CD ¼ coeliac disease; EMA ¼ endomysial antibodies; F/u ¼ follow-up; GFD ¼ gluten-free diet;
HLA ¼ human leukocyte antigen; IgA ¼ immunoglobulin A; IgG ¼ immunoglobulin G; OEGD ¼ oesophagogastroduodenoscopy;
TG2 ¼ transglutaminase type 2.

Errata

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REFERENCE

1.

Husby S, Koletzko S, Korponay-Szabo´ IR, et al. European Society for Pediatric Gastroenterology, Hepatology, and Nutrition Guidelines for the Diagnosis
of Coeliac Disease. J Pediatr Gastroenterol Nutr 2012;54:136–60.

Use of Enteral Nutrition for the Control of Intestinal Inflammation in Pediatric

Crohn Disease: Erratum

I

n the article that appeared on page 298 of the February 2012 issue, the article type was given as ‘‘Clinical Guideline.’’ The article type is
‘‘Clinical Report.’’

REFERENCE

1. Critch J, Day AS, Otley A, et al. Use of Enteral Nutrition for the Control of Intestinal Inflammation in Pediatric Crohn Disease. J Pediatr Gastroenterol Nutr

2012;54:298–305.

Asymptomatic person at genetic risk for CD

Explain implication of positive test result(s) and get consent for testing

HLA DQ testing (+/-Anti-TG2)

HLA positive

for

DQ2 and/or DQ8

Not CD,

no risk for CD

Anti-TG2 & total IgA*

Consider retesting in intervals or
if symptomatic

EMA

Marsh 0-1

Marsh 2 or 3

*or specific IgG based tests

HLA negative

for

DQ2 and DQ8

Positive Anti-TG2

< 3x normal

Anti-TG2 negative

Not CD

EMA positive

EMA negative

OEGD & biopsies:

1 x bulbus & 4 x pars

descendens, proper

histological work up

CD+

GFD
& F/u

Unclear case

F/u on normal diet

Consider: false pos.

serology, false neg.

biopsy or potential CD

Consider: age, false neg. results,
exclude IgA deficiency and history
of low gluten intake or drugs

Positive Anti-TG2

>3x normal

Consider:

transient/false pos.

anti-TG2

F/u on normal diet with

further serological testing

FIGURE 2. Asymptomatic patient. See Fig. 1 for definitions.

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