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Oona Nieminen, MD, *Maria Hukkinen, MD, PhD, †Reetta Kivisaari, MD, PhD,
*
*
Annika Mutanen, MD, PhD, ‡Laura Merras-Salmio, MD, PhD, and *§Mikko P. Pakarinen, MD, PhD
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ABSTRACT
Objectives: Although excessive intestinal dilatation associates with wors- What Is Known
ened outcomes in pediatric short bowel syndrome (SBS), little is known
about the natural history and definition of pathological dilatation. We • In short bowel syndrome (SBS) remaining bowel
addressed fore-, mid-, and hind-gut dilatation in children with SBS, who undergoes structural changes.
had not undergone autologous intestinal reconstructive (AIR) surgery, in • Dilatation of remaining intestine associates with
relation to controls. prolonged parenteral nutrition (PN) dependence.
Methods: SBS children without history of AIR surgery (n = 59) and age- • Remaining small intestinal length is the major deter-
matched controls without any disclosed intestinal pathology (n = 140) were minant of enteral autonomy.
included. Maximum diameter of duodenum, small bowel (SB), and colon
were measured in each intestinal contrast series during 2002 to 2020 and
What Is New
expressed as diameter ratio (DR) to L5 vertebrae height. Predictive ability
of DR for weaning off parenteral nutrition (PN) was analyzed with Cox
proportional hazards regression models using multiple cutoffs. • All segments of remaining bowel dilate to abnormal
Results: Duodenum (DDR), SB (SBDR), and colon (CDR) DR were 53%, levels in children with SBS.
183%, and 23% higher in SBS patients compared to controls (P < 0.01 for • The degree of duodenal and small bowel dilatation
all). The maximal DDR and SBDR measured during follow-up is associated
is greatest in young PN dependent patients with
with current PN dependence and young age. DDR correlated with SBDR
SBS.
(r = 0.586, P < 0.01). Patients with maximal DDR less than 1.5, which was
• Duodenal diameter ratio to fifth lumbar verte-
also the 99th percentile for controls, were 2.5-fold more likely to wean off
bra height >1.5 strongly predicts prolonged PN
PN (P = 0.005), whereas SBDR and CDR were not predictive for PN dura-
dependence
tion.
Conclusions: All segments of remaining bowel, especially SB, dilate above
normal levels in children with SBS. In SBS children without AIR surgery, remaining bowel undergoes structural changes to compensate the
PN dependence and young age is associated with duodenal and small intes- loss of absorptive surface, including increase in width and length
tinal dilatation, while duodenal dilatation also predicted prolonged PN. (4–9). Anatomical factors improving the likelihood of weaning off
PN include remaining small bowel (SB) length over 40–50 cm,
Key Words: diameter ratio, enteral autonomy, intestinal failure intact ileocecal valve (ICV), and preserved colon (5,6,10–12). In
children with SBS, excessive bowel dilatation associates with pro-
(JPGN 2023;77: 720–725) longed PN dependence and worsened outcomes (9). It is thought
bowel dilatation impairs motility and promotes bacterial over-
I
growth (BO), predisposing to bowel derived bloodstream infections
ntestinal failure (IF) is defined as reduced intestinal capacity and IF-associated liver disease (13–15). Symptomatic bowel dilata-
for absorption, requiring long-term parenteral nutrition (PN) to tion is commonly treated with autologous intestinal reconstructive
maintain sufficient nutrition and growth (1,2). Short bowel syn- (AIR) surgery, designed to reduce harmful dilatation while simul-
drome (SBS) due to extensive bowel resection is the most common taneously increasing SB length and thereby improving bowel func-
reason for IF (3). Children with SBS possess significant adaptive tion and outcomes (5,12,15,16). However, correct patient selection
capacity to bowel resection, and they have better chances of reach- for AIR surgery remains challenging as cutoff for abnormal harm-
ing enteral autonomy compared to adults (4). After resection, the ful bowel dilatation remains unclear (17).
Received April 21, 2023; accepted August 26, 2023. Sources of Funding: This study was supported by research grants from the
From the *Department of Pediatric Surgery, Pediatric Liver and Gut Sigrid Jusélius Foundation (MPP), the Finnish Pediatric Research Foun-
Research Group, Pediatric Research Center, Helsinki University Hos- dation (MPP), and Helsinki University Hospital Fund (MPP).
pital and University of Helsinki, Helsinki, Finland, the †Department of The authors report no conflicts of interest.
Pediatric Radiology, Medical Imaging Center, Helsinki University Hos- Supplemental digital content is available for this article. Direct URL cita-
pital and University of Helsinki, Helsinki, Finland, the ‡Department of tions appear in the printed text, and links to the digital files are provided
Pediatric Gastroenterology, Helsinki University Hospital and University in the HTML text of this article on the journal’s Web site (www.jpgn.
of Helsinki, Helsinki, Finland, and the §Department of Women’s and org).
Children’s Health, Karolinska Institute, Stockholm, Sweden. Copyright © 2023 by European Society for European Society for Pediatric
Address correspondence and reprint requests to Oona Nieminen, MD, Gastroenterology, Hepatology, and Nutrition and North American Soci-
Helsinki University Hospital, New Children’s Hospital, PO BOX 281, ety for Pediatric Gastroenterology, Hepatology, and Nutrition.
00029 Helsinki, Finland (e-mail: oona.nieminen@fimnet.fi). DOI: 10.1097/MPG.0000000000003934
Our previous study showed SB diameter more than twice vertebra, when the bowel segment and vertebra height were clearly
of lumbar vertebrae height associated with reduced probability of visible to record accurately (15). Caecum and sigma were excluded
weaning off PN and survival (9,18). However, that study included as points of diameter measurements for colon. DR was calculated
patients who had undergone AIR surgery without normal controls, for duodenum (DDR), SB (SBDR), and colon (CDR) by dividing
and addressed only SB dilatation, while significance of duodenal the absolute maximum diameter of each intestinal segment by the
and colonic dilatation remains unclear (18). Here, by analyzing 5th lumbar vertebra height. For each patient, both first and greatest
duodenum, SB, and colon dilatation in relation to normal con- (maximal) DR for duodenum, SB, and colon during follow-up were
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trols while excluding patients who had undergone AIR surgery, we analyzed.
aimed to address natural history and define cutoffs for abnormal
bowel dilatation in pediatric SBS. Statistical Methods
Continuous data are expressed as median values and IQRs.
Categorical data are expressed as frequencies. Spearman rank
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Nieminen et al JPGN • Volume 77, Number 6, December 2023
TABLE 1. Patient characteristics the time of contrast series, whereas first CDR correlated weakly
Number of patients 59 positively with age (r = 0.332, P = 0.04) (Figure 1, Supplemental
Number of contrast series/patient, median (IQR) 2 (2–4) Digital Content 1, http://links.lww.com/MPG/D301). Accordingly,
maximal DDR (r = −0.674, P < 0.01) and SBDR (r = −0.579, P <
Male gender, n (%) 33 (56%)
0.01) correlated negatively with age, while maximal CDR showed
Underlying diagnosis, n (%) no correlation with age (r = 0.213, P = 0.19) (Figure 2, Supplemen-
Necrotizing enterocolitis 31 (53%) tal Digital Content 2, http://links.lww.com/MPG/D302).
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Other (meconium peritonitis) 1 (1.7%) the only variable related with maximal DDR while both PN depen-
dence and NEC diagnosis were associated with maximal SBDR.
Gestational age, wk 31 (25–36)
Only small bowel atresia diagnosis is associated with maximal
Birth weight, g 1440 (743–2575) CDR (Table 2). In regression models for factors associated with
Enterostomy, n (%) 6 (10%) first DDR, SBDR, and CDR, young age, treatment before the year
Ileocecal valve preserved, n (%) 24 (40%) 2009, gestational age, birth weight, and PN dependence were asso-
ciated with SBDR (Table 1, Supplemental Digital Content 4, http://
SB length, cm 50 (30–83) links.lww.com/MPG/D304).
SB length, % of normal 33 (19–48)
Colon length, % of normal 100 (53–100) Cutoffs for Abnormal Dilatation
Duration of parenteral nutrition, mo 8.4 (3.9–15) According to 99th percentiles of control group, normal
DDR, SBDR, and CDR (cutoff 1) was 1.5, 2.1, and 3.8, respectively
Age at the latest recorded follow-up, y 5.7 (1.7–9.3) (Fig. 1). Based on AUROC analyses, optimal maximal DR cutoffs
Deceased, n (%) 4 (6.9%) for being off PN at the time of contrast series (cutoff 2) were 1.5
IQR = interquartile range; SB = small bowel. for DDR, 3.0 for SBDR, and 2.6 for CDR (Figure 3, Supplemental
Digital Content 3, http://links.lww.com/MPG/D303). When analyz-
ing similarly the first available contrast series for each patient, opti-
mal DR cutoffs (cutoff 3) were 1.4 for DDR, 1.3 for SBDR, and 2.5
for CDR (Figure 3, Supplemental Digital Content 3, http://links.
lww.com/MPG/D303).
DISCUSSION
FIGURE 1. A box plot displaying diameter ratio for duodenum, Treatment of children with SBS aims at reaching enteral
small bowel, and colon in SBS patients and intestine healthy autonomy to decrease PN-related morbidity and mortality (20,22).
controls. Outliers presented as dots. Solid horizontal line represents We found that SBS patients have abnormally dilatated duodenum,
99th percentile of control group DR (cutoff 1). Dashed horizontal SB and colon compared to intestine healthy controls, with the
line represents cutoff 2 defined as maximum sum of sensitivity greatest dilatation seen in the remaining SB. In our patients, pre-
and specificity in AUROC model assessing the predictive value of dictors for weaning off PN not only included remaining SB length
maximal DR for PN dependence. AUROC = areas under receiving and presence of ICV, but also duodenum DR below 1.5. Our mul-
operating characteristic curves; DR = diameter ratio; PN = paren- tiple cutoff determination methods suggested DDR exceeding 1.5
teral nutrition; SBS = short bowel syndrome; denotes abnormal dilatation while estimated cutoffs for SBDR and
CDR showed more variability.
The use of contrast series to measure bowel length and
Duodenal and Small Intestinal Dilatation width has been previously shown to correlate well with intraopera-
Associated with PN and Young Age tive measurements (23). We have previously shown that standard-
Among SBS patients, first DDR (r = −0.480, P < 0.01) and ization of bowel width to lumbar vertebra height, which aims to
SBDR (r = −0.624, P < 0.01) correlated negatively with age at standardize intestinal width to the physical size of patients, more
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TABLE 2. Maximal duodenum, small bowel, and colon diameter ratio in relation to different variables assessed with simple linear regression and multiple regression adjusted for
variables found significant in simple linear regression
Duodenum Small bowel Colon
www.jpgn.org
Simple regression Multiple regression Simple regression Multiple regression Simple regression
β (95% CI) P value β (95% CI) P value β (95% CI) P value β (95% CI) P value β (95% CI) P value
Age at contrast series −0.05 (−0.10 to 0.0) 0.036 −0.03 (−0.08 0.184 −0.10 (−0.19 to −0.02) 0.020 −0.02 (−0.11 0.693 0.01 (−0.07 to 0.08) 0.800
to 0.02) to 0.08)
Treatment before 0.04 (−0.46 to 0.54) 0.900 1.10 (0.26 to 2.00) 0.011 0.78 (−0.07 0.071 −0.26 (−0.92 to 0.39) 0.400
year 2009 to 1.67)
Gender 0.15 (−0.26 to 0.56) 0.500 0.11 (−0.60 to 0.82) 0.800 −0.05 (−0.57 to 0.48) 0.900
ICV 0.37 (−0.03 to 0.78) 0.067 −0.11 (−0.83 to 0.60) 0.800 −0.30 (−0.83 to 0.23) 0.300
SBA vs other 0.37 (−0.22 to 0.97) 0.200 0.45 (−0.57 to 1.50) 0.400 −0.78 (−1.40 to −0.13) 0.021
diagnosis
NEC vs other −0.07 (−0.48 to 0.33) 0.700 0.81 (0.14 to 1.50) 0.019 0.81 (0.38 to 0.010 0.35 (−0.15 to 0.86) 0.200
JPGN • Volume 77, Number 6, December 2023
diagnosis 2.00)
PN dependent at time 0.57 (0.14 to 0.99) 0.010 0.46 (0.01 to 0.045 1.20 (0.43 to 2.00) 0.003 1.20 (0.38 to 0.005 −0.19 (−0.69 to 0.32) 0.500
of contrast series 0.91) 2.00)
PN length in total 0.0 (−0.01 to 0.0) 0.400 0.0 (−0.01 to 0.0) 0.500 0.0 (0.0 to 0.01) 0.300
PN length at time of 0.0 (−0.01 to 0.0) 0.500 0.0 (−0.01 to 0.01) 0.400 0.01 (−0.01 to 0.02) 0.300
contrast series
Gestational age 0.0 (−0.04 to 0.03) >0.900 −0.07 (−0.13 to 0.01) 0.020 0.05 (−0.12 0.574 −0.04 (−0.09 to 0.01) 0.130
to 0.22)
Birth weight 0.0 (0.0 to 0.0) 0.900 0.0 (0.0 to 0.0) 0.040 −0.0 (−0.0 0.618 0.0 (0.0 to 0.0) 0.200
to 0.0)
SB length (cm) 0.0 (0.0 to 0.01) 0.300 0.0 (−0.01 to 0.01) 0.600 0.0 (−0.01 to 0.0) 0.200
SB length (cm) as 0.16 (−0.13 to 0.45) 0.300 0.27 (−0.25 to 0.79) 0.300 −0.08 (−0.40 to 0.25) 0.600
categorical*
SB length (%) 0.01 (0.00 to 0.02) 0.044 0.01 (−0.0 to 0.073 0.01 (−0.01 to 0.02) 0.200 −0.01 (−0.02 to 0.0) 0.300
0.01)
SB length (%) as 0.11 (−0.23 to 0.45) 0.500 0.28 (−0.32 to 0.87) 0.400 −0.18 (−0.56 to 0.19) 0.300
categorical†
Colon length (%) 0.0 (0.0 to 0.01) 0.089 0.0 (−0.01 to 0.01) 0.600 −0.01 (−0.02 to 0.0) 0.300
Colon length (%) as 0.21 (−0.03 to 0.45) 0.089 0.03 (−0.40 to 0.45) >0.900 −0.03 (−0.45 to 0.38) 0.900
categorical‡
Endostomy −0.49 (−1.20 to 0.27) 0.200 −0.43 (−1.60 to 0.72) 0.500
β = unstandardized coefficient; CI = confidence interval; ICV = ileocecal valve; NEC = necrotizing enterocolitis; PN = parenteral nutrition; SB = small bowel; SBA = small bowel atresia. * SB length in
cm divided into 3 groups: <20 cm, between 20 and 40 cm, and ≥ 40 cm. † SB length in percentage of normal divided into 3 groups: <10%, between 10% and 25%, and ≥ 25%. ‡ Colon length in percentage
of normal divided into 3 groups: <50%, between 50% and 75%, and ≥75%.
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Abnormal Bowel Dilatation in Pediatric SBS
Nieminen et al JPGN • Volume 77, Number 6, December 2023
TABLE 3. Univariate cox hazard ratios (HR) with 95% confidence preterm with a greater potential to intestinal adaptation, possibly
intervals (CI) for weaning off parenteral nutrition contributing to their tendency for both SB dilatation and reaching
intestinal autonomy (26,27). Indeed, we found NEC patients almost
Variable HR (95% CI) P value
twice more likely to wean off PN compared to other etiologies
ICV preserved 3.15 (1.61–6.14) <0.001 (25,28–30). The association between SB dilatation and treatment
NEC vs other etiology 1.90 (1.01–3.55) 0.046 era suggests spontaneous oral feeding ad libitum, instead of arti-
Gestational age 0.95 (0.90–1.00) 0.032
ficial tube feeding, may decrease the tendency for abnormal bowel
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dilatation (20).
Birth weight 1.00 (1.00–1.00) 0.026 There have been no previous attempts to set cutoff values for
SB 15%–30% Reference pathological bowel dilatation, while previous research has largely
SB under 15% 0.18 (0.02–1.43) 0.105 focused on SB dilatation (9,18). To our knowledge, this is the first
study analyzing the degree of bowel dilatation not only in SB but
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JPGN • Volume 77, Number 6, December 2023 Abnormal Bowel Dilatation in Pediatric SBS
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