Short bowel syndrome (SBS), a subgroup of intestinal failure, is a condition that occurs after major resection of the small intestine due to congenital or acquired lesions that result in malabsorption [12]. Throughout the past decades, there have been a variety of definitions for SBS. When evaluating the short bowel, the focus used to be on the length of the small intestine. However, recently, definitions have been based more on the function of the remaining bowel than on the length of the small intestine [34]. Thus, SBS is generally defined as either requiring parenteral nutrition (PN) for >60 days after small bowel resection or having a remnant small bowel length (RSBL) <25% of that expected for gestational age [56].

According to a previous study, the overall incidence of pediatric SBS was 24.5 per 100,000 live births, with its incidence increased in premature birth [7]. Commonly, major resection of the small bowel is caused by necrotizing enterocolitis (NEC), although it can also occur due to midgut volvulus, intestinal atresia, or motility disorders such as chronic intestinal pseudoobstruction (CIPO) [8]. In one study, the mortality rate of SBS was 27% over 5 years [9]. The mortality was primarily due to complications related to PN. Children with SBS are initially dependent on PN for survival. They may require long-term PN support for several years. As a result, some patients need PN administered at home rather than in a hospital.

Unfortunately, PN and central venous catheters used for PN can be risk factors contributing to the high morbidity and mortality of SBS. For example, sepsis due to catheter-related bloodstream infections (CRBSI) and cholestasis often develops into PN-associated liver disease (PNALD). Factors such as RSBL, preservation of the ileocecal valve (ICV), and anatomical type of SBS are also known to significantly impact the morbidity and mortality of SBS [1011121314]. Thus, it is important to study pediatric SBS despite its low incidence because it is a major cause of intestinal failure with a high mortality rate.

Malnutrition and growth failure are critical problems in the pediatric population. About 54% of SBS patients who finally discontinue PN can achieve enteral autonomy. It has been reported that the length of the small intestine or the etiology is related to enteral autonomy [1314]. Studies on growth outcomes of pediatric SBS patients often show significant increases in height and weight during the follow-up period, although a large number of children remain below average and catch-up [15]. Unfortunately, few studies have evaluated surgical aspects, nutritional aspects, and prognostic factors of SBS [16]. Although remaining bowel length, underlying disease, and preservation of the ICV have been found to be factors correlated with growth and ability to wean from PN, studies have shown inconsistent results [171819].

Thus, this study reviewed pediatric SBS patients from our center, aiming to analyze clinical outcomes including growth and PN dependence based on etiology and anatomical type.

Patients diagnosed with SBS at Seoul National University Children’s Hospital between January 2004 and December 2018 were retrospectively reviewed. In this study, SBS was defined as the need for PN for more than 60 days after small bowel resection because of gastrointestinal intolerance or a bowel length of less than 25% of bowel length predicted for gestational age [56]. Patients with intestinal failure who underwent only colon resection without small bowel resection and those with intestinal failure due to malabsorption were excluded from this study.

By reviewing medical records, the following data were collected and analyzed: demographics (such as onset age, sex, gestational age, birth weight, and underlying etiology), postoperative follow-up data including surgical procedure, anatomical type of SBS, PN support, growth outcomes, and complications such as CRBSI, PNALD, and mortality. Anatomical types of SBS are classified as follows: (1) type I (small intestine resection and presence of enterostomy), (2) type II (small intestine resection with jejunocolic anastomosis), and (3) type III (small intestine resection with jejunoileal anastomosis and intact colon) [820]. Absolute RSBL was measured during the initial surgery related to SBS. The percentage of expected RSBL was calculated by comparing the measured length with the expected length based on postconceptional age [21]. CRBSI was defined as the identification of bacteria from both peripheral and central line blood cultures, where the same pathogen was detected in both samples [22]. PNALD was defined as a direct bilirubin level of 2.0 mg/dL or higher on laboratory tests after 2 weeks of starting PN, excluding other causes of elevated bilirubin unrelated to PN [23]. Growth outcome was calculated as weight-for-age in z-score according to the World Health Organization growth chart [24]. Data from all patients, including those who died during follow-up, were analyzed until the point of their last available clinical data to minimize bias in outcome assessment.

Distribution of continuous variables is reported as mean and standard deviation. Categorical variables are presented as numbers and percentages. Statistical analyses included the Kruskal-Wallis test, chi-square test, and Fisher exact test. Significance was considered when the P-value was less than 0.05. After conducting the Kruskal-Wallis test, post-hoc analysis using Dunn test was performed to compare groups and determine significant differences between specific groups. All statistical analyses were performed using IBM SPSS Statistics for Windows ver. 25.0 (IBM Corp.).

This study was approved by the Institutional Review Board of Seoul National University Hospital (No. SNUH 1809-108-974), and the requirement for informed consent was waived.

Table 1 presents the general demographics of 55 pediatric SBS patients in our center. The most common underlying etiology was NEC, followed by motility disorder, total colonic aganglionosis (TCA), and midgut volvulus. Of these patients, 52.7% were born preterm (<gestational age 37 weeks) and 87.3% were diagnosed with SBS before the age of 1 year. The mean absolute RSBL was 52.4 ± 39.1 cm and the percentage of expected RSBL was 32.2% ± 20.9%. Regarding anatomical types, type I, type II, and type III accounted for 40%, 32.7%, and 27.3%, respectively. Table 2 summarizes the outcomes of all patients. The mean follow-up period was 82.7 ± 64.7 months. At the last follow-up, 21 patients (38.2%) had a weight below the 3rd percentile. The mean weight-for-age (z-score) was -2.00 ± 2.07. The mean duration of PN was 21.0 ± 25.5 months, with 43.6% of patients receiving home PN to continue their nutrition. Twenty-nine patients (52.7%) were weaned off PN. Incidence rates of CRBSI and PNALD were 36.4% and 20.0%, respectively. Two patients in the NEC group died during the follow-up period due to sepsis, at 2 and 15 months of age, respectively. Both were included in the analyses of growth and PN-related outcomes up to their time of death. The early mortality of one patient may have introduced potential survivorship bias when interpreting long-term outcomes. Fig. 1 shows the relationship between underlying etiology and anatomical types. In the NEC group, 66.7% of patients were classified as type II. On the other hand, most (93.3%) motility disorders and all (100%) TCA cases were type I with enterostomy. Midgut volvulus was evenly split between type II and type III, while all atresia cases fell under type III.

SBS is a severe condition characterized by a significant reduction in the small bowel length, often leading to dependence on PN. Over the years, the definition of SBS has evolved, with a shift in focus from bowel length to functionality of the remaining bowel [346]. This trend reflects the recognition that even with a relatively long remnant bowel, some patients may still require prolonged PN due to functional deficits. In our study, the mean expected RSBL was 32.2%, which was longer than the typical SBS definition cutoff of 25%. This might be due to our center’s approach of performing earlier surgical interventions or adopting more conservative bowel resections. However, the rate of the PN weaning was relatively low compared to other studies [1325]. This might indicate that a substantial number of patients still face significant challenges in achieving enteral autonomy despite having more than 25% of expected RSBL. This contrasted with other studies where RSBL was shorter, highlighting variability in patient outcomes depending on different contributing factors such as etiology and anatomical type [13262728].

In our cohort, the most predominant cause was NEC, which aligned with previous reports on the etiology of pediatric SBS [1314]. The difference of the present study compared to other studies was the relatively high proportion of motility disorders such as CIPO [202930]. We also had a few unique cases, such as one patient who developed SBS following bowel perforation during air reduction for intussusception and another patient with superior mesenteric artery injury leading to bowel ischemia during retroperitoneal tumor resection. The distribution of anatomical types also reflected underlying etiologies, with NEC being primarily associated with type II while motility disorders being mostly classified as type I. This anatomical distribution is critical for understanding how different surgical outcomes and postoperative management strategies are necessary according to etiology.

Growth failure remains a significant issue for pediatric SBS patients, even for those who have eventually achieved enteral autonomy [3132]. As shown in Fig. 2, a majority of our patients (90.9%) had growth measurements below the 50th percentile, with 38.2% falling below the 3rd percentile. The overall mean weight-for-age (z-score) for all patients was -2.00 ± 2.07, which was comparable to or lower than growth outcomes reported in other studies [3334]. In the study by McLaughlin et al. [34], the weight-for-age (z-score) at 2 years of age for pediatric SBS was 0.90 ± 1.10. This difference might be attributed to the fact that our cohort data reflected growth outcomes at the last follow-up after a longer-term period, along with higher rates of prematurity and a greater prevalence of motility disorders as an etiology. In the analysis by etiology and anatomical type, lower weight-for-age (z-score) was observed for cases with motility disorders and type I anatomy. Children with motility disorders commonly have high output jejunostomy and often face ongoing gastrointestinal complications, which can hinder their nutritional absorption and growth. This is consistent with a previous study showing that malabsorption, losses through large volumes of stool, recurrent sepsis, and attempts to reduce or discontinue PN due to PNALD could contribute to inadequate growth [32].

Achieving enteral autonomy, defined as independence from PN, remains a primary goal in SBS management. In our study, 52.7% of patients were weaned off PN, which aligned with the results of other studies [2628]. As reported in previous literature, certain factors such as RSBL, the presence of the ICV, and underlying diseases play critical roles in determining whether PN can be successfully discontinued [6142835]. In a study by Kong et al. [36], preservation of the ileum was associated with an increased possibility of PN weaning, which was attributed to the ileum’s greater adaptive potential in nutrition and fluid absorption compared to the jejunum. Our study showed that patients with motility disorders had significantly longer PN durations and prolonged dependency on intravenous nutrition compared to patients with NEC or intestinal atresia. Additionally, patients with type I had longer PN durations than patients with type III. Patients with type I were also less likely to be weaned off PN and more likely to require home PN. These findings could be explained by the loss of ICV in type I patients, along with the fact that they underwent more extensive ileal resection compared to other types, leading to a reduced absorptive capacity. In contrast, type III patients, who have more intact bowel anatomy and a preserved ICV, were better equipped for enteral nutrition, leading to faster PN weaning. In these type I patients with high-output stomas, to support enteral adaptation, our center typically initiates trophic feeding in the early phase to stimulate mucosal adaptation, followed by gradual advancement using elemental enteral formulas (e.g., Neocate [Nutricia], Monowell [Korea Medifood], and Elemental 028 [Nutricia]) based on individual tolerance. Continuous feeding is preferred in these patients to increase mucosal contact and enhance absorption. For selected patients with a distal stoma, refeeding protocols are applied to improve distal bowel adaptation and fluid absorption. Oral intake is actively encouraged in parallel with tube feeding to reduce the risk of oral aversion during prolonged nonoral nutrition.

CRBSI and PNALD are major causes of morbidity and mortality in pediatric SBS patients who require long-term vascular access for PN. In this report, incidence rates of CRBSI and PNALD were 36.4% and 20.0%, respectively, aligning with rates reported in other studies [3738]. Analysis by anatomical type showed the highest incidence of CRBSI and PNALD in type I, although no statistically significant differences were observed between groups, which could be attributed to a retrospective study design and a relatively small sample size. A previous study has shown that the presence of an enterocutaneous stoma is associated with a higher risk of CRBSI due to microbial imbalances and an overabundance of conditional pathogens [39]. Additionally, other research studies have found that ileum resection and enterostomy can block the enterohepatic circulation of bile acids, leading to cholestasis and subsequent liver disease [2728]. The higher burden of infection and cholestasis among patients with enterocutaneous stomas underscores the need for vigilant management and possibly earlier transition to alternative nutritional strategies.

Although stoma-related complications such as dehydration, electrolyte imbalance, stoma prolapse or retraction, and peristomal skin breakdown were not systematically evaluated in this study, they remain important clinical concerns, particularly for patients with type I SBS. However, in our center, elemental formulas and distal stoma refeeding protocols are routinely employed in the management of high-output stomas to reduce fluid and electrolyte loss, enhance nutrient absorption, and mitigate stoma-related morbidity.

Improving outcomes for pediatric SBS requires a comprehensive approach centered on achieving enteral autonomy. Surgical interventions such as bowel lengthening procedures and small intestine transplantation in severe cases can significantly enhance intestinal adaptation [4041]. For patients requiring prolonged PN, extended hospitalization can increase the risk of infections and nutritional complications, potentially diminishing their quality of life. Therefore, effective home PN programs and multidisciplinary management are crucial for supporting near-normal growth and reducing complications. At our center, the home PN program and advanced home-care services can support SBS patients who require long-term PN, with catheter management by a skilled nurse that could help reduce catheter-related infections such as CRBSI [42]. Additionally, developing personalized nutrition plans based on each patient’s underlying etiology and anatomical type might be essential.

This study has several limitations. First, it was a single-center study with a relatively small sample size, which might limit the generalizability of our findings. Second, this study could not fully control potential factors that might influence enteral nutrition regimens, infection occurrences, antibiotics use, and other anthropometric parameters due to its retrospective nature. Third, longitudinal growth data at standardized time points (e.g., 6 months, 1 year, 2 years) were not consistently available, which limited our ability to analyze catch-up growth or growth trajectories over time. Fourth, although this study found that outcomes in SBS patients varied according to etiology or anatomical type, it did not establish their significance as independent predictive factors. Further studies should focus on identifying factors that could predict successful weaning from PN and improving outcomes in pediatric SBS patients. Prospective studies investigating long-term quality of life and functional outcomes in SBS should also be a priority.

In conclusion, this study suggests that clinical outcomes in pediatric SBS patients can vary according to underlying etiology and anatomical type. Findings of this study suggest that tailored interventions based on these factors could potentially enhance patient outcomes. Further research is needed to understand their roles as independent prognostic factors to develop better treatment strategies for SBS.