Short bowel syndrome (SBS) refers to a malabsorptive condition due to the reduction
of more than 75% of small intestine's length, which is under the minimum length for
absorbing nutrients and maintaining normal nutritional status. SBS is a serious complication
that occurs in infants, which is often caused by conditions such as necrotizing enterocolitis,
intestinal atresia, or other conditions that require bowel resection. SBS affects
the ability of the intestine to absorb nutrients, losing micronutrients and electrolytes
needed for the child's development, thereby delaying the child's development, increasing
the risk of abnormal development, causing physical disabilities, and increasing the
risk of neonatal mortality if necessary treatment is not provided promptly.[1]
[2]
Currently, parenteral nutrition (PN) is one of the fundamental therapeutic approaches
in the treatment and management of SBS in neonates.[3]
[4] PN has been proven through previous studies around the world as it is highly effective,
has few complications, increases the chances of survival, and improves the quality
of life of infants with SBS.[3]
[4] However, if using the PN method for a long time, the negative effects of PN on their
babies are significant, especially with liver function. Another method used is total
parenteral nutrition (TPN), which has also been documented in the literature for its
effectiveness in improving child development and nutrient absorption until the babies
can be adapted to their existing body condition.5 In addition, in cases where the infant is unable to adapt, liver and nerve functions
are severely affected, bowel transplantation should be considered.[5] To optimize the SBS treatment, a multiperspective approach and the participation
of clinical experts from a variety of disciplines such as gastrointestinal, surgical,
nursing, nutrition, psychology, and social disciplines are required. For each infant
with SBS, personalized approaches are needed to help improve the child's overall condition.[6]
[7] To provide evidence about SBS management in a low-middle-income country, we reviewed
50 infant cases with SBS to examine the effectiveness of SBS management in a tertiary
hospital in Vietnam.
Materials and Methods
Study Design and Sampling Method
A case series was performed from March 2019 to 2020 on infants who were diagnosed
with short bowel syndrome and treated at National Children's Hospital from May 2016
to December 2020. We included all infants diagnosed with short bowel syndrome with
at least one of the following criteria[2]: (1) based on the remaining bowel length after surgery: residual jejunoileal segment
≤75 cm for those 1-year old and below or ≤ 100 cm for those aged over 1 year; or (2)
based on bowel function after surgery: after small bowel resection, the patient must
be fed intravenous support for more than 42 days due to bowel dysfunction. Patients
were excluded if (1) patient's family and/or guardians did not allow patients to participate
in the study; (2) the medical record was incomplete; and (3) infants with comorbidities
requiring long-term PN such as complex congenital heart, chyme pleural effusion, oropharyngeal
tumor, etc. Patients were conveniently recruited. During the study period, a total
of 50 patients with short bowel syndrome from May 2016 to December 2020 were reviewed.
The Institutional Review Board of the National Children's Hospital approved the study
protocol (Code: 1424/BVNTW-VNCSKTE).
Study Procedure and Data Collection
The patient was admitted to the hospital and evaluated for clinical and laboratory
features before undergoing bowel resection (T0). After surgery, patients were treated for short bowel syndrome with different regimens
based on each patient. Patients were evaluated for clinical and laboratory characteristics
before (T1) and after (T2) treatment for short bowel syndrome.
In this study, we developed a standardized medical record with all the information
required. We then screened and selected patients who matched the inclusion and exclusion
criteria. Research team members explained to the patient's caregiver the purpose and
significance of the study and asked if the infant could participate in the study.
After obtaining the consent of the caregivers, the children were included in the study.
We divided the patients who met the study criteria into two groups. For the group
of children who were already treated with PN at the hospital, the patient's information
was collected into the standardized medical record. In addition, these patients were
scheduled for a follow-up visit, or if the child was unable to visit the hospital,
the caregiver was called to inquire about the child's current medical condition according
to the information in the standardized medical record. For the group of children who
participated in the study after starting treatment, we collected information according
to standardized medical records through clinical examination and paraclinical tests.
Data collectors were carefully trained to ensure consistent data quality and high
accuracy. The collected data were also cross-checked to ensure that the information
was not incorrect or missing. The collected data in this study included the following
factors.
General Information
Child's medical history: including information on age, gender, obstetric history, birth weight, cause of short
bowel syndrome, reason for hospital stay, number of hospital stays, number of surgeries,
complications experienced, the length of the remaining bowel from the angle of Treitz,
and the status of the ileo-jejunal and colonic valves. Causes of bowel resection were
collected from the surgical record, discharge diagnosis, and physical examination.
In the study, the main causes of short bowel syndrome in children included necrotizing
enterocolitis, megacolon, intestinal atresia, midgut volvulus, and others.
Clinical Symptoms
Nutritional status: The nutritional status of a child was determined by measuring weight and height.
Children were weighed with SECA electronic scale. The undernutrition status of children
was assessed according to the World Health Organization's standards based on the Z-score
threshold compared with the reference population.[8]
where
-
The measured weight was the weight of the patient.
-
The mean of the reference population was the average weight of children of the same
age in Vietnam.
-
Standard deviation was the standard deviation of the weight of children of the same
age in Vietnam.
Malnutrition status of children was divided according to the following levels:
-
+ No malnutrition: −2 standard deviation (SD)
-
+ Moderate malnutrition: −2SD to −3SD
-
+ Severe malnutrition: from −3SD to −4SD
Water and electrolyte malabsorption and nutritional deficiencies: including information on the number of bowel movements per day, stool characteristics,
degree of dehydration, and manifestations of electrolyte disturbances. In addition,
children were evaluated for anemia, deficit Vitamin A, Ca and Mg +2, Vitamin D, diarrhea,
raw stool, and dehydration.[9]
Infections: including infections such as surgical site infections, catheter infections, and sepsis
and other complications if present such as liver failure or osteoporosis
Nutritional status: includes complete or partial PN and enteral nutrition.
Classification of short bowel syndrome: based on the surgical report, surgeon consultation, and clinical examination, including
three types: (1) type 1: resection of ileum with or without ileocecal valve resection;
(2) type 2: partial jejunal resection, ileostomy, and terminal jejunal drainage; (3)
type 3: mainly jejunal resection, preserving more than 10 cm of terminal ileum and
colon.
Laboratory Indicators
Indices to assess the malabsorption of water, electrolytes, and nutrients were collected.
Hypokalemia disorder was classified according to three levels: mild (serum potassium
concentration from 3 to 3.5 mmol/L); moderate (< 2.5 mmol/L); and severe (< 2 mmol/L).[10] The state of hypomagnesemia was assessed according to two levels: mild (including
manifestations such as anorexia, nausea, vomiting, muscle weakness, and asthenia)
and severe (including neuromuscular disorders, cardiovascular disorders, metabolic
disorders, etc.).[11] Blood counts, hemodynamics, and blood biochemistry tests were performed at the time
of admission, after surgery, and weekly monitoring during treatment until the patient
was discharged, including the hemoglobin (g/L), hematocrit (L/L); prothrombin time
(%); international normalized ratio; fibrinogen (g/L); albumin (g/L); sodium, potassium,
calcium (g/L); and micronutrients in the blood such as iron, zinc, magnesium, vitamin
D, phosphorus (mmol/L). The indicators of complications and infections were also collected,
including white blood cell count, neutrophil leukocyte percentage (%), blood infection,
wound infection, catheter infection, and liver and kidney function.
Information about Treatment
Child rearing status: information collected includes:
-
Complete intravenous nutrition, complete oral nutrition, or combined intravenous and
oral nutrition.
-
Intravenous feeding route: peripheral vein, central vein, and peripheral vein placed
in the center.
-
Mean time of intravenous PN nutrition after surgery.
-
Time to start oral feeding after small intestine resection.
-
Feeding route: oral feeding or feeding pump through the nasogastric tube.
Feeding methods: complete breast milk, fully hydrolyzed milk, combination of breast milk and hydrolyzed
milk, and combination of solid food.
Length of hospital stay: calculated in days from the time of admission to the time of discharge, including
the length of stay in the hospital for treatment of comorbidities or acquired during
treatment.
Information about Treatment Outcomes
We evaluated treatment outcomes according to the following levels ([Table 1]).
Table 1
Criteria for evaluating the results of treatment of short bowel syndrome
|
Criteria
|
Good
|
Fair
|
Poor
|
|
Clinical symptom
|
Children no longer had short bowel syndrome
|
Patients had mild symptoms after treatment such as less watery stools (3–5 times/d),
greasy stools, mild malnutrition.
|
Patients with severe clinical symptoms after treatment such as moderate or severe
malnutrition; diarrhea ≥ 6 times/d, with signs of dehydration and electrolyte disturbances
|
|
Laboratory results
|
Laboratory parameters were within normal limits or there was a mild disorder but no
clinical manifestations
|
Laboratory parameters were close to normal and there were no clinical manifestations
|
Patients with large changes in laboratory parameters suggesting severe anemia, electrolyte
disturbances
|
|
Nutrition
|
The patient stopped being dependent on PN and was able to eat and drink independently
by mouth completely
|
The patient was on oral nutrition but partially dependent on the PN
|
Patients who were completely dependent on PN or must maintain HPN
|
|
Complication
|
No complications or mild complications such as wound infection but stable treatment
during treatment
|
There might be complications during treatment such as sepsis, catheter infection but
were treated stably
|
Patients with severe complications such as unstable sepsis, IFALD, or death
|
|
Reoccurrence
|
The patient did not have to be readmitted because of symptoms of short bowel syndrome
|
The patient was readmitted after the first postoperative discharge due to severe symptoms
of the disease
|
The patient was readmitted several times after discharge since the first postoperative
period due to complications as well as clinical symptoms of short bowel syndrome.
|
Abbreviations: HPN, home parenteral nutrition; IFALD, intestinal failure-associated
liver disease; PN, parenteral nutrition.
Complications: Complications during treatment were noted, including catheter infection, bacteremia,
catheter occlusion, central venous thrombosis, hyperglycemia, micronutrient deficiencies,
confusion, and organ dysfunction.
Statistical Analysis
Data were analyzed using SPSS 20.0 software. Descriptive statistics were performed.
Paired t-test was performed to assess the difference in clinical and laboratory indicators
between, before, and after the intervention. Statistical significance was determined
with p-value < 0.05.
Results
Of 50 patients, most of them were male (60%) and 6 months old or below (90.0%). SBS
mainly in the group of children ≤ 6 months old (90%). The majority of them had SBS
due to necrotizing enterocolitis (42.0%), followed by megacolon (22.0%) and intestinal
atresia (14.0%). Most of the patients with SBS had type 2 (54.0%) and were in the
acute phase (62.0%). Only 40.0 and 34.0% of patients preserved colon and ileocecum
valve, respectively. The common clinical symptoms included diarrhea (39.0%), dehydration
(30.0%), malnutrition (52.0%), and greasy stool (34.0%). There were 24.0% patients
having severe malnutrition. ([Table 2])
Table 2
Demographic and clinical characteristics
|
Characteristic
|
Frequency (n)
|
Percentage (%)
|
|
Gender (n = 50)
|
Male
|
30
|
60.0
|
|
Female
|
20
|
40.0
|
|
Age group (n = 50)
|
≤ 6 mo
|
45
|
90.0
|
|
> 6–12 mo
|
2
|
4.0
|
|
> 12 mo
|
3
|
6.0
|
|
Birth history (n = 50)
|
Full months
|
35
|
70.0
|
|
Prematurity
|
15
|
30.0
|
|
Causes of short bowel syndrome (n = 50)
|
Necrotizing enterocolitis
|
21
|
42.0
|
|
Megacolon
|
11
|
22.0
|
|
Intestinal atresia
|
7
|
14.0
|
|
Midgut volvulus
|
8
|
16.0
|
|
Others
|
3
|
6.0
|
|
Classification of short bowel syndrome (n = 50)
|
Type 1
|
6
|
12.0
|
|
Type 2
|
27
|
54.0
|
|
Type 3
|
17
|
34.0
|
|
Phases of short bowel syndromes (n = 50)
|
Acute phase
|
31
|
62.0
|
|
Adaptation phase
|
13
|
26.0
|
|
Maintenance phase
|
6
|
12.0
|
|
Condition (n = 50)
|
Preserved colon
|
20
|
40.0
|
|
Preserved ileocecum valve
|
17
|
34.0
|
|
None
|
13
|
26.0
|
|
Clinical symptoms (n = 50)
|
Malnutrition
|
26
|
52.0
|
|
Diarrhea
|
39
|
78.0
|
|
Greasy stool
|
17
|
34.0
|
|
Signs of dehydration
|
30
|
60.0
|
|
Electrolyte disturbances
|
9
|
18.0
|
|
Malnutrition levels (n = 50)
|
Not malnutrition (≥ − 2SD)
|
24
|
48.0
|
|
Moderate malnutrition (from −2SD to −3SD)
|
14
|
28.0
|
|
Severe malnutrition (from −3SD to −4SD)
|
12
|
24.0
|
Abbreviations: SD, standard deviation.
[Table 3] shows the laboratory characteristics of patients with SBS before treatment. Vitamin
D3 deficit had the highest proportion at 80%, followed by hemoglobin deficit (75.5%),
hypoalbuminemia (68.1%), prothrombin deficit (64.3%), and phosphorus deficit (61.5%).
Only 12.5% of patients had lack of zinc.
Table 3
Laboratory characteristics of short bowel syndrome before surgery
|
Laboratory characteristics
|
Total
|
Mean ± SD
|
Min
|
Max
|
Abnormal condition
|
|
n
|
%
|
|
Hemoglobin (g/L)
|
49
|
124.2 ± 26.0
|
61
|
184
|
37
|
75.5
|
|
Prothrombin (%)
|
42
|
69.9 ± 22.7
|
26
|
117
|
27
|
64.3
|
|
Electrolyte disturbance
|
Sodium (mmol/L)
|
47
|
136.1 ± 6.8
|
120.3
|
166
|
23
|
48.9
|
|
Potassium (mmol/L)
|
48
|
4.0 ± 0.73
|
2.5
|
5.4
|
22
|
45.8
|
|
Albumin (g/L)
|
47
|
33.3 ± 7.3
|
19.2
|
51.3
|
32
|
68.1
|
|
Micronutrient deficiency
|
Total calcium (mmol/L)
|
44
|
2.09 ± 0.46
|
0.94
|
2.75
|
26
|
59.1
|
|
Iron (mmol/L)
|
10
|
11.17 ± 8.28
|
0.2
|
23.9
|
4
|
40.0
|
|
Zinc (mmol/L)
|
8
|
15.85 ± 11.77
|
7.3
|
40.98
|
1
|
12.5
|
|
Vitamin D3 (mmol/L)
|
5
|
30.35 ± 24.21
|
16.89
|
73.34
|
4
|
80.0
|
|
Phosphorus (mmol/L)
|
13
|
1.28 ± 0.47
|
0.58
|
2.21
|
8
|
61.5
|
|
Magnesium (mmol/L)
|
27
|
0.72 ± 0.17
|
0.44
|
1.01
|
9
|
33.3
|
[Table 4] reveals the characteristics of treatment process. Most of the patients received
both enteral nutrition and TPN (96%) approaches. One patient died during treatment.
Among the remaining 49 patients, the majority of them received PN through peripheral
veins (75.5%), followed by central vein (20.4%). The common nourishing solutions included
NaCl 0.9%, ringer, glucose (82.6%), and electrolyte: NaCl 10%, KCl 10% (63.0%), albumin
(60.8%) and lipids (39.1%). There were 71.4% of patients receiving oral feeding, and
hydrolyzed milk was the primary feeding method (67.3%).
Table 4
Treatment characteristics
|
Characteristics
|
Frequency (n)
|
Percentage (%)
|
|
Nourishing lines
|
Enteral nutrition (EN)
|
1
|
2.0
|
|
Total parenteral nutrition (TPN)
|
1
|
2.0
|
|
Combining EN and TPN
|
48
|
96.0
|
|
Method of parenteral nutrition
|
Peripheral veins
|
37
|
75.5
|
|
Central vein
|
10
|
20.4
|
|
Peripheral inserted central catheter
|
2
|
4.1
|
|
Nourishing solutions
|
Albumin
|
28
|
60.8
|
|
Lipids
|
18
|
39.1
|
|
Red blood cell
|
17
|
36.9
|
|
Acid amin
|
12
|
23.9
|
|
Infusion: NaCl 0,9%, ringer, glucose
|
38
|
82.6
|
|
Electrolyte: NaCl 10%, KCl 10%
|
29
|
63.0
|
|
Micronutrient: Mgso4 10%, Cacl2, Vitamin AD
|
11
|
23.9
|
|
Vitamin K1
|
17
|
36.9
|
|
Feeding route
|
Through the nasogastric tube
|
14
|
28.5
|
|
Orally administered
|
35
|
71.4
|
|
Feeding methods
|
Breast milk completely
|
2
|
4.1
|
|
Hydrolyzed milk completely
|
33
|
67.3
|
|
Combined
|
6
|
12.2
|
|
Combined with more solid food
|
8
|
16.3
|
[Table 5] shows the progress of SBS treatment. The rate of malnutrition reduced from 52 to
36%, and the rate of diarrhea decreased from 78 to 62%. However, these changes were
not statistically significant (p > 0.05). Only hemoglobin was found to have significant improvement after treatment
compared to before treatment (p < 0.001). Overall, 26.0% of the patients had good treatment outcomes, 46% had fair
outcomes, and 28% had poor outcomes. There were three cases who died after treatment
(6.0%). Eighteen percent of patients suffered from sepsis, followed by wound infection
at 10%. Weight, red blood cell, prothrombin, albumin, and potassium increased significantly
after treatment compared to results before treatment (p < 0.05).
Table 5
Treatment outcomes
|
Characteristics
|
After surgery and before treatment
|
After treatment
|
p-Value
|
|
n
|
%
|
n
|
%
|
|
Clinical symptoms
|
|
Malnutrition
|
26
|
52.0
|
18
|
36.0
|
0.107
|
|
Diarrhea
|
39
|
78.0
|
31
|
62.0
|
0.081
|
|
Laboratory characteristics
|
|
Deficit Hemoglobin
|
37
|
74.0
|
17
|
34.0
|
<0.001
|
|
Deficit Prothrombin
|
27
|
54.0
|
19
|
38.0
|
0.108
|
|
Hypoalbuminemia
|
32
|
64.0
|
23
|
46.0
|
0.070
|
|
Electrolyte disturbance
|
27
|
54.0
|
18
|
36.0
|
0.070
|
|
Treatment outcomes
|
|
Good
|
|
|
13
|
26.0
|
–
|
|
Fair
|
|
|
23
|
46.0
|
|
|
Poor
|
|
|
14
|
28.0
|
|
|
Complications
|
|
|
|
|
|
|
Wound infection
|
|
|
5
|
10.0
|
–
|
|
Catheter infection
|
|
|
1
|
2.0
|
–
|
|
Sepsis
|
|
|
9
|
18.0
|
–
|
|
Intestinal failure-associated liver disease
|
|
|
1
|
2.0
|
–
|
|
Death
|
|
|
3
|
6.0
|
–
|
|
Mean ± SD
|
Mean ± SD
|
|
|
Weight (kg)
|
5.46 ± 2.94
|
5.68 ± 2.90
|
0.001
|
|
Red blood cell (T/L)
|
3.58 ± 0.64
|
3.94 ± 0.81
|
0.005
|
|
Hemoglobin (g/L)
|
106.47 ± 23.04
|
113.8 ± 21.83
|
0.083
|
|
Prothrombin (%)
|
65.54 ± 17.90
|
78.14 ± 16.60
|
0.001
|
|
Albumin (mmol/L)
|
30.45 ± 6.43
|
36.03 ± 7.67
|
0.001
|
|
Sodium (mmol/L)
|
133.27 ± 8.46
|
135.88 ± 4.38
|
0.059
|
|
Potassium (mmol/L)
|
3.68 ± 0.85
|
4.04 ± 0.69
|
0.004
|
Abbreviations: SD, standard deviation.
Overall, patients mainly had fair treatment outcomes (46%), followed by poor results
(28%), and good results (26%). [Fig. 1] shows poor treatment outcomes mainly in patients with type 3 short bowel syndrome
(47.1%), patients with type 2 short bowel syndrome had fair outcomes (59.3%), and
patients with type 1 had good outcomes. However, the difference was not statistically
significant with p > 0.05.
Fig. 1 Treatment outcome according to types of short bowel syndrome
Discussion
The study provides some preliminary evidence on the outcome of treatment of short
bowel syndrome in infants at a tertiary hospital in Vietnam. The main treatment goals
in short bowel syndrome are to maintain the nutritional status of the patient and
to normalize the macronutrient and micronutrient status.[12]
[13] However, nutritional care for children with the chronic intestinal disease remains
a challenge for many pediatricians. Nutritional support for short bowel syndrome patients
is complex and must be individualized based on each patient's acute and chronic medical
conditions and problems.[14]
[15]
The results of the study showed that the percentage of patients with improved clinical
and subclinical symptoms before discharge was high. Clinical and laboratory parameters
both increased after treatment, especially weight, prothrombin, albumin, and potassium.
It indicated that the treatment solved disease symptoms, changed the patient's nutritional
status, as well as changed important indicators affecting the metabolism and development
of children. Children after treatment could return to normal development. The overall
assessment showed that patients mainly had good and fair treatment outcomes, meaning
that after treatment, the patient could gradually return to a normal life, and stop
receiving PN completely without serious complications. However, 26% of patients still
had a poor treatment outcome, including patients who died, had severe complications
after treatment, or had not stopped receiving PN completely and had to be rehospitalized.
These patients were mainly patients with short bowel syndrome type 3, who had a large
jejunal resection. This is understandable when the jejunum is where most of the nutrients
needed for body development are absorbed. Therefore, for these patients, other interventions
such as surgical treatment or intestinal transplantation are required to enable the
patient to achieve normal growth.
Sepsis and hepatic failure due to intravenous nutrition were the two main causes of
death in the majority of studies.[12]
[13]
[16] In this study, there were nine children (18%) with sepsis complications recorded.
Sepsis was the cause of death of one child in the study. It was a male child, who
underwent surgery for intestinal atresia at 1 day of age, followed by ileostomy and
closed drainage 2 weeks later. After this period, the patient's condition did not
improve, the child was lethargic, continuously underwent mechanical ventilation and
vasopressor therapy, and the body experienced severe infection and toxicity. We supposed
that the cause was the anastomotic leaks. On day 6, after surgery to close the ileostomy,
the patient died from toxic septic shock and multiple organ failure. We also recorded
one case of liver failure due to PN with clinical symptoms including progressive jaundice;
blood bilirubin and liver enzymes elevated; and albumin and prothrombin decreased.
After treatment, the patient returned to normal condition. Another complication was
that surgical site infection was still at a high rate (nine patients), which showed
that the work of ensuring sterility and postoperative nursing care were not sufficient.
Two children died from respiratory failure. This was the result of many causes such
as premature birth, poor patient condition and inadequate organ function, malnutrition,
infection due to short bowel syndrome, major surgery, and difficult postoperative
period. The patient was constantly on a ventilator after surgery and could not remove
the endotracheal tube to breathe. The patient eventually developed respiratory failure
and died.
The limitation in the treatment of patients with short bowel syndrome in our study
was the insufficient medical and surgical treatments. The use of supportive drugs,
such as the combination of using trace elements such as iron, zinc, and vitamins intravenously
and intestinally, was still limited. We recorded that during the treatment period,
only two patients received oral Vitamin A and D. The patient had not undergone procedures
to prolong the length of the intestine, making the adaptation process of the remaining
bowel more difficult and time-consuming. The nutritional status when discharged from
the hospital was not good due to the lack of care and treatment to meet the patient's
needs as well as the limited guidance for relatives to take care of the child for
treatment at home. In addition, the child had not used intravenous feeding with a
catheter at home although the remaining intestine was not fully adapted. This caused
children to be readmitted to the hospital many times after discharge with repeated
diarrhea, dehydration, or malnutrition.
