Keywords surgery - stoma - sodium - supplementation - growth
Introduction
In young children (age ≤ 3 years), a small bowel stoma or colostomy might be necessary
in the treatment of congenital intestinal diseases or abdominal sepsis.[1 ]
[2 ] Stomas come with a substantial risk of morbidity. Taking into account both stoma
creation and closure, major stoma-related morbidity (Clavien–Dindo grade ≥ III) occurs
in 39% of the children.[3 ] Moreover, a stoma increases the loss of fluids and nutrients, which might result
in impaired growth.[4 ] This growth impairment at a young age can negatively impact long-term development
and cognitive ability, in particular, when it occurs in the first 9 months of life.[5 ]
[6 ] Moreover, this impairment of growth in itself is associated with an increased risk
of stoma-related complications and the need for reoperations.[7 ] For these reasons, some surgeons recommend early stoma closure, within 6 weeks following
formation.[3 ]
[4 ]
[8 ]
[9 ]
[10 ]
Children treated by a small bowel stoma are thought to be more prone to growth impairment
than children treated by colostomy. The higher risks of a high-output stoma and loss
of absorbent function of the small bowel and colon distal of the stoma are suggested
to cause this difference between both levels of stoma.[11 ]
[12 ] To what extent such different levels of stoma limit growth in young children is
not well known.
Next, type of intestine used to create the stoma, other patient-specific factors,
such as proximal small bowel stomas (within 50 cm of Treitz) and undergoing major
small bowel resection (≥ 30 cm), might decrease functional bowel length even more,
which could further impair growth. Moreover, experimental studies are linking inadequate
sodium supply with impaired growth in case of urine sodium levels of 30 mmol/L or
less.[13 ]
[14 ] Sodium supplementation might restore the cellular sodium environment and stimulate
growth, for which reason this became common practice at many institutions over the
past 20 years. However, there are no guidelines on the optimal management of sodium
supplementation in the presence of a stoma.[15 ]
Therefore, the aim of this study was to evaluate (1) the effect of constructing either
a small or large bowel stoma on growth in young children and (2) the effect of certain
patient-specific factors (early stoma closure, having a proximal stoma, undergoing
major small bowel resection (≥ 30 cm), or adequate sodium supplementation) on growth
status at stoma closure and within a year following closure expressed by weight-for-age
Z scores.
Methods
Patients and Management
All consecutive young children (≤ 3 years of age) with a small bowel stoma (jejunostomy
or ileostomy) or large bowel stoma (colostomy), created between 1998 and 2018 at our
tertiary university medical center, were identified from a surgical administrative
database. Patients were included in this analysis if (1) they underwent stoma closure
and (2) if birth weight, weight at stoma creation and closure, and at least one weight
measurement after closure were available. The medical ethical committee of the Academic
Medical Center in Amsterdam reviewed and approved the observational study (reference:
W18_233#18.278) design. Patients and parents received an opt-out letter for consent.
Following consent, patient records were checked for eligibility. Data were retrieved
and stored in an electronic database (Castor EDC).
Data Extraction
We (L.D.E.S. and I.V.) extracted information concerning: gender, prematurity (defined
as gestational age < 37 weeks), duration of pregnancy, underlying disease, time to
stoma closure (early closure was defined as closure within 6 weeks following creation),
need for readmission for stoma closure, need for total parenteral nutrition (TPN)
following stoma creation, number of centimeters of small bowel resected (major resection
was defined as ≥ 30 cm, independent of age), proximal location of a small bowel stoma
(defined as within 50 cm of the ligament of Treitz), weight before stoma creation
(weight closest to creation with a maximum of 3 days before creation), weight at stoma
closure (weight closest to closure with a maximum of 3 days before or after closure),
weight after stoma closure (first measure which was reported in a minimum of 3 months
and a maximum of 1 year after closure) and if sodium supplementation was given after
stoma creation.
Growth was measured with weight-for-age Z-scores and was calculated with the growth
calculator of the Youth Health Department (JGZ).[16 ] The weight-for-age Z-score (or standard deviation [SD] score) is a measure of the
SD for weight from the median value of a reference population matched for duration
of pregnancy, age, and sex.[16 ] The Z-score can be used to discriminate between a child that is gaining weight at
a slower (or faster) rate than the reference population and is well suited for a cohort
with prematures.[17 ]
Malnourishment was defined according to the World Health Organization's definition;
a weight-for-age Z-score between −3 and −2 was classified as mildly malnourished,
and a score weight-for-age Z-score below −3 as severely malnourished.[18 ]
The difference between Z-score at stoma creation and closure was calculated to express
growth curve in the presence of a stoma, with a negative growth curve indicating growth
impairment. The difference between Z-score at stoma closure and Z-score within the
year after closure was used to express the growth curve after stoma closure.
Urinary sodium levels were obtained from spot urinary samples obtained after the stoma
creation. The current regime at our institute is to evaluate urinary sodium two to
three times a week and to start supplementation if urinary sodium is less than 30 mmol/L.
Following stoma formation, the lowest urinary sodium measurement for each patient
was used defining a urine sodium level of 30 mmol/L or lower as deficient and 10 mmol/L
or lower as severely deficient.[14 ]
[15 ]
[19 ]
There is no official protocol for sodium supplementation at our institute. However,
in general practice, 2 mmol/kg oral sodium chloride daily is started, which could
be increased with steps of 1 mmol/kg in case of urine sodium levels of 30 mmol/L or
lower. If after the start of sodium supplementation, the urinary sodium values were
more than twice the levels of 30 mmol/L or lower, the sodium supplementation was defined
as inadequate.
Outcome Measures
The primary outcome was weight-for-age Z-scores. Comparative analyses of the primary
outcome were performed between different time points: at the time of creation, closure,
and within a year after closure. This was reviewed separately for patients with a
small bowel stoma and a colostomy. Differences in Z-scores at closure and within a
year following closure were compared between the following groups: (1) early and nonearly
closed stomas, (2) proximal and nonproximal small bowel stomas, (3) patients who received
a major small bowel resection (larger than 30 cm) and those who did not, and (4) adequate
versus nonadequate supplementation of sodium.
Statistical Analysis
Descriptive data were reported with a median with the interquartile range (IQR). Comparison
of changes in Z-scores following stoma closure and a year after closure was done by
Friedman's test with post hoc Wilcoxon signed rank test in case of significant results.
Comparison between the characteristics of young children with a small bowel stoma
and a colostomy was performed with chi-square tests for categorical data, t -tests for parametric continuous data, and the Mann–Whitney's U tests for nonparametric continuous data. Comparison of changes in Z-scores following
stoma closure and a year after closure was done by Wilcoxon's rank-sum test for all
secondary outcome measures. Comparison of Z-scores at stoma closure between different
groups at closure or at a year following closure was done by Mann–Whitney's U tests. All analyses were performed with IBM SPSS statistics, version 23 (IBM Corp.,
Armonk, New York, United States).
Results
Patient Characteristics
A total of 172 young children were included in our analysis. Of all infants, 61% (105/172)
were male and the median gestational age was 36 weeks (IQR: 32–38) of which 54% (93/172)
were born prematurely. In total, 58% (99/172) of the patients received a small bowel
stoma. Of the patients with a small bowel stoma, 10% (10/99) received a jejunostomy
and 90% (89/99) an ileostomy. Of all these small bowel stomas, 20% (20/99) were proximal
small bowel stomas. The median length of resected small bowel in those treated by
ileostomy was 7 cm (IQR: 2–13), and 11% (10/89) received a resection of more than
30 cm. In six (6%) patients treated by a small bowel stoma, data were missing on length
of resection. A colostomy was created in 42% (73/172) of the patients. Out of all
small bowel stomas, 43% (43/99) were created for treatment of necrotizing enterocolitis.
Treatment for an anorectal malformation was the most common (50/73, 63%) reason for
a colostomy. Median time to stoma closure was 15 weeks (IQR: 8–30) with a median follow-up
of 5 years (IQR: 2–9) after stoma closure. Early closure was performed in 21% (21/99)
of the small bowel stomas and 1% (1/73) of the colostomies. A comparison of the patient
characteristics of children treated with either small bowel stomas or colostomies
is presented in [Table 1 ].
Table 1
Baseline characteristics
Characteristic
Small bowel stoma (n = 99)
Colostomy (n = 73)
p -Value
Male gender, n (%)
61 (62)
44 (60)
0.89
Premature, n (%)
65 (66)
28 (38)
≤ 0.01
Median duration pregnancy (IQR), wk
34 (30–38)
37 (35–39)
≤ 0.01
Underlying disease, n (%)
Anorectal malformation
0
50 (69)
≤ 0.01
Necrotizing enterocolitis
43 (44)
7 (10)
Hirschsprung's disease
13 (13)
7 (10)
Intestinal atresia
12 (12)
4 (6)
Meconium ileus
14 (14)
1 (1)
Complex gastroschisis
6 (6)
1 (1)
Other
11 (11)
3 (4)
Median age at stoma formation (IQR), d
8 (2–17)
3 (1–31)
0.08
Median time to stoma closure (IQR), wk
9 (6.3–15)
28 (18–42)
≤ 0.01
Stoma creation and closure in same admission, n (%)
39 (41.5)
1 (1.4)
≤ 0.01
Median time of follow-up (IQR), y
4 (1.25–7)
7 (4–12)
≤ 0.01
Abbreviation: IQR, interquartile range.
Changes in Z-scores from Birth until a Year after Stoma Closure
The individual Z-scores for birth weight, weight at the time of stoma creation and
closure, and weight measurement within the first year after closure are presented
in [Fig. 1 ] and the information on nutritional status and growth are presented in [Table 2 ]. In the presence of a stoma, 61% (105/172) of the young children were declining
on the growth chart with a median Z-score for weight for age of −3.1 (IQR: −5.6 to
−1.23) in the small bowel stoma group and −1.45 (IQR: −2.3 to −0.62) in the colostomy
group at the time of stoma closure. This resulted in severe malnourishment during
the stoma closure in 51% (50/99) of the patients with a small bowel stoma, and 16%
(12/73) of those with a colostomy. Median time to stoma closure was 9 weeks (IQR:
6.3–15) in patients treated by a small bowel stoma and 28 weeks (IQR: 18–42) in the
case of a colostomy. After stoma closure, most young children were thriving with a
positive tract on the growth chart, 74% (73/99) versus 58% (42/73) in the small bowel
stoma and colostomy groups, respectively.
Table 2
Comparison of nutritional status and growth in infants with a small bowel stoma and
colostomy
Characteristic
Small bowel stoma (N = 99)
Colostomy (N = 73)
p -Value
TPN after stoma creation, n (%)
74 (76)
24 (37)
≤ 0.01
Sodium supplementation after stoma creation, n (%)[a ]
71 (86)
24 (49)
≤ 0.01
TPN poststoma closure, n (%)
57 (62)
4 (6)
≤ 0.01
Nutrition status at the time of stoma closure, n (%)
Normal
38 (38)
49 (67)
≤ 0.01
Malnourished
11 (11)
12 (16)
Severely malnourished
50 (51)
12 (16)
Positive growth tract presence stoma, n (%)
40 (40)
27 (40)
0.65
Positive growth tract after stoma closure, n (%)
73 (74)
42 (58)
0.03
Abbreviation: TPN, total parenteral nutrition.
a Sodium supplementation unknown small bowel stoma n = 16, colostomy n = 24.
Fig. 1 Bar chart median Z-score weight for age (IQR) at birth, stoma formation, stoma closure,
and within the year after stoma closure. IQR, interquartile range.
The change in Z-score from the time point of stoma formation to stoma closure and
to the time point within 3 months to a year after closure (mean: 9.2 months, SD: 5
months) was significant in both patient groups treated by small bowel stoma (p < 0.00) as well as colostomies (p = 0.04). Post hoc test showed that within small bowel stomas, this difference in
Z-score was most profound between stoma formation and stoma closure (p < 0.00) showing a decline in Z-score as well as the moment of stoma closure and within
a year following closure (p < 0.00) showing an incline. Z-scores did not differ significantly between moment
of stoma formation and within a year following closure (p = 0.44). In colostomies, the post hoc test showed a borderline nonsignificant (p = 0.07) difference in Z-scores between the moment of stoma closure and within a year
following closure. The differences in Z-scores between formation and closure (p = 0.10) and formation and within a year following closure (p = 0.24) were similar.
Factors Influencing Growth in Patients Treated with a Stoma
There was no significant difference in Z-score at the moment of closure (p = 0.19) as well as the Z-score within the year after closure (p = 0.20) when comparing patients who had early closure and those who had not. The
age at closure differed significantly (p < 0.00) between those who had an early closure (median 11 months; IQR: 9–14) and
those who had not (median: 16 months; IQR: 11–21).
Those treated with a proximal small bowel stoma had significantly lower Z-scores (p = 0.01) at stoma closure compared with those with a nonproximal small bowel stoma,
but weight within a year after closure did not differ between both groups (p = 0.07). Moreover, those who received a major small bowel resection had a lower Z-score
at stoma closure (p = 0.04) than those with less than 30 cm of resected small bowel. This significant
difference disappeared within a year after closure at which moment the Z-scores did
not differ between the groups (p = 0.27).
From the 172 young children, 49% (84/172) had data regarding urinary sodium measurements.
After the creation of a small bowel stoma, 92% (55/60) of the young children had a
mild or severe sodium deficiency, following a colostomy, this was 83% (20/24) ([Table 3 ]). Of the young children with a small bowel stoma, 92% (55/60) received sodium supplementation.
In 68% (41/60) of patients, there were more than two urine sodium levels less than
30 mmol/L after the start of supplementation, indicating inadequate sodium supplementation.
In the patients with a colostomy, 54% (13/24) received sodium supplementation which
was inadequate in 29% (7/24). The median Z-score at stoma closure of adequately supplemented
children was −2.4 (IQR: −4.3 to −1.3) which is lower than the median in nonadequately
supplemented children which was −1.7 (IQR: −3.4 to −0.5). This difference was borderline
nonsignificant (p = 0.06). A year after closure, this difference remained nonsignificant (p = 0.42). Also, there was no correlation (p = 0.50) between adequate sodium supplementation and a positive growth curve in the
presence of a stoma.
Table 3
Comparison of urinary sodium levels after creation of a small bowel stoma and colostomy
and the effect of sodium supplementation
Characteristic
Small bowel stoma (n = 60)
Colostomy (n = 24)
Lowest urine sodium level, mmol/L
> 30
5 (8)
4 (17)
10–30
31 (52)
11 (46)
< 10
24 (40)
9 (37)
Sodium supplementation
Adequate
14 (24)
6 (25)
Inadequate
41 (68)
7 (29)
None
5 (8)
11 (46)
Discussion
In the presence of a stoma, the majority (61%) of the patients were declining on the
growth chart. This resulted in severe malnourishment in 51% of the young children
with a small bowel stoma and in 16% of the patients with a colostomy at the time of
stoma closure. After stoma closure, the decline in Z-scores is reversed in most young
children; 67% showed a positive trend on the growth chart within a year following
stoma closure. The decline in growth during the treatment with a stoma is more profound
in small bowel stomas compared with colostomies. Growth at stoma closure was significantly
more impaired in those treated with a proximal small bowel stoma and those who received
a stoma after major small bowel resection. Early closure did not significantly affect
Z-scores at stoma closure, although closure is realized at a significantly younger
age. Within a year following closure, none of the evaluated factors had a significant
influence on the Z-scores.
Our results are in line with previous reports in small cohorts of infants treated
with a stoma for multiple abdominal diseases and show that in the presence of both
small and large bowel stomas, a decline in growth can be expected.[14 ] Those treated with a small bowel stoma and specifically those treated with a proximal
small bowel stoma or those undergoing major small bowel resection seem most at risk.
Stoma excretion from the small bowel is higher in nutrients than excretion from colostomies
which suggests that in the latter, more nutrients are resorbed which might contribute
to this difference in growth.[20 ] This could also explain why more patients treated with a small bowel stoma were
in need of TPN following stoma formation compared with colostomies. This difference
in functional proximal bowel might also explain why patients with more proximal stomas
and those who underwent a major resection have significant lower Z-scores at stoma
closure. Another explanation could be found in the differences in the types of disease
which result in small bowel stomas, in our cohort mostly necrotizing enterocolitis.
In patients treated for necrotizing enterocolitis, length of resected intestine and
prolonged inflammation both negatively influence growth.[8 ]
[21 ]
It seems that stoma closure as soon as possible is a necessity for growth in all young
patients which is in line with previous findings.[4 ] Even those at highest risk of growth impairment at the moment of stoma closure (patients
treated by proximal ileostomy and those who underwent a major small bowel resection)
show similar growth within a year following closure compared with patients with nonproximal
small bowel stomas and those who did not underwent a major resection. This suggests
that patients experience catch-up growth following stoma closure, even when there
is less functional small bowel left, either due to resection or due to underdevelopment
caused by disuse. Since stoma closure seems such an important condition for growth,
this could be seen as an argument for early closure. In young children, there is no
consensus on the optimal timing of stoma closure. Some surgeons would wait for a safe
weight (e.g., > 2.5 kg) to reduce the risk of surgery in a fragile patient.[22 ] Other, more recent studies report no significant difference in postoperative complications
when a stoma is closed early (within 6–8 weeks), even with a low body weight.[18 ]
[23 ] An argument against early closure is the assumed risk of adhesions which might result
in a difficult operation. However, in patients treated for necrotizing enterocolitis,
there was no difference in the presence of adhesions between early and late closure
of stomas.[24 ] Within our own cohort, we could not provide evidence that early closure may also
lead to higher Z-scores at closure compared with nonearly closure. A reason could
be that early closure in our cohort was mostly performed due to stoma complications,
such as high-output or repeated prolapses, which might themselves have negatively
influenced growth. Still, we showed that early closure results in the same amount
of catch-up growth within a year following closure as in those nonearly closure. Since
early closure results in a significantly lower age at closure compared with nonearly
closure, we can at least say that it seems that early closure results in an early
shift to catch-up growth gaining weeks of advantage.
Besides growth impairment, other complications after stoma creation can occur such
as surgical site infections and high-output stomas.[3 ] Moreover, closing the stoma also leads to both short-term complications, such as
anastomotic leakage, and long-term morbidity, such as adhesion-related small bowel
obstruction and incisional hernia.[12 ]
[25 ] Taking into account the high risk of complications and the risk of growth impairment,
one might consider performing primary anastomosis instead of stoma creation with a
lower threshold. Primary anastomosis has been shown to be feasible in selected patients
treated for necrotizing enterocolitis or intestinal atresia.[12 ]
[26 ]
[27 ] Some situations, such as bowel perforation or meconium peritonitis, might necessitate
stoma creation, but the associated risk of morbidity should be taken into account
when deciding on whether or not to create a stoma.
In the presence of a stoma, oral sodium supplementation has been reported to improve
weight gain.[14 ]
[15 ]
[28 ] Supplementation will counter the loss of sodium, which is partly excreted via stoma
production, predominantly in small bowel stomas. However, sodium is also lost via
renal excretion which is most prominent in premature born children.[29 ] This might explain why patients with a colostomy in this study were sometimes also
found to be sodium depleted. Both the diagnosis and risk of sodium depletion in young
children with a stoma are poorly understood. However, young children with a low urine
sodium concentration (< 30 mmol/L) have been shown to gain significantly less weight
than those with normal urine sodium levels.[19 ] We could not verify these results in our cohort. There are currently no guidelines
for correct sodium supplementation in young children with a stoma, and there are only
small reports with suggested treatment protocols specifically for premature born neonates.[15 ] The lack of sufficient sodium supplementation in our cohort is indicating the need
for a clearly defined protocol for oral sodium supplementation in young children with
a stoma. An important part of such a protocol is how to evaluate the true body sodium
levels and what substrate to use. There are multiple possibilities opted, the best
method of which is suggested to be a 24-hour urine collection.[15 ] This method is often too burdensome for young children who recently underwent surgery,
and insertion of a urinary catheter would be required. Another suggested option is
to make use of serum sodium.[15 ] However, venipuncture for diagnosis is the primary cause for neonatal anemia, and
therefore, regular determination of serum sodium is not recommended.[30 ] In practice, urinary sodium concentration measured from a spot urine sample is an
acceptable, noninvasive, and inexpensive method. Still, the question is what level
of spot urine sodium reflects true sodium deficiency. It could be that a change in
definitions, for instance only defining inadequate supplementation after three measurements
of 30 mmol/L or lower, would prove a better reflection of the true sodium levels.
This could explain why we could not find a correlation between adequate supplementation
and positive growth and why it seemed that adequately supplemented children showed
a trend toward lower Z-scores at closure than nonadequately supplemented children,
although other explanations, such as delayed growth, might apply.
Limitations of this study are the retrospective design which resulted in exclusion
of a proportion of our cohort due to missing data regarding Z-scores. This might have
led to selection bias, for instance due to over/underinclusion of certain types of
diseases, and possibly type II errors, for instance in the evaluation of patients
receiving early closure. Also, patients were not randomly assigned to receive certain
treatments, such as early closure or major small bowel resection. This could have
resulted in allocation bias, possibly influenced by factors such as disease severity
or occurrence of stoma-related complications. Moreover, weight measurement was all
single measurement which could vary from day to day. Growth is a complex process affected
directly or indirectly by a multitude of interrelated factors which is why it is hard
to determine the exact etiology of growth impairment. Our results seem to show that
growth decreases in the presence of a stoma, which in most patients is only reversed
after stoma closure. It could be that other confounding factors, for instance diet,
might explain at least some of these changes in growth. Finally, due to the retrospective
nature of this study, we were limited in the factors we could retrieve. There are,
for instance, other manners of assessing nutritional status of patients such as weight
for height and middle upper arm circumference and other factors that could influence
weight such as fluid balance. We also could not retrieve information on refeeding,
which has been opted to have a positive effect on growth in neonates, specifically
prematures with low birth weight, treated with an intestinal stoma.[31 ]
Conclusion
A weighted decision on the creation of a stoma and timely stoma closure is important,
considering the negative impact that a stoma has on growth in the majority of children.
This impact might be decreased by preventing small bowel stomas when possible, specifically
those more proximal than 50 cm before Treitz, and limiting small bowel resection.
Moreover, most young children with a stoma do receive sodium supplementation, but
there is no guidance on optimal supplementation and in a large proportion the supplementation
seems to be inadequate. Since stoma closure seems essential in reversing the negative
effect seen in most patients with a stoma, we opt that early closure, especially in
children treated by small bowel stomas, results in an early shift to catch-up growth.
Since there are currently no guidelines focusing on the moment of stoma reversal as
well as sodium supplementation and monitoring in these patients, this demands future
attention.
