Dual x-ray absorptiometry monitoring in pediatric short bowel syndrome: an integrative review

Blum, Angelica Godoi Romagnoli; Russo, Tais Daiene Hortencio; Nogueira, Roberto José Negrão

doi:10.1590/1984-0462/2024/42/2023064

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Brasil

Revista Paulista de Pediatria

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Brasil

Español English

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Sumário

Review Article • Rev. paul. pediatr. 42 • 2024 • https://doi.org/10.1590/1984-0462/2024/42/2023064 copy

Dual x-ray absorptiometry monitoring in pediatric short bowel syndrome: an integrative review

Monitorização por absortometria com duplo raio X na síndrome do intestino curto pediátrica: uma revisão integrativa

Authorship SCIMAGO INSTITUTIONS RANKINGS

ABSTRACT

Objective:

To analyze the bone health of pediatric patients with short bowel syndrome intestinal failure (SBS-IF).

Data source:

An integrative literature review was performed using the data published in the MEDLINE-PubMed and Scientific Electronic Library Online (SciELO) databases between January 2010 and April 2021, and through a manual search of the reference lists of relevant studies. Studies were included if they assessed bone mineral density by the Dual X-Ray Absorptiometry (DXA) technique, incorporated pediatric patients (up to 20 years of age) with SBS under parenteral nutrition (PN) and were written in English. Eleven primary sources met the inclusion criteria for this study.

Data synthesis:

Pediatric patients with SBS-IF under long-term parenteral nutrition experienced frequent changes in bone metabolism, leading to osteoporotic fractures and growth failure. These patients have deficiencies in multiple nutrients, such as calcium, magnesium, phosphorus, and vitamin D. Consequently, there are variations in the secretion and regulation of the parathyroid hormone. In addition, the pharmacotechnical limitations related to calcium and phosphorus in the PN solution, use of glucocorticoids, and difficulty performing physical activity are risk factors for the development of metabolic bone disease in pediatric patients with SBS-IF.

Conclusions:

Low bone mineral density was associated with a high risk of developing osteoporosis, fractures, and growth deficiency in pediatric patients with SBS-IF on PN therapy in the long term.

Keywords:
Intestinal failure; Pediatric; Parenteral nutrition; Absorptiometry, photon

	Criteria	Appleman et al.²⁰20 Appleman SS, Kalkwarf HJ, Dwivedi A, Heubi JE. Bone deficits in parenteral nutrition-dependent infants and children with intestinal failure are attenuated when accounting for slower growth. J Pediatr Gastroenterol Nutr. 2013;57:124-30. https://doi.org/10.1097/MPG.0b013e318291fec5 https://doi.org/10.1097/MPG.0b013e318291...	Demehri et al.¹⁶16 Demehri FR, Simha S, Stephens L, Harris MB, Arnold MA, Brown PI, et al. Pediatric intestinal failure: predictors of metabolic bone disease. J Pediatr Surg. 2015;50:958-62. https://doi.org/10.1016/j.jpedsurg.2015.03.018 https://doi.org/10.1016/j.jpedsurg.2015....	Diamanti et al.¹³13 Diamanti A, Bizzarri C, Basso MS, Gambarara M, Cappa M, Daniele A, et al. How does long-term parenteral nutrition impact the bone mineral status of children with intestinal failure? J Bone Miner Metab. 2010;28:351-8. https://doi.org/10.1007/s00774-009-0140-0 https://doi.org/10.1007/s00774-009-0140-...	Khan et al.²⁴24 Khan FA, Fisher JG, Bairdain S, Sparks EA, Zurakowski D, Modi BP, et al. Metabolic bone disease in pediatric intestinal failure patients: prevalence and risk factors. J Pediatr Surg. 2015;50:136-9. https://doi.org/10.1016/j.jpedsurg.2014.10.010 https://doi.org/10.1016/j.jpedsurg.2014....	Kvammen et al.²⁵25 Kvammen JA, Thomassen RA, Kjeserud CN, Sæland C, Godang K, Bollerslev J, et al. Bone mineral density and vitamin D in paediatric intestinal failure patients receiving home parenteral nutrition. Clin Nutr ESPEN. 2020;39:234-41. https://doi.org/10.1016/j.clnesp.2020.06.006 https://doi.org/10.1016/j.clnesp.2020.06...	Louazon et al.²¹21 Louazon T, Poinsot P, Restier L, Belmalih A, Loras-Duclaux I, Marotte S, et al. A prospective case-control pilot study to evaluate bone microarchitecture in children and teenagers on long-term parenteral nutrition using HR-pQCT. Sci Rep. 2021;11:9151. https://doi.org/10.1038/s41598-021-88366-6 https://doi.org/10.1038/s41598-021-88366...	Mutanen et al.²²22 Mutanen A, Mäkitie O, Pakarinen MP. Risk of metabolic bone disease is increased both during and after weaning off parenteral nutrition in pediatric intestinal failure. Horm Res Paediatr. 2013;79:227-35. https://doi.org/10.1159/000350616 https://doi.org/10.1159/000350616...	Nader et al.²³23 Nader EA, Lambe C, Talbotec C, Acramel A, Pigneur B, Goulet O. Metabolic bone disease in children with intestinal failure is not associated with the level of parenteral nutrition dependency. Clin Nutr. 2021;40:1974-82. https://doi.org/10.1016/j.clnu.2020.09.014 https://doi.org/10.1016/j.clnu.2020.09.0...	Olieman et al.¹⁴14 Olieman JF, Penning C, Spoel M, Ijsselstijn H, van den Hoonaard TL, Escher JC, et al. Long-term impact of infantile short bowel syndrome on nutritional status and growth. Br J Nutr. 2012;107:1489-97. https://doi.org/10.1017/S0007114511004582 https://doi.org/10.1017/S000711451100458...	Pichler et al.¹²12 Pichler J, Chomtho S, Fewtrell M, Macdonald S, Hill SM. Growth and bone health in pediatric intestinal failure patients receiving long-term parenteral nutrition. Am J Clin Nutr. 2013;97:1260-9. https://doi.org/10.3945/ajcn.112.057935 https://doi.org/10.3945/ajcn.112.057935...	Poinsot et al.⁹9 Poinsot P, Geoffroy P, Braillon P, Denis A, Loras-Duclaux I, Marotte S, et al. Longitudinal bone mineralization assessment in children treated with long-term parenteral nutrition for severe intestinal failure. JPEN J Parenter Enteral Nutr. 2018;42:613-22. https://doi.org/10.1177/0148607117701399 https://doi.org/10.1177/0148607117701399...
1	Aims and objectives clearly stated	+		+	+	+	+	+	+	+	+	+
2	Hypothesis/research questions clearly specified	+	+	+	+	+	+	+	+	+	+	+
3	Dependent and independent variables clearly stated	+	+	+	+	+	+	+	+	+	+	+
4	Variables operationalized	+	+			+	+		+	+		+
5	Design adequately described		+	+	+	+	+	+	+	+	+	+
6	Appropriate methods	+	+	+	+	+	+	+	+		+	+
7	Instruments used tested for reliability and validity	+	+	+	+	+	+	+	+	+	+	+
8	Source of sample, inclusion/exclusion, and response rates described	+	+	+	+	+	+	+	+	+	+	+
9	Statistical errors discussed									+		+
10	Ethical considerations	+		+	+	+		+	+	+	+	+
11	Was the piloted study						+
12	Statistically appropriate analysis	+	+	+	+	+	+	+	+		+	+
13	Results reported and clear	+	+	+	+	+	+	+	+	+	+	+
14	Results reported related to hypothesis and literature	+	+	+	+	+	+	+	+	+	+	+
15	Limitations reported	+	+	+	+	+	+	+		+		+
16	Conclusions do not go beyond limit of data and results		+				+			+
17	Findings able to be generalized								+
18	Implications discussed	+	+	+	+	+	+	+	+	+	+	+
19	Existing conflict of interest with sponsor					+
20	Data available for scrutiny and reanalysis	+	+	+	+	+	+	+	+	+	+	+

Author/Country	Type of study	Study period	N	Results/findings
Appleman et al.²⁰20 Appleman SS, Kalkwarf HJ, Dwivedi A, Heubi JE. Bone deficits in parenteral nutrition-dependent infants and children with intestinal failure are attenuated when accounting for slower growth. J Pediatr Gastroenterol Nutr. 2013;57:124-30. https://doi.org/10.1097/MPG.0b013e318291fec5 https://doi.org/10.1097/MPG.0b013e318291... /USA	Cross-sectional	Not reported	20	Vitamin D deficiency, growth retardation
Demehri et al.¹⁶16 Demehri FR, Simha S, Stephens L, Harris MB, Arnold MA, Brown PI, et al. Pediatric intestinal failure: predictors of metabolic bone disease. J Pediatr Surg. 2015;50:958-62. https://doi.org/10.1016/j.jpedsurg.2015.03.018 https://doi.org/10.1016/j.jpedsurg.2015.... /USA	Retrospective, cohort	2006–2012	36	Fractures, bone pain, vitamin D deficiency^* * No statistical significance. , hyperparathyroidism
Diamanti et al.¹³13 Diamanti A, Bizzarri C, Basso MS, Gambarara M, Cappa M, Daniele A, et al. How does long-term parenteral nutrition impact the bone mineral status of children with intestinal failure? J Bone Miner Metab. 2010;28:351-8. https://doi.org/10.1007/s00774-009-0140-0 https://doi.org/10.1007/s00774-009-0140-... /Italy	Longitudinal prospective	2005–2007	24	Fractures
Khan et al.²⁴24 Khan FA, Fisher JG, Bairdain S, Sparks EA, Zurakowski D, Modi BP, et al. Metabolic bone disease in pediatric intestinal failure patients: prevalence and risk factors. J Pediatr Surg. 2015;50:136-9. https://doi.org/10.1016/j.jpedsurg.2014.10.010 https://doi.org/10.1016/j.jpedsurg.2014.... /USA	Retrospective, cohort	2004–2013	65	Vitamin D deficiency^* * No statistical significance. , hyperparathyroidism
Kvammen et al.²⁵25 Kvammen JA, Thomassen RA, Kjeserud CN, Sæland C, Godang K, Bollerslev J, et al. Bone mineral density and vitamin D in paediatric intestinal failure patients receiving home parenteral nutrition. Clin Nutr ESPEN. 2020;39:234-41. https://doi.org/10.1016/j.clnesp.2020.06.006 https://doi.org/10.1016/j.clnesp.2020.06... /Norway	Observational cross-sectional	2007 (March to September)	69	Impaired growth
Louazon et al.²¹21 Louazon T, Poinsot P, Restier L, Belmalih A, Loras-Duclaux I, Marotte S, et al. A prospective case-control pilot study to evaluate bone microarchitecture in children and teenagers on long-term parenteral nutrition using HR-pQCT. Sci Rep. 2021;11:9151. https://doi.org/10.1038/s41598-021-88366-6 https://doi.org/10.1038/s41598-021-88366... /France	Cross-sectional, case-control	March 2014 to June 2015	11and 22 (patients and controls)	No diferences for bone densities in patients undergoing chronic PN
Mutanen et al.²²22 Mutanen A, Mäkitie O, Pakarinen MP. Risk of metabolic bone disease is increased both during and after weaning off parenteral nutrition in pediatric intestinal failure. Horm Res Paediatr. 2013;79:227-35. https://doi.org/10.1159/000350616 https://doi.org/10.1159/000350616... /Finland	Cross-sectional	1984–2010	41	Fractures, vitamin D deficiency, hyperparathyroidism
Nader et al.²³23 Nader EA, Lambe C, Talbotec C, Acramel A, Pigneur B, Goulet O. Metabolic bone disease in children with intestinal failure is not associated with the level of parenteral nutrition dependency. Clin Nutr. 2021;40:1974-82. https://doi.org/10.1016/j.clnu.2020.09.014 https://doi.org/10.1016/j.clnu.2020.09.0... /France	Single center retrospective, cross-sectional	January 2016 to December 2018	40	Bone fractures^* * No statistical significance. after a mild trauma, and vitamin D deficiency^* * No statistical significance.
Olieman et al.¹⁴14 Olieman JF, Penning C, Spoel M, Ijsselstijn H, van den Hoonaard TL, Escher JC, et al. Long-term impact of infantile short bowel syndrome on nutritional status and growth. Br J Nutr. 2012;107:1489-97. https://doi.org/10.1017/S0007114511004582 https://doi.org/10.1017/S000711451100458... /Netherlands	Cross-sectional	2005–2007	31	Short stature
Pichler et al.¹²12 Pichler J, Chomtho S, Fewtrell M, Macdonald S, Hill SM. Growth and bone health in pediatric intestinal failure patients receiving long-term parenteral nutrition. Am J Clin Nutr. 2013;97:1260-9. https://doi.org/10.3945/ajcn.112.057935 https://doi.org/10.3945/ajcn.112.057935... /Austria	Prospective, cohort	2002–2010	12	Short stature
Poinsot et al.⁹9 Poinsot P, Geoffroy P, Braillon P, Denis A, Loras-Duclaux I, Marotte S, et al. Longitudinal bone mineralization assessment in children treated with long-term parenteral nutrition for severe intestinal failure. JPEN J Parenter Enteral Nutr. 2018;42:613-22. https://doi.org/10.1177/0148607117701399 https://doi.org/10.1177/0148607117701399... /France	Retrospective, cohort	2004–2014	31	Vitamin D deficiency

Author	Age	BMD	Time of PN	DXA assessments and time after weaned off PN
Appleman et al.²⁰20 Appleman SS, Kalkwarf HJ, Dwivedi A, Heubi JE. Bone deficits in parenteral nutrition-dependent infants and children with intestinal failure are attenuated when accounting for slower growth. J Pediatr Gastroenterol Nutr. 2013;57:124-30. https://doi.org/10.1097/MPG.0b013e318291fec5 https://doi.org/10.1097/MPG.0b013e318291...	Median: 26 Min-Max (6–127) months	Lumbar (15%), Total (12%), ↓ in IF than the control group	Median: 18.5 Min-Max (4–103) months	Not reported
Demehri et al.¹⁶16 Demehri FR, Simha S, Stephens L, Harris MB, Arnold MA, Brown PI, et al. Pediatric intestinal failure: predictors of metabolic bone disease. J Pediatr Surg. 2015;50:958-62. https://doi.org/10.1016/j.jpedsurg.2015.03.018 https://doi.org/10.1016/j.jpedsurg.2015....	≥6 years and diagnosed until 18 years	Lumbar: Mean±SD: -1.36±1.47 First DXA Mean±SD: -1.36±1.18 Second DXA	Mean±SD: 5.1±5.4 years	Not reported
Diamanti et al.¹³13 Diamanti A, Bizzarri C, Basso MS, Gambarara M, Cappa M, Daniele A, et al. How does long-term parenteral nutrition impact the bone mineral status of children with intestinal failure? J Bone Miner Metab. 2010;28:351-8. https://doi.org/10.1007/s00774-009-0140-0 https://doi.org/10.1007/s00774-009-0140-...	Mean±SD: (5.1±2.9) years	Total Mean±SD: -2.5±1.2^* * p<0.001	Mean±SD: 32.4±28.8 months	Not reported
Khan et al.²⁴24 Khan FA, Fisher JG, Bairdain S, Sparks EA, Zurakowski D, Modi BP, et al. Metabolic bone disease in pediatric intestinal failure patients: prevalence and risk factors. J Pediatr Surg. 2015;50:136-9. https://doi.org/10.1016/j.jpedsurg.2014.10.010 https://doi.org/10.1016/j.jpedsurg.2014....	≥5 to 20 years	DXA less or equal–2 Mean±SD: 1772.9±1453.7 DXA greater–2 Mean±SD: 1126.1±1194.3 p=0.09 ↓ 22 childrens (22/65)–40%	Mean±SD: 44.2± 43.2 (unity)	DXA less or equal – 2 Mean±SD: 2127.9±1921.9 DXA greater – 2 Mean±SD: 2187.2±1300.0 p=0.92 32 days
Kvammen et al.²⁵25 Kvammen JA, Thomassen RA, Kjeserud CN, Sæland C, Godang K, Bollerslev J, et al. Bone mineral density and vitamin D in paediatric intestinal failure patients receiving home parenteral nutrition. Clin Nutr ESPEN. 2020;39:234-41. https://doi.org/10.1016/j.clnesp.2020.06.006 https://doi.org/10.1016/j.clnesp.2020.06...	Mean±SD: 10.1±3.5 years	Total median: -0.4 and Lumbar: -0.9	>6 months	Not reported
Louazon et al.²¹21 Louazon T, Poinsot P, Restier L, Belmalih A, Loras-Duclaux I, Marotte S, et al. A prospective case-control pilot study to evaluate bone microarchitecture in children and teenagers on long-term parenteral nutrition using HR-pQCT. Sci Rep. 2021;11:9151. https://doi.org/10.1038/s41598-021-88366-6 https://doi.org/10.1038/s41598-021-88366...	Median: 16 Min-Max (9–19) years	Spine total: Median (Min-Max) and BMC (g): 40 (14–66) and BMD (g/cm²): 0.8 (0.4–0.9) and Whole body: Median (Min-Max) BMC (g): 1198 (441–1832) and BMD (g/cm²): 0.81 (0.54–0.96)	Median: 10.3 Min-Max (6.4–18.3) years	Not reported
Mutanen et al.²²22 Mutanen A, Mäkitie O, Pakarinen MP. Risk of metabolic bone disease is increased both during and after weaning off parenteral nutrition in pediatric intestinal failure. Horm Res Paediatr. 2013;79:227-35. https://doi.org/10.1159/000350616 https://doi.org/10.1159/000350616...	Mean: 9.9 Min-Max (0.2–27^† † adults with infantile SBS ) years	Lumbar: Mean: -2.1 Min-Max (-4.1–0.9) Femur: Mean: -0.9 Min-Max (-2.7–1.1)	Mean: 41 Min-Max (0.7–250) months	Lumbar: Mean: -1.2 Min-Max (-3.2–0.9). Femur: Mean: -0.8 Min-Max (-2.6–0.7) 9.0 years min-max (0.3–27)
Nader et al.²³23 Nader EA, Lambe C, Talbotec C, Acramel A, Pigneur B, Goulet O. Metabolic bone disease in children with intestinal failure is not associated with the level of parenteral nutrition dependency. Clin Nutr. 2021;40:1974-82. https://doi.org/10.1016/j.clnu.2020.09.014 https://doi.org/10.1016/j.clnu.2020.09.0...	Mean±SD: 12.4±4.5 years Median: 12.2 years	BMI mean±SD: -0.5±1.3 – Median: -0.4 BMI ≤-2 SD [n(%)]: 7 (18)	Mean±SD: 12.4±4.4 years Median: 12.4 years	Not reported
Olieman et al.¹⁴14 Olieman JF, Penning C, Spoel M, Ijsselstijn H, van den Hoonaard TL, Escher JC, et al. Long-term impact of infantile short bowel syndrome on nutritional status and growth. Br J Nutr. 2012;107:1489-97. https://doi.org/10.1017/S0007114511004582 https://doi.org/10.1017/S000711451100458...	Mean±SD: 11.8±4.2) years	Total: Mean±SD: -0.04±1.4 and Lumbar: Mean±SD: -0.47±1.2 – BMC: Mean±SD: -1.0±1.1	Median: 110 Min-Max (43–2345) days	Not reported
Pichler et al.¹²12 Pichler J, Chomtho S, Fewtrell M, Macdonald S, Hill SM. Growth and bone health in pediatric intestinal failure patients receiving long-term parenteral nutrition. Am J Clin Nutr. 2013;97:1260-9. https://doi.org/10.3945/ajcn.112.057935 https://doi.org/10.3945/ajcn.112.057935...	5 to 14 years	Total: Mean±SD: -1.3±1	Median: 4.5 Min-Max (2–11.4) years	Not reported
Poinsot et al.⁹9 Poinsot P, Geoffroy P, Braillon P, Denis A, Loras-Duclaux I, Marotte S, et al. Longitudinal bone mineralization assessment in children treated with long-term parenteral nutrition for severe intestinal failure. JPEN J Parenter Enteral Nutr. 2018;42:613-22. https://doi.org/10.1177/0148607117701399 https://doi.org/10.1177/0148607117701399...	Median 2.9 Min-Max (0.40–13.3) years	TBMC^‡ ‡ Low bone mass was defined by a TBMC z score ≤-2). Median: -1.9(-5.3 to 2.6) – first DXA TBMC^‡ ‡ Low bone mass was defined by a TBMC z score ≤-2). : Median: -1.14(-2.25 to 1.84) – Last DXA	Median: 2.7 Min-Max (0.1–12.7) years	Not reported

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[1] Corresponding author: E-mail: a.romagnoli@hotmail.com (A. G. R. Blum)