Low FODMAPs diet for functional abdominal pain disorders in children: critical review of current knowledge

Pensabene, Licia; Salvatore, Silvia; Turco, Rossella; Tarsitano, Flora; Concolino, Daniela; Baldassarre, Maria Elisabetta; Borrelli, Osvaldo; Thapar, Nikhil; Vandenplas, Yvan; Staiano, Annamaria; Saps, Miguel

doi:10.1016/j.jped.2019.03.004

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Review articles • J. Pediatr. (Rio J.) 95 (6) • Nov-Dec 2019 • https://doi.org/10.1016/j.jped.2019.03.004 copy

Low FODMAPs diet for functional abdominal pain disorders in children: critical review of current knowledge^☆ ☆ Please cite this article as: Pensabene L, Salvatore S, Turco R, Tarsitano F, Concolino D, Baldassarre ME, et al. Low FODMAPs diet for functional abdominal pain disorders in children: critical review of current knowledge. J Pediatr (Rio J). 2019;95:642-56. , ^☆☆ ☆☆ Study conducted at University Magna Graecia of Catanzaro, Department of Medical and Surgical Sciences, Catanzaro, Italy.

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ABSTRACT

Objective:

This narrative review aimed to provide practitioners a synthesis of the current knowledge on the role of a low Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols diet in reducing symptoms associated with functional abdominal pain disorders in children. This review is focused on the pathophysiology, efficacy and criticism of low Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols diet in children.

Sources:

Cochrane Database, Pubmed and Embase were searched using specific terms for Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols diet interventions and functional abdominal pain disorders.

Summary of the findings:

In children, only one Randomized Control Trial and one open-label study reported positive results of low Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols diet; one Randomized Control Trial showed exacerbation of symptoms with fructans in children with Irritable Bowel Syndrome; no effect was found for the lactose-free diet whilst fructose-restricted diets were effective in 5/6 studies.

Conclusions:

In children there are few trials evaluating low Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols in functional abdominal pain disorders, with encouraging data on the therapeutic efficacy particularly of fructose-restricted diet. Additional efforts are still needed to fill this research gap and clarify the most efficient way for tailoring dietary restrictions based on the patient's tolerance and/or identification of potential biomarkers of low Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols efficacy, to maintain nutritional adequacy and to simplify the adherence to diet by labeling Fermentable Oligosaccharides Disaccharides Monosaccharides and Polyols content in commercial products.

Keywords
Functional abdominal pain disorders; Fermentable oligosaccharides; Disaccharides; Monosaccharides; Polyol diet; Children

Nutrients	Low FODMAP content
Cereals	Gluten free products, rice, corn pasta, tortilla chips, quinoa, oats, polenta, sourdough, noodles
Milk products Cheese	Lactose free products, rice milk, soy milk, sorbets Hard cheeses, Cheddar, Parmesan, mozzarella, Swiss, firm tofu, tempeh, Brie, Camembert
Fruits	Bananas, cantaloupe, carambola, durian, honeydew melon, kiwi, orange, passion fruit, pawpaw, all berries (raspberries, blueberries, cranberries, strawberries) except than blackberries, tangelo, grapes, grapefruit, all nuts (except cashew and pistachios, and less than ten), almonds (less than 10), macadamia, olives, pumpkin seeds, flax and chia seeds, coconut, lemon, limes, papaya, rhubarb
Vegetables	Bamboo shoot, bok choy, capsicum, celery, chives, choko, choy sum, corn, eggplant, green bean, bean sprouts, lettuce, parsnip, pumpkin, silverbeet, tomato, potatoes, spring onion (green part only), garlic-infused oil, bell peppers, Swiss chard, carrots, spinach, zucchini, beet root (no more than four slices), broccoli (no more than 1/2 cup)
Legumes	Canned pumpkin, canned chickpeas, canned lentils
Sweeteners	Honeydew, golden syrup, maple syrup, glucose, sucrose (table sugar), aspartame, stevia, molasses, any sweeteners not containing fructose and not ending in "-ol"
References	Khan et al., 2015⁵⁴54 Khan MA, Nusrat S, Khan MI, Nawras A, Bielefeldt K. Low-FODMAP diet for irritable bowel syndrome: is it ready for prime time?. Dig Dis Sci. 2015;60:1169-77.; Barrett, 2017⁵⁵55 Barrett JS. How to institute the low-FODMAP diet. J Gastroenterol Hepatol. 2017;32:8-10.; Varney et al., 2017⁵⁶56 Varney J, Barrett J, Scarlata K, Catsos P, Gibson PR, Muir JG. FODMAPs: food composition, defining cutoff values and international application. J Gastroenterol Hepatol. 2017;32:53-61.; Monash University Low FODMAP Diet App., 2016⁵⁷57 Monash University Low FODMAP Diet app; 2016. Available from: http://www.med.monash.edu.au/cecs/gastro/fodmap/iphone-app.html [cited 27.03.19]. http://www.med.monash.edu.au/cecs/gastro... ; Canadian Digestive Health Foundation, 2019⁵⁸58 Digestive Health Foundation. Available from: http://www.CDHF.ca [cited 27.03.19]. http://www.CDHF.ca... ; Magge and Lembo, 2012⁵⁹59 Magge S, Lembo A. Low-FODMAP diet for treatment of irritable bowel syndrome. Gastroenterol Hepatol (NY). 2012;8:739-45.

Study	Methodology	Participants	Intervention	Duration of diet	Outcome measures and instruments	Key results
Chumpitazi et al., 2014⁹³93 Chumpitazi BP, Hollister EB, Oezguen N, Tsai CM, McMeans AR, Luna RA, et al. Gut microbiota influences low fermentable substrate diet efficacy in children with irritable bowel syndrome. Gut Microb. 2014;5:165-75.	Open-label prospective study	Children aged 7-17 years (n = 8) with IBS	Low FODMAP diet	7 days	Frequency of pain episodes; Instruments: Stool and Pain Diaries	Significantly (p < 0.05) reduction in pain frequency, pain severity, and pain-related interference with activities. > 50% decrease in abdominal pain frequency was obtained with the LFD in four children (50%) identified as responder
Chumpitazi et al., 2015⁹⁰90 Chumpitazi BP, Cope JL, Hollister EB, Tsai CM, McMeans AR, Luna RA, et al. Randomised clinical trial: gut microbiome biomarkers are associated with clinical response to a low FODMAP diet in children with irritable bowel syndrome. Aliment Pharmacol Ther. 2015;42:418-27.	Randomized, double-blind, cross-over study, with wash-out period	Children aged 7-17 years (n = 33) with IBS	Low FODMAP vs. TACD diet	2 days	Children pain episodes frequency; Instruments: Pain and Stool Diary	16 children were initially treated with the low FODMAP diet while 17 began with the TACD; children on low FODMAP reported a decrease in daily abdominal pain episodes vs. children on following TACD [1.1 ± 0.2 (SEM) vs. 1.7 ± 0.4 pain episodes per day, respectively; p < 0.05].
Chumpitazi et al., 2018¹⁰⁸108 Chumpitazi BP, McMeans AR, Vaughan A, Ali A, Orlando S, Elsaadi A, et al. Fructans exacerbate symptoms in a subset of children with irritable bowel syndrome. Gastroenterol Hepatol. 2018;16:219-25.	Double-blind placebo-controlled (maltodextrin) cross-over trial with wash-out	Children with mean age 12.4 + 2.2 years (n = 23) and IBS	Fructans or maltodextrin (0.5 g/kg; maximum, 19 g).	3 days	Children pain episodes frequency; Instruments: Pain and Stool and Food Diaries	The fructan-containing diet was associated with significantly more severe bloating and flatulence and more mean episodes of abdominal pain/day (3.4 - 2.6) compared to the maltodextrin-containing diet (2.4 - 1.7) (p < 0.01). More frequent abdominal pain while on the fructan-containing diet has been reported by 18 children (78.2%) and 12 (52.2%) qualified as fructan sensitive (defined as an increase of ≥30% abdominal pain frequency following fructan ingestion);
Däbritz et al., 2014¹²⁴124 Däbritz J, Mühlbauer M, Domagk D, Voos N, Henneböhl G, Siemer ML, et al. Significance of hydrogen breath tests in children with suspected carbohydrate malabsorption. BMC Pediatr. 2014;14:59.	Retrospective study	Children aged 3-18 years with RAP (n = 206)	Lactose, fructose and/or sorbitol restricted diet	longer than 12 months in 55 patients [47%]	Improvement of symptoms; Instruments: follow-up questionnaire	Sorbitol malabsorption has been diagnosed in 109/146 (75%) children; 27/31 (87%) had an improvement on a sorbitol-restricted diet. 55/142 (39%) children had fructose malabsorption. The number of children who specifically responded to a fructose-restricted diet is unclear, due to several patients in this cohort having multiple positive carbohydrate tests
Dearlove et al., 1983¹⁰⁹109 Dearlove J, Dearlove B, Pearl K, Primavesi R. Dietary lactose and the child with abdominal pain. Br Med J. 1983;286:1936102.	Prospective study	Children aged >3 years with RAP (n = 39)	Lactose restricted diet	2 weeks	Improvement of symptoms; Instruments: not specified	One-third of the children reported benefit from the lactose free diet, but no correlation was found with results of the lactose tolerance test, breath hydrogen estimation, or response to lactose challenges
Escobar et al., 2014¹³¹131 Escobar MA, Lustig D, Pflugeisen BM, Amoroso PJ, Sherif D, Saeed R, et al. Fructose intolerance/malabsorption and recurrent abdominal pain in children. J Pediatr Gastroenterol Nutr. 2014;58:498-501.	Retrospective study	Children aged 2- 19 years with RAP (n = 222)	Low-fructose diet	2 months (not clearly specify)	Improvement of symptoms; Instruments: Pain scale score	93/121 patients (76.9%) with BTH positive reported resolution of symptoms on a low-fructose diet (p < 0.0001) compared to 55/101 patients (54.4%) with negative BHT for fructose (p = 0.37).
Gijsbers et al., 2012¹²²122 Gijsbers CF, Kneepkens CM, Buller HA. Lactose and fructose malabsorption in children with recurrent abdominal pain: results of double-blinded testing. Acta Paediatr. 2012;101:e411-5.	Prospective study with DBPC test of provocation	Children aged 4-16 years with RAP (n = 220)	Low-lactose and/or fructose diet	3 days of provocation test	Resolution of abdominal pain with elimination, recurrence with provocation and disappearance with re- elimination; Instruments: not specified	Pain resolved upon elimination in 24/38 patients with lactose malabsorption, and in 32/49 with fructose malabsorption. A positive open provocation with lactose and fructose has been reported in 7/23 and 13/31 patients. DBPC provocation test done in 6/7 and 8/13 patients was negative in all, but a few children continued to report abdominal symptoms upon intake of milk or fructose.
Gomara et al., 2008¹²⁸128 Gomara RE, Halata MS, Newman LJ, Bostwick HE, Berezin SH, Cukaj L, et al. Fructose intolerance in children presenting with abdominal pain. J Pediatr Gastroenterol Nutr. 2008;47:303-8.	Prospective study	Children aged 7-17 years (n = 32) FGIDs	Low-fructose and low-sorbitol diet	2 weeks	Improvement in their GI symptoms; Instruments: not specified	9 of 11 patients (81%) with positive fructose breath test results, reported almost immediate improvement in GI symptoms but a significant reduction only for abdominal pain and bloating (p < 0.05)
Gremse et al., 2003¹¹¹111 Gremse DA, Greer AS, Vacik J, DiPalma JA. Abdominal pain associated with lactose ingestion in children with lactose intolerance. Clin Pediatr. 2003;42:341-5.	Randomized, double-blind, cross-over study	Children aged 3 -17 years with RAP (n = 30)	Lactose-hydrolyzed or lactose-containing milk	14 days	Improvement in their GI symptoms; Instruments: Daily diaries	A significant increase in abdominal pain was experienced by study participants during the lactose ingestion period when compared to the lactose-free period (total scores 7.5 + 2.7 vs. 4.1 + 1.4, p = 0.021)
Hammer et al., 2018¹³⁰130 Hammer V, Hammer K, Memaran N, Huber WD, Hammer K, Hammer J. Relationship between abdominal symptoms and fructose ingestion in children with chronic abdominal pain. Dig Dis Sci. 2018;63:1270-9.	Prospective trial	Children with RAP, with history suggestive of a possible association of symptoms with fructose ingestion (n = 82)	Fructose breath testing using: 1 g/kg body weight up to maximum of 25 g	-	Severity of clinical symptoms. Instruments: symptom questionnaire	A total of 33 children (40%) had malabsorption; fructose ingestion induced symptoms in 31 (38%), but only 15 (46%) with malabsorption were symptomatic; fructose malabsorption did not significantly correlate with fructose-induced symptoms; clinical symptoms correlated only with symptoms experienced during the breath test (p < 0.001, r ² = 0.21) but not with malabsorption (NS)
Iacovou et al., 2018⁹⁸98 Iacovou M, Mulcahy EC, Truby H, Barrett JS, Gibson PR, Muir JG. Reducing the maternal dietary intake of indigestible and slowly absorbed short-chain carbohydrates is associated with improved infantile colic: a proof-of-concept study. J Hum Nutr Diet. 2018;31:256-65.	Single-blind, open-label, interventional study.	Exclusively breastfeeding mothers and their infants aged 2-17 weeks who met the Wessel Criteria for infantile colic (n = 18)	Maternal low FODMAP diet	7 days	Infant crying-fussing durations (minutes), Instruments: Baby Day Diary	Infant crying-fussing durations fell by 73 [301-223] min (n = 13; p = 0.007), as well as crying episodes (p = 0.01) and fussing durations (p = 0.011). "Much more content" babies were reported at end of study by their mothers
Lebenthal et al., 1981¹¹⁰110 Lebenthal E, Rossi TM, Nord KS, Branski D. Recurrent abdominal pain and lactose absorption in children. Pediatrics. 1981;67:828-32.	Prospective study	Children aged 6-14 years (n = 69) RAP	Low-lactose diet	12 months	Improvement in RAP; Instruments: Symptoms Diary	Symptoms of RAP resolved in 40% lactose malabsorbers, in 38.4% lactose absorbers after 12 months of elimination diet and in 41.7% lactose absorbers following a regular diet.
Wintermeyer et al., 2012¹²⁹129 Wintermeyer P, Baur M, Pilic D, Schmidt-Choudhury A, Zilbauer M, Wirth S. Fructose malabsorption in children with recurrent abdominal pain: positive effects of dietary treatment. Klin Padiatr. 2012;224:17-21.	Prospective study	Children aged 3-14 years (n = 75) with RAP	Low-fructose and low-sorbitol diet	4 weeks	Improvement of frequency and intensity of abdominal pain; Instruments: nonstandard questionnaire	A median reduction of weekly pain frequency from a mean of 3.64 + 1.6 before diet to a mean of 1.46 + 1.4 (p < 0.001) under fructose restriction was reported. The median intensity of pain decreased from 6 (mean 5.83 + 2.0) before intervention to 3 (mean 3.4 + 2.5; p < 0.001) on diet. A significant improvement of daily stool frequency, nausea, sleep problems, missed school days was also reported on diet
Wirth et al., 2014⁹⁷97 Wirth S, Klodt C, Wintermeyer P, Berrang J, Hensel K, Langer T, et al. Positive or negative fructose breath test results do not predict response to fructose restricted diet in children with recurrent abdominal pain: results from a prospective randomized trial. Klin Padiatr. 2014;226:268-73.	Prospective, blinded randomized interventional trial	103 children with RAP: 51 restricted diet (group A), 52 standard diet (group B)	Fructose-restricted diet vs. standard diet	2 weeks	1. Pain intensity (measured by questionnaire) 2. Pain frequency (as above) 3. "Secondary symptoms score" (SSS) created from 8 parameters (nausea, vomiting, fatigue, sleep disturbance, headache, dizziness, anorexia, and use of pain relievers).	There was a significant decrease on pain score (from a median 5.5 to 4) in group A and no significant changes in group B (5.3-5) two weeks after intervention. Frequency of abdominal pain decreased in both groups but without significant difference, while SSS improved only in group A from median 6 to 3.5.

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[1] * Corresponding author. E-mail:pensabene@unicz.it (L. Pensabene).