Efficacy of Dietary Therapy for Eosinophilic Esophagitis in Children and Adults: An Updated Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Protocol
2.2. Selection of Studies and Search Strategy
2.3. Inclusion and Exclusion Criteria
2.4. Data Extraction
2.5. Risk of Bias Assessment
2.6. Study Outcomes and Statistical Analysis
2.7. Subgroup Analysis
2.8. Certainty of Evidence
3. Results
3.1. Literature Search Results and Characteristics of Included Documents
3.2. Risk of Bias and Quality Assessment
First Author, Publication Years | Design | Period | Country | N Patients (Complete Diet) | Population | Male/Female (%) | Dietary Treatment | Diet Duration (Weeks) | N Histologic Responders (%) | N. Clinical Responders (%) | Clinical Response Method |
---|---|---|---|---|---|---|---|---|---|---|---|
Kelly et al., 1995 [23] | Prospective | 1992–1994 | USA | 10 | Children/Adolescents (0–12.5) | 60/40 | Elemental | At least 6 | 9/10 (90%) | 10/10 (100%) | Symptom improvement |
Liacouras C et al., 2005 [24] | Retrospective | 1994–2004 | USA | 239 | Children | 74.5/25.5 | Allergy-test directed diet (SPT, APT) | 4–6 | 18/75 (24%) | 18/75 (24%) | Symptom improvement |
Elemental | 4–6 | 160/164 # (97.6%) | 160/164 # (97.6%) | Symptom improvement | |||||||
Kagalwalla AF et al., 2006 [25] | Retrospective | 2001–2005 | USA | 60 | Children | 80/20 | SFED | 6 | 26/35 (74.3%) | 32/35 (91.4%) | Symptom improvement |
Elemental | 6 | 22/25 (88%) | 25/25 (100%) | Symptom improvement | |||||||
Quaglietta et al., 2007 [26] | Prospective | 2005–2006 | Italy | 7 | Children | - | Allergy-test directed diet (SPT, APT) | 24 | 0/7 (0%) | - | Symptom improvement |
Kewalramani et al., 2009 [55] | Prospective | - | USA | 13 | Children/Adolescents (1–19) | - | Allergy-test directed diet (SPT, ImmunoCAP) | 12 | 6/13 (46.1%) | - | - |
Hiremath G et al., 2010 [56] | Retrospective | - | USA | 13 | Children | 70/30 | Allergy-test directed diet (SPT, APT) | - | 8/13 (61.5%) | - | - |
Muir RJ et al., 2010 [57] | Prospective | - | Australia | 13 | Children/Adolescents (1–15) | 84.6/15.4 | SFED | 6 | 5/13 (38.5%) | 13/13 (100%) | Symptom improvement |
Rizo-Pascual JM et al., 2011 [27] | Prospective | 2001–2009 | Spain | 17 (14) | Children (2.8–14.5) | 82.4/17.6 | Elemental | 8 | 3/3 (100%) | 3/3 (100%) | Asymptomatic |
Allergy-test directed diet (IgE, SPT) | 8 | 5/11 (45.4%) | 5/11 (45.4%) | Asymptomatic | |||||||
Gonsalves N et al., 2012 [6] | Prospective | 2006–2010 | USA | 50 | Adolescents/Adults (19–76) | 50/50 | SFED | 6 | 37/50 (74%) | 47/50 (94%) | Dysphagia resolution |
Henderson C et al., 2012 [28] | Retrospective | 1999–2011 | USA | 95 | Children/Adolescents (<21) | 77.9/22.1 | Elemental | 12 | 47/49 (95.9%) | - | - |
SFED | 12 | 21/26 (80.8%) | |||||||||
Allergy-test directed diet (SPT, APT) | 12 | 15/23 (65.2%) | |||||||||
Kagalwalla AF et al., 2012 [29] | Retrospective | 2006–2011 | USA | 111 | Children | - | Allergy-test directed diet | 6 | 52/82 (63.4%) | - | Symptom improvement |
Elemental | 6 | 10/12 (83.3%) | - | ||||||||
OFED (milk) | 6 | 11/17 (64.7%) | - | ||||||||
Molina Infante J et al., 2012 [30] | Prospective | - | Spain | 22 | Adolescents/Adults (>18) | 77.3/22.7 | Allergy-test directed diet (SPT, PPT, APT) | 6 | 4/15 # (26.7%) | 4/15 (26.7%) | Symptom improvement |
Spergel J et al., 2012 [31] | Retrospective | 2000–2011 | USA | 470 | Children | - | Elemental | - | 144/151 (95.4%) | - - | - - |
Allergy-test directed diet (IgE, SPT, APT) | - | 169/319 (53%) | |||||||||
Al-Hussaini A et al., 2013 [32] | Retrospective | 2009–2012 | Saudi Arabia | 13 | Children | 61.5/38.5 | Elemental | 8 | 3/3 (100%) | - | - |
Allergy-test directed diet (SPT, RAST) | 8 | 4/10 (40%) | |||||||||
Gonsalves N et al., 2013 [58] | Prospective | - | USA | 28 | Both | FFED | 6 | 15/28 (53.6%) | - | Symptom improvement | |
Lucendo AJ et al., 2013 [7] | Prospective | 2008–2010 | Spain | 67 | Adolescents/Adults (17–60) | 82.1/17.9 | SFED | 6 | 49/67 (73.1%) | 67/67 (100%) | Symptom improvement |
Peterson et al., 2013 [33] | Prospective | 2009–2011 | USA | 18 | Adolescents/Adults (19–58) | 55.6/44.4 | Elemental | 2–4 | 17/18 (94.4%) | - | Symptom improvement |
Colson D et al., 2014 [34] | Retrospective | 2006–2012 | France | 59 | Children | 62.7/37.8 | SFED + AAF | 8 | 35/51 (68.6%) | 58/59 (98.3%) | Symptom improvement |
SFED | 8 | 6/8 (75%) | |||||||||
Molina-Infante J et al., 2014 [8] | Prospective | 2012–2014 | Spain | 52 | Adolescents/Adults (>14) | 63.5/36.5 | FFED | 6 | 28/52 (53.8%) | 35/52 (67.3%) | DSS |
SFED | 6 | 34/47 (72.3%) | |||||||||
Rodríguez-Sánchez J et al., 2014 [35] | Prospective | 2011–2013 | Spain | 17 | Adolescents/Adults (>14) | 76.5/23.5 | SFED | 6 | 9/17 (52.9%) | - | VAS-EoE score |
Wolf WA et al., 2014 [36] | Retrospective | 2006–2012 | USA | 31 | Adolescents/Adults (>18) | 48.4/51.6 | Allergy-test directed diet (SPT) | 6 | 6/19 (31.6%) | 15/22 (68.2%) | Symptom improvement |
SFED | 6 | 5/9 (55.6%) | 7/9 (77.8%) | ||||||||
Homan M et al., 2015 [37] | Retrospective | 2005–2012 | Slovenia | 25 | Children/Adolescents (0–18) | 92/8 | SFED | - | 8/13 (61.5%) | 9/13 (69.2%) | Asymptomatic |
Allergy-test directed diet (IgE, SPT, APT) | - | 9/19 (47.4%) | 10/19 (52.6%) | ||||||||
Elemental | - | 1/1 (100%) | - | ||||||||
Leung J et al., 2015 [38] | Retrospective | - | USA | 100 (34) | Children/Adolescents (8–18) | 78/22 | OFED (milk) | 8 | 13/22 (59.1%) | - | - |
Elemental | 8 | 12/12 (100%) | |||||||||
van Rhijn B et al., J 2015 [39] | Prospective | - | Netherlands | 15 | Adults | 86.7/13.3 | Allergy-test directed diet (microarray) | 6 | 1/15 (6.7%) | - | - |
Philpott H et al., 2016 [40] | Prospective | 2013–2015 | Australia | 56 | Adolescents/Adults (>18) | 67.9/32.1 | SFED | At least 2 | 29/56 (51.8%) | - | - |
Constantine G et al., 2017 [41] | Retrospective | 2006–2012 | USA | 14 | Adolescents/Children | 85.7/14.3 | Allergy-test directed diet (APT, SPT) | At least 12 | 6/10# (60%) | 9/14 (64%) | Symptom improvement |
Kagalwalla AF et al., 2017 [9] | Prospective | 2011–2016 | USA | 78 | Children/Adolescents (<18) | 66.7/33.3 | FFED | 6–8 | 50/78 (64.1%) | - | |
Molina-Infante J et al., 2017 [42] | Prospective | 2014–2016 | Spain | 130 | Both | 72.3/27.7 | TFED | 6 | 56/130 (43.1%) | 98/130 (75.4%) | DSS |
FFED | 6 | 66/110 (60%) | |||||||||
SFED | 6 | 74/93 (79.6%) | |||||||||
Reed C et al., 2017 [43] | Retrospective | 2008–2017 | USA | 52 (50) | Adolescents/Adults (>18) | 59.6/40.4 | SFED | - | 8/18 (44.4%) | 38/52 (73.1%) | Dysphagia resolution |
Allergy-test directed diet (SPT, RAST) | - | 11/32 (34.4%) | |||||||||
Warners MJ et al., 2017 [44] | Prospective | 2014–2015 | Netherlands | 21 (17) | Adults | 70.6/29.4 | Elemental | 4 | 12/17 (70.6%) | 17/17 (100%) | SDI and RDQ |
Eckmann JD et al., 2018 [45] | Prospective | 2014–2016 | USA | 8 | Adults | 50/50 | SFED * | 6 | 7 (1 *)/8 (87.5%) | 8/8 (100%) | MDQ-30 |
Dellon ES et al., 2019 [46] | Prospective | - | USA | 43 | Adolescents/Adults (>18) | - | SFED | 6 | 15/24 (62.5%) | - | - |
Allergy-test directed diet (IgG4) | 6 | 4/19 (21.1%) | |||||||||
Kliewer K et al., 2019 [59] | Prospective RCT | - | USA | 63 | Children/Adolescents (6–17) | - | OFED (milk) | 12 | 15/34 # (44.1%) | - | PEESS V2.0 |
FFED | 12 | 7/17 # (41.2%) | |||||||||
Teoh T et al., 2019 [47] | Retrospective | 2013–2016 | Canada | 31 | Children/Adolescents (<16) | 83.9/16.1 | OFED (milk) | 8 | 18/31 (58.1%) | 28/31 (90.3%) | Symptom improvement |
Iglesia E et al., 2020 [48] | Retrospective | - | USA | 8 | Adolescents/Adults (12–67) | 22/78 | TFED | 6–8 | 2/2 (100%) | 7/8 (78%) | - |
FFED | 6–8 | 3/3 (100%) | |||||||||
SFED | 6–8 | 6/8 (75%) | |||||||||
Wong J et al., 2020 [49] | Retrospective | - | USA | 152 (21) | Children/Adolescents (<21) | 76.3/23.7 | OFED (dairy) | - | 3/12 (25%) | - | - |
SFED | - | 5/9 (55.6%) | |||||||||
de Rooij WE et al., 2022 [50] | Prospective RCT | 2017–2020 | Netherlands | 41 | Adults | 64/40 | FFED | 6 | 5/20 (25%) | - | SDI |
FFED + AAF | 6 | 10/21 (47.6%) | |||||||||
Wang L et al., 2022 [51] | Retrospective | 2012–2019 | USA | 68 | Adolescents/Adults (>18) | 52.9/47.1 | SFED * | 6 | 42 (4 *)/68 (55.9%) | - | - |
Wechsler JB et al., 2022 [11] | Prospective | 2012–2017 | USA | 41 | Children/Adolescents (2–18) | 75.6/24.4 | OFED (milk) | 8–12 | 21/41 (51.2%) | 37/41 (90.2%) | - |
Zalewski A et al., 2022 [52] | Retrospective | 2006–2021 | USA | 213 | Adolescents/Adults | 54/46 | SFED * | 6 | 123 (8 *)/213 (57.7%) | 164/213 (77%) | Symptom improvement |
Alexander JA et al., 2023 [53] | Prospective | 2016–2018 | USA | 40 | Adolescents/Adults (18–65) | - | SFED * | 6 | 30 (2 *)/40 (75%) | - | EEsAI PRO |
Kliewer K et al., 2023 [12] | Prospective RCT | 2016–2019 | USA | 129 | Adolescents/Adults (>18) | 54.3/45.7 | OFED (milk) | 6 | 23/67 (34.3%) | - | EEsAI PRO |
SFED | 6 | 25/62 (40.3%) | |||||||||
Visaggi P et al., 2023 [54] | Retrospective | 2017–2022 | Italy & UK | 58 | Adults (>18) | SFED | 6 | 33/58 (56.9%) | 21/28 (75%) | Symptoms improvement |
3.3. Effectiveness of Dietary Interventions to Induce Histologic Remission of EoE
3.3.1. Elemental Diet
3.3.2. Empiric Six-Food Elimination Diet (SFED)
3.3.3. Empiric Four-Food Elimination Diet (FFED)
3.3.4. Empiric Two Food Elimination Diet (TFED)
3.3.5. One-Food Elimination Diet (OFED) (Milk Avoidance)
3.3.6. Allergy Testing-Directed Food Elimination Diet
3.4. Subgroup and Sensitivity Analyses
3.5. Effectiveness of Dietary Interventions on Symptomatic Improvement of EoE
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
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Dietary Treatment | N | Patients (n) | Overall Efficacy (%, 95% CI) | I2 | Publication Bias † | |
---|---|---|---|---|---|---|
Any dietary treatment | 66 | 2825 | 60.6% (54.6–66.5%) | 90% | 0.106 | |
Exclusive feeding with an elemental diet | 12 | 465 | 94.5% (92.3–96.4%) | 39.8% | 0.582 | |
Six-food elimination diet | 22 | 993 | 63.9% (58.5–69.2%) | 63.6% | 0.572 | |
Four-food elimination diet | 7 | 329 | 54.7% (45.7–63.6%) | 57.5% | 0.965 * | |
Two-food elimination diet | 2 | 132 | 44.3% (36.1–52.8%) ‡ | - | - | |
One-food (milk) elimination diet | 7 | 224 | 46.4% (40–52.9%) ‡ | 49.8% | 0.326 * | |
Allergy testing-directed food elimination | 16 | 682 | 39.5% (30.3–49.2%) | 78.8% | 0.787 | |
Subgroups according to patients’ age | ||||||
Any dietary treatment | Children | 34 | 1389 | 63.4% (53.7–72.6%) | 91.7% | 0.328 |
Adults | 27 | 1104 | 54.1% (46.9–61.3%) | 82.4% | 0.482 | |
Both ages | 9 | 332 | 70.8% (52.9–85.8%) | 84.9% | 0.728 * | |
Exclusive feeding with an elemental diet | Children | 9 | 381 | 95.2% (92.9–97.1%) ‡ | 10.2% | 0.324 * |
Adults | 2 | 35 | 82.7% (69–93%) ‡ | - | - | |
Both ages | 1 | 49 | - | - | - | |
Six-food elimination diet | Children | 5 | 137 | 67.5% (59.6–74.9%) ‡ | 34.7% | 0.306 * |
Adults | 14 | 600 | 63.5% (56.1–70.7%) | 69.9% | 0.518 | |
Both ages | 4 | 256 | 60.6% (54.6–78%) ‡ | 51.8% | 0.441 * | |
Four-food elimination diet | Children | 4 | 129 | 59.5% (51–67.6%) ‡ | 0.2% | 0.287 * |
Adults | 4 | 197 | 52.7% (45.8–59.6%) ‡ | 55.3% | 0.410 * | |
Both ages | 1 | 3 | - | - | - | |
Two-food elimination diet | Children | 1 | 25 | - | - | - |
Adults | 1 | 105 | - | - | - | |
Both ages | 1 | 2 | - | - | - | |
One-food (milk) elimination diet | Children | 5 | 145 | 53.7% (45.7–61.6%) | 0% | 0.142 * |
Adults | 1 | 67 | - | - | - | |
Both ages | 1 | 12 | - | - | - | |
Allergy testing-directed food elimination | Children | 10 | 572 | 45.7% (34.4–57.2%) | 79.6% | 0.583 * |
Adults | 5 | 100 | 26.4% (18.5–35.2%) ‡ | 21.9% | 0.377 * | |
Both ages | 1 | 10 | - | - | - | |
Subgroup analysis according to study design | ||||||
Any dietary treatment | Prospective | 31 | 1203 | 54.4% (47.4–61.4%) | 82.5% | 0.590 |
Retrospective | 35 | 1622 | 66.4% (57.4–74.9%) | 92% | 0.182 | |
Exclusive feeding with an elemental diet | Prospective | 4 | 48 | 84.5% (73.5–93%) ‡ | 22.7% | 0.768 * |
Retrospective | 8 | 417 | 95.4% (93.2–97.2%) ‡ | 10.6% | 0.340 * | |
Six-food elimination diet | Prospective | 11 | 477 | 64.6% (55.2–73.5%) | 76.3% | 0.359 |
Retrospective | 11 | 516 | 61.6% (57.4–65.7%) ‡ | 24.3% | 0.814 | |
Four-food elimination diet | Prospective | 6 | 326 | 55.4% (50.1–60.8%) ‡ | 53% | 0.128 * |
Retrospective | 1 | 3 | - | - | - | |
Two-food elimination diet | Prospective | 1 | 130 | - | - | - |
Retrospective | 1 | 2 | - | - | - | |
One-food (milk) elimination diet | Prospective | 3 | 142 | 41.6% (33.8–49.7%) ‡ | 35.4% | 0.398 ** |
Retrospective | 4 | 82 | 54.6% (44–64.9%) ‡ | 42.5% | 0.436 * | |
Allergy testing-directed food elimination | Prospective | 6 | 80 | 24.2% (11.6–39.6%) | 58.6% | 0.031 * |
Retrospective | 10 | 602 | 47.5% (37.5–57.6%) | 76.5% | 0.782 * |
N | Patients (n) | Overall Efficacy (%, 95% CI) | I2 | Publication Bias * | |
---|---|---|---|---|---|
SPT + APT | 7 | 225 | 42.6% (24.4–61.2%) | 86.3% | 0.904 |
IgE + SPT | 4 | 66 | 39.9% (28.8–51.6%) | 0% | 0.125 |
IgE + SPT + APT | 2 | 338 | 52.7% (47.3–57.9%) | - | - |
Dietary Treatment | N | Patients (n) | Overall Efficacy (%, 95% CI) | I2 | Publication Bias † | |
---|---|---|---|---|---|---|
Subgroups according to geographic origin of studies | ||||||
Any dietary treatment | Europe | 19 | 775 | 54% (44.9–63%) | 82.3% | 0.581 |
North America | 43 | 1968 | 64.1% (56.2–71.7%) | 91.8% | 0.320 | |
Exclusive feeding with an elemental diet | Europe | 3 | 21 | 75.7% (57–90.3%) ‡ | 0% | 0.257 ** |
North America | 8 | 441 | 95.2% (93–97%) ‡ | 21.3% | 0.074 * | |
Six-food elimination diet | Europe | 7 | 354 | 70% (65.1–74.6%) ‡ | 49.7% | 0.062 * |
North America | 13 | 571 | 63.8% (56.4–70.9%) | 61.6% | 0.903 | |
Four-food elimination diet | Europe | 3 | 203 | 51.2% (38.2–64.1%) | 69.6% | 0.302 ** |
North America | 4 | 126 | 59.7% (51.2–68%) ‡ | 52.6% | 0.883 * | |
Two-food elimination diet | Europe | 1 | - | - | - | - |
North America | 1 | - | - | - | - | |
One-food (milk) elimination diet | Europe | - | - | - | - | - |
North America | 7 | 224 | 46.4% (40–52.9%) ‡ | 49.8% | 0.326 * | |
Allergy testing-directed food elimination | Europe | 5 | 67 | 25% (9.2–45.4%) | 70.3% | 0.131 * |
North America | 10 | 605 | 45.5% (34.9–56.2%) | 79.7% | 0.624 * | |
Subgroups according to risk of bias of source studies | ||||||
Any dietary treatment | Low/moderate | 51 | 2384 | 63.7% (56.8–70.3%) | 90.8% | 0.245 |
High | 15 | 441 | 49.4% (39.4–49.5%) | 75.7% | 0.559 | |
Exclusive feeding with an elemental diet | Low/moderate | 10 | 450 | 94.8% (92.6–96.6%) ‡ | 43% | 0.152 |
High | 2 | 15 | 84.3% (63.9–97.2%) | - | - | |
Six-food elimination diet | Low/moderate | 18 | 855 | 65.6% (60.2–70.9%) | 57% | 0.791 |
High | 4 | 138 | 55.8% (36.9–73.8%) | 77.2% | 0.943 | |
Four-food elimination diet | Low/moderate | 5 | 271 | 59.8% (54–65.5%) ‡ | 15.3% | 0.410 * |
High | 2 | 58 | 38.3% (26.5–50.9%) ‡ | - | - | |
Two-food elimination diet | Low/moderate | 2 | 132 | 44.3% (36.1–52.8%) ‡ | - | - |
One-food (milk) elimination diet | Low/moderate | 3 | 94 | 55.2% (45.2–64.9%) ‡ | 0% | 0.310 ** |
High | 4 | 130 | 40.1% (32–48.6%) ‡ | 52.8% | 0.620 * | |
Allergy testing-directed food elimination | Low/moderate | 13 | 582 | 39.3% (29.6–49.49%) | 76% | 0.392 |
High | 3 | 100 | 35.8% (5.8–74.3%) | 87.8% | 0.266 ** |
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Arias, Á.; Tejera-Muñoz, A.; Gutiérrez-Ramírez, L.; Molina-Infante, J.; Lucendo, A.J., on behalf of the EUREOS Guidelines Committee. Efficacy of Dietary Therapy for Eosinophilic Esophagitis in Children and Adults: An Updated Systematic Review and Meta-Analysis. Nutrients 2024, 16, 2231. https://doi.org/10.3390/nu16142231
Arias Á, Tejera-Muñoz A, Gutiérrez-Ramírez L, Molina-Infante J, Lucendo AJ on behalf of the EUREOS Guidelines Committee. Efficacy of Dietary Therapy for Eosinophilic Esophagitis in Children and Adults: An Updated Systematic Review and Meta-Analysis. Nutrients. 2024; 16(14):2231. https://doi.org/10.3390/nu16142231
Chicago/Turabian StyleArias, Ángel, Antonio Tejera-Muñoz, Lucía Gutiérrez-Ramírez, Javier Molina-Infante, and Alfredo J. Lucendo on behalf of the EUREOS Guidelines Committee. 2024. "Efficacy of Dietary Therapy for Eosinophilic Esophagitis in Children and Adults: An Updated Systematic Review and Meta-Analysis" Nutrients 16, no. 14: 2231. https://doi.org/10.3390/nu16142231