Interventions to Enhance Achievement to Independent Oral Feeds in Premature Infants: A Scoping Review

Abstract

Aim

To assess the effectiveness of interventions aimed at facilitating the transition from full tube to independent oral feeds in premature infants.

Methods

Scoping review methodology using the Preferred Reporting items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA_ScR). A search of six databases (EMBASE, MEDLINE, CINAHL, Web of Science, COCHRANE, and OT Seeker), using keywords related to oral feeding and premature infants retrieved 11,870 articles. Full-text screening was completed for 36 articles, and 21 articles were included in this review.

Results

Review of the 21 articles revealed five intervention types: oral stimulation (n = 14), swallow/gustatory stimulation (n = 3), olfactory stimulation (n = 2), tactile/kinesthetic stimulation (n = 1), and auditory stimulation (n = 1). Oral stimulation had the most studies with consistent evidence supporting its beneficial effect to facilitate achievement to independent oral feeds, swallow/gustatory stimulation appeared to have some benefit, but evidence for olfactory, tactile/kinesthetic, and auditory stimulation was sparse.

Conclusion

Oral stimulation has the most studies with consistent evidence, and thus is suggested as a suitable early intervention strategy that can be used by health providers to facilitate the achievement to independent oral feeds in premature infants. The alternate forms of stimulation have limited evidence and necessitate further studies to confirm their benefits.

Keywords:

• Bottle feeding
• breast feeding
• neonatal intensive care unit
• preterm infants
• sensorimotor

Introduction

Infants born very preterm (≤32 wk gestation) are at high risk of encountering oral feeding difficulties due to immature oral motor skills and lack of coordination of sucking, swallowing and respiration (Fucile et al., 2022; Jadcherla et al., 2010; Lau, 2016; Viswanathan & Jadcherla, 2020). Up to 40% of very premature infants may encounter oral feeding difficulties while in the NICU (Jadcherla et al., 2010). Oral feeding difficulties in this population are a prominent concern to parents and health professionals because they often delay hospital discharge, may persist beyond hospitalization and lead to long-term feeding problems that have negative consequences on children’s physical growth, acquisition of developmental milestones and quality of life (Fucile et al., 2022; Jadcherla et al., 2010; Lau, 2016; Viswanathan & Jadcherla, 2020). Moreover, studies report families experience increased level of stress due to their infant’s difficulty with oral feeds (Aagaard et al., 2015; Silverman et al., 2021).

Safe and competent oral feeding entails the ability to coordinate suck, swallow, and respiration processes (Lau, 2016). Achievement of such coordination necessitates the function of multiple systems, including musculoskeletal, cardio-respiratory, gastrointestinal, and neurological systems (Fucile et al., 2019). Infants born preterm, particularly those less than 32 wk’ gestational age (GA) are developmentally unable to coordinate the sucking, swallowing and breathing necessary for safe and competent oral feeding (Jadcherla et al., 2010; Mizuno & Ueda, 2003, 2006). Thus, they must be fed via nasogastric tube until they are deemed “ready” to commence oral feeds by the neonatal team. Studies report the time to transition from full tube to independent oral feeds is inversely related to degree of prematurity (Crapnell et al., 2013; Dodrill et al., 2008). For infants born less than 26 wk GA and less than 32 wk GA, the average days to transition from tube to oral feeds has been documented to take 15 ± 8 days and 8 ± 5 days, respectively (Crapnell et al., 2013; Dodrill et al., 2008). Moreover, time to transition from full tube to independent oral feeds is further compounded by number and type of neonatal medical comorbidities, including chronic lung disease, necrotizing enterocolitis, and intraventricular hemorrhages (Crapnell et al., 2013; Dodrill et al., 2008).

Unlike full-term infants who are almost always able to successfully oral feed from birth, many premature infants display difficulties establishing oral feeding competency. Some of the most common oral feeding difficulties experienced by premature infants include poor lip seal, disorganized sucking pattern, weak suck strength, and uncoordinated suck-swallow-breathe which often leads to episodes of apnea, bradycardia, and/or oxygen desaturations while feeding (Crapnell et al., 2013; Lau, 2016; Lau et al., 2012; Park et al., 2015; Pineda et al., 2020). Studies have found that such oral feeding difficulties impede on the achievement of independent oral feeds (Aagaard et al., 2015; Chung et al., 2014; Fucile et al., 2019; Fucile, Phillips, et al., 2019; Jadcherla et al., 2010; Pickler et al., 2015; Schanler et al., 1999; Silberstein et al., 2009).

The primary focus of care in the neonatal intensive care unit (NICU) is on saving lives and minimizing the occurrence of neonatal comorbidities such as chronic lung disease or necrotizing enterocolitis. Very little attention is paid to maintain rudimentary sucking skills and to promote appropriate maturation of oral feeding skills (Pickler et al., 2015). However, neonatal oral feeding difficulties necessitate prolonged clinical management, lengthen hospitalization, impede on infant-parent bonding, and increase family stress (Aagaard et al., 2015; Chung et al., 2014; Fucile et al., 2019; Fucile, Phillips, et al., 2019; Jadcherla et al., 2010; Pickler et al., 2015; Schanler et al., 1999; Silberstein et al., 2009). Such consequences have enormous economic and social costs. Over the last two decades, attention has shifted to provide early intervention aimed at maintaining or enhancing rudimentary oral feeding skills to facilitate the transition from full tube to independent oral feeds was introduced (Fucile et al., 2002). Several researchers corroborate this theory (Amaizu et al., 2008; Crapnell et al., 2013; Park et al., 2015). To the author’s knowledge there has been no review to assess the degree of evidence available to support this theory. Therefore, the purpose of this scoping review was to assess the available evidence on the effectiveness of interventions aimed at facilitating the transition from full tube to independent oral feeds in premature infants. A scoping review methodology was selected because it is the best approach to address what is known about this concept, to map the body of literature in this area (i.e. to identify what is the nature of the evidence for this intervention approach), and to identify gaps for future research. The findings from this scoping review will provide clinicians and researchers with a comprehensive understanding on the effectiveness of early interventions to facilitate achievement to independent oral feeds in premature infants.

Methods

A scoping review was performed using the Preferred Reporting items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA_ScR) as a guide (Tricco et al., 2018). The aim of the scoping review was to address the following research questions: (1) What is the available evidence on early intervention strategies to maintain or promote oral feeding skills?; (2) What is the nature of the evidence for this intervention?; (3) What is known about this concept?; and (4) What are the knowledge gaps in this area?. A comprehensive search of six databases (EMBASE, MEDLINE, CINAHL, Web of Science, COCHRANE, OT Seeker) was conducted. The limits applied included: (1) human; (2) infant, newborn; (3) English language; and (4) year of publication from 2000 to 2022. The key search terms used included: oral feed*; breast feed*; bottle feed*; suck*; infant, premature; sensorimotor; oral; tactile; kinesthetic; olfactory; auditory; gustatory; stimulation. All of these key search terms were used for all six databases and extensions in the endings of key search terms were included in the search strategy.

To be included in this review, articles must have met the following inclusion criteria: (1) include premature infants born less than 34 wk of gestation irrespective of medical status; (2) test an intervention that was administered in the NICU, prior to or at the start of oral feeds, and aimed at enhancing oral feeding skills; (3) outcome measure included time to transition from full tube to independent oral feeds; and (4) be of high quality according to the American Occupational Therapy Association guide on levels and strength of evidence (AOTA, 2023) [i.e. randomized clinical trial (RCT, 1B) or prospective cohort or low quality RCT (2B)]. Articles were excluded if the studies: (1) were not from a peer-reviewed journal; (2) were scoping or systematic reviews; (3) focused on maternal intervention e.g. support group; (4) modified environmental factors e.g. dimming lights; (5) focused on feeding equipment e.g. type of nipple; or (6) concentrated on a feeding approach to advance oral feeds such as scheduled vs demand (cue-based) feeds.

Articles were independently screened for inclusion by two trained assessors (GH and SM) at each stage of the PRISMA framework (Moher et al., 2009). Any discrepancies were resolved with a third researcher (SF). The titles and abstracts were first screened separately for relevance according to the above inclusion and exclusion criteria. A full-text review was then conducted by the two assessors. For the full-text review, a data abstraction sheet was created to ensure both assessors were abstracting the same information. Each assessor was trained by the senior author (SF) to complete the data abstraction sheet to ascertain that the appropriate data was abstracted by the two assessors. The following data were abstracted and compared for each article: Year of publication, level of evidence, method (sample composition, sample size), type of intervention, and findings for the main outcome measure (time to transition from full tube to independent oral feeds). The level of evidence was determined using the American Occupational Therapy Association guide on levels and strength of evidence (AOTA, 2023).

Results

Figure 1 illustrates the search flow of selection of articles. The article searches were conducted between June 2021 to December 2022 and generated a total of 11,870 articles from six electronic databases. After removing duplicates, 10,314 articles titles and abstracts were screened by two assessors independently for relevance according to the inclusion and exclusion criteria. Thirty-six articles were retrieved for full-text reading. Of these, 15 articles were excluded because they did not meet the inclusion criteria for this scoping review. Table 1 provides a summary of all the studies included in this scoping review (Arora et al., 2018; Asadollahpour et al., 2015; Bache et al., 2014; Bala et al., 2016; Boiron et al., 2007; Cao Van et al., 2018; Çelik et al., 2022; Davidson et al., 2019; Fucile et al., 2002, 2011; Ghomi et al., 2019; Heo et al., 2022; Lau & Smith, 2012; Le et al., 2022; Lessen, 2011; Lyu et al., 2014; Negi et al., 2022; Rocha et al., 2007; Thakkar et al., 2018; Yildiz & Oksuzoglu, 2020; Younesian et al., 2015; D. Zhang et al., 2021).

Figure 1. PRISMA flow diagram.

Table 1. Overview of studies included in the scoping review.

Author(s), year Country	Study design Level of evidence	Participants N GA (x ± SD wks) BW (grams)	Intervention	Result Time to attainment to independent oral feeds x ± SD days p Value
Oral
Negi et al., 2022 India	RCT Three-group design 2B	N = 44 N = 20 Experimental 1 30.51 ± 1.60 1086.80 Experimental 2 N = 11 31.20 ± 0.91 2078.10 Control N = 10 30.18 ± 2.28 1923.50	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Program called oral stimulation program developed by Fucile et al. (2002) Procedure, 15-min, 1x/day, for 10 days, before gavage feeds. Experimental 2 Tactile stimulation A 15-min program, of stroking the neck, back/chest, and limbs. Procedure, same as above. Control Standard care	Experimental 1 nonnutritive sucking 6.2 ± 0.6 vs Experimental 2 Oral stimulation 6.3 ± 0.5 vs Control 9.3 ± 1.3 p < 0.0001
Çelik et al., 2022 Turkey	RCT Two-group design 1B	N = 70 Experimental N = 35 32.91 ± 1.54 1964.14 ± 360.73 Control N = 35 33.03 ± 1.56 2004.14 ± 515.72	Experimental 1 Oral stimulation A program of peri- and intra-oral input. Procedure, 15-min, 3x/day, for start of oral feeds to independent oral feeds, 15 min before a gavage feed. Control Standard care	Experimental 1 6.71 ± 4.78 vs Control 14.20 ± 13.76 p = 0.002
Ghomi et al., 2019 Iran	RCT Two-group design 1B	N = 30 Experimental N = 14 197.50 ± 6.02 days 1275.0 ± 239.23 Control N = 16 197.6 ± 7.09 1220.0 ± 159.23	Experimental 1 Oral stimulation A program of peri- and intra-oral input. Adapted from the premature infant oral motor intervention (PIOMI). Procedure, 5-min, 1x/day, for 10 days, before a gavage feed. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 8.07 ± 2.58 vs Control 14.33 ± 4.70 p < 0.001
Thakkar et al., 2018 India	RCT Two-group design 1B	N = 102 Experimental N = 51 32.1 ± 0.8 1314.04 ± 105 Control N = 51 32.39 ± 0.6 1316.13 ± 80	Experimental 1 Oral stimulation A program of peri- and intra-oral input. Program called modified premature infant oral motor intervention (modified-PIOMI) Procedure, 5-min, 2x/day, from start of oral feeds to independent oral feeds, before gavage feeds. Control Sham Intervention A researcher observed infant only. Procedure, same as above.	Experimental 1 8.58 ± 1.05 vs Control 13.16 ± 0.71 p < 0.001
Arora et al., 2018 India	RCT Two-group design 1B	N = 73 Experimental 30 ± 0.9 N = 36 1040.0 ± 120.6 Control N = 37 30.5 ± 0.6 1063.6 ± 79.5	Experimental 1 Oral stimulation A program of peri- and intra-oral input. Program called premature infant oral motor intervention (PIOMI). Procedure, 5-min, 1x/day, for 7 days, before a gavage feed. Control Unstructured stroking. Procedure, same as above.	Experimental 1 4.0 ± 0.8 vs Control 6.6 ± 1.0 p < 0.001
Bala et al., 2016 India	RCT Two-group design 1B	N = 51 Experimental N = 25 30.9 ± 1.7 1285 ± 283 Control N = 26 30.3 ± 1.5 1212.0 ± 323.0	Experimental 1 Oral stimulation A 5-step program of peri- and intra-oral input, provided by mothers. Procedure, 5x/day, before oral feeds, until independent oral feeds achieved (spoon feeding). Control Standard care	Experimental 1 7 (5–15) vs Control 13 (7–21) p = 0.03
Younesian et al., 2015 Iran	RCT Two-group design 2B	N = 20 Experimental N = 10 31.20 ± 0.78 1590 ± 0.52 Control N = 10 30.90 ± 0.73 1548 ± 0.52	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Program called oral stimulation program developed by Fucile et al. (2002) Control Standard care	Experimental 1 13.2 ± 4.31 vs Control 26.9 ± 4.79 p = 0.0000
Asadollahpour et al., 2015 Iran	RCT Three-group design 1) Non-nutritive sucking 2) Oral stimulation 3) Control 1B	N = 32 Experimental 1 N = 11 30.18 ± 1.77 1406.36 Experimental 2 N = 10 30.01 ± 1.95 1343.01 Control N = 11 30.29 ± 1.95 1393.46	Experimental 1 Non-nutritive sucking Sucking on gloved finger Procedure, 5-min, 3x/day, for 10 days, during gavage feeds. Experimental 2 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Program called oral stimulation program developed by Fucile et al. (2002) Procedure, 15-min, 1x/day, for 10 days, before gavage feeds. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 16.72 ± 8.94 vs Experimental 2 Oral stimulation 18.20 ± 9.18 vs Control 24.27 ± 9.42 p > 0.05 NS
Y. Zhang et al., 2014 China	RCT Four-group design 1) Nonnutrive sucking 2) Oral stimulation 3) Combined oral stimulation and Non-nutritive sucking 4) Control 1B	N = 108 Experimental 1 N = 25 30.9 ± 1.7 1548.2 ± 233.8 Experimental 2 N = 27 31.1 ± 1.3 1541.9 ± 272.9 Experimental 3 N = 29 31.0 ± 1.4 1579.3 ± 280.7 Control N = 27 31.1 ± 1.2 1651.5 ± 310.1	Experimental 1 Nonnutritive sucking Sucking on a pacifier Procedure, 5-min-7–8x/day, prior to gavage feeding, started when off respiratory support until independent oral feeds achieved. Experimental 2 Oral stimulation A program of peri- and intra-oral input. Procedure, 12-min, 1x/day, prior to gavage, started when off respiratory support feeding until independent oral feeds achieved. Nonnutritive sucking and Oral Stimulation Experimental 3 Same as above two. Control Standard care	Experimental 1 nonnutritive sucking 10.0 ± 5.0 vs Experimental 2 Oral stimulation 9.6 ± 3.8 vs Experimental 3 Combined 8.1 ± 2.7 vs Control 14.6 ± 6.8 p = 0.000 control vs 3 experimental groups. No significant difference between the 3 experimental groups.
Bache et al., 2014 Luxembourg	RCT Two-group design 1B	N = 101 Experimental N = 54 31.4 ± 1.5 1560.0 ± 403.1 Control N = 47 31.3 ± 1.7 1582.0 ± 350.7	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Program called oral stimulation program developed by Fucile et al. (2002) Procedure, 15-min, 1x/day, for 10 days, before gavage feeds. Control Sham intervention A researcher observed infant only. Procedure, same as above.	Experimental 1 16.9 ± 9.2 vs Control 16.0 ± 6.9 p = 0.625 NS
Lessen, 2011 USA	RCT Two-group design 2B	N = 19 Experimental N = 10 28.1 ± 0.6 1017.3 ± 127.1 Control N = 9 28.0 ± 0.9 913.3 ± 87.7	Experimental 1 Oral Stimulation A program of peri- and intra-oral input. Program called premature infant oral motor intervention (PIOMI) Procedure: 5-min, 1x/day, 10 days, prior to gavage feeding Control Sham intervention. A researcher observed infant only. Procedure, same as above	Experimental 1 18.1 ± 3.7 days vs Control 23.45 ± 5.8 days p = 0.029 NS. When birth weight included as a co-variate, no longer significant. p = 0.068
Boiron et al., 2007 France	RCT Four-group design 1) Oral stimulation + oral support 2) Oral stimulation 3) Oral support 4) Control 1B	N = 43 Experimental 1 N = 9 31.3 ± 0.49 1718 ± 128 Experimental 2 N = 11 31.1 ± 0.42 1446.0 ± 106 Experimental 3 N = 12 31.6 ± 0.35 1714.0 ± 131 Control N = 11 31.1 ± 0.36 1442.0 ± 92	Experimental 1 Oral stimulation A program of peri- and intra-oral input. Procedure, 12-min, 1x/day, for 14-days, before gavage feeds. Experimental 2 Oral support, support to cheeks and jaw during oral feeds Procedure, 10-min, 2x/day during oral feeds. Experimental 3 Oral stimulation + oral support Same as above Control Standard care.	Experimental 1 5.6 ± 0.8 vs Experimental 2 7.8 ± 1.1 vs Experimental 3 6.5 ± 1.1 vs Control 11.2 ± 1.6 p < 0.010 A significant difference between the 4 groups was observed for transition time, p < 0.01 Post-hoc test, the transition time for the control was significantly different from the experimental groups but not between groups
Rocha et al., 2007 Brazil	RCT Two-group design 2B	N = 20 Experimental N = 10 Control N = 10	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Adapted from Fucile et al. (2002) Procedure, 15-min, 1x/day, for 10 days, before gavage feeds. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 38 ± 16 days of life vs Control 47 ± 17 days of life Experimental group achieved full oral feeds 10.4 days earlier than control p = 0.03
Fucile et al., 2002 USA	RCT Two-group design 1B	N = 32 Experimental N = 16 28.2 ± 1.3 Control N = 16 28.1 ± 1.1	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Intervention developed by Fucile et al. Procedure, 15-min, 1x/day, for 10 days, before gavage feeds. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 11.4 ± 4 vs Control 1.8 ± 7 p = 0.005
Swallow/gustatory
Sun Heo et al., 2022 Korea	RCT Three-group design 1) Direct swallow training 2) Direct swallow training and Oral stimulation 3) Control 1B	N = 186 Experimental 1 N = 63 29 ± 1 1213 ± 280 Experimental 2 N = 63 29 ± 2 1241 ± 328 Experimental 3 N = 60 28 ± 1 1159 ± 308	Experimental 1 Direct swallow training (DST) Swallow exercises with a bolus of formula 0.02–0.2 ml every 30 secs Procedure, 15-min, 1x/day, 5x/week, during gavage feeds until independent oral feeds achieved. Note-a 15 min sham also provided. Experimental 2 Oral stimulation (OSMS) A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. adapted from Fucile et al. (2002) Note a 15-min of direct swallow was also provided. Procedure, same as above. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 DST 17.1 ± 9.9 Experimental 2 DST + OSMS 14.8 ± 9.4 Control 21.1 ± 15.3 p = 0.020 Post-hoc test, control vs experimental 2 was significant p = 0.021
Le et al., 2022 China	RCT Three-group design 1) Oral stimulation 2) Oral stimulation and swallow with breastmilk 3) Control 1B	N = 68 Experimental 1 29.96 ± 1.65 N = 25 Experimental 2 30.17 ± 1.53 N = 23 Control N = 20 29.95 ± 1.54	Experimental 1 Oral Stimulation A program of peri- and intra-oral input, used the program called premature infant oral motor intervention (PIOMI) Procedure, 5-min, 1x/day, 10 days, during garage feedings. Experimental 2 Oral Stimulation and swallow with breastmilk Researcher dipped finger with mothers BM Procedure, same as above. Control Standard care	Experimental 1 Oral stimulation 17.96 ± 6.06 vs Experimental 2 Oral stimulation + swallow 15.96 ± 5.43 vs Control 22 ± 7.9 p = 0.0024 control vs. experimental 2 p = 0.4229 experimental 1 vs experimental 2.
Lau & Smith, 2012	RCT Three-group design 1) Nonnutrive sucking 2) Swallow exercise 3) Control 1B	N = 70 Experimental 1 25 28.1 ± 0.4 Experimental 2 22 28.4 ± 0.5 Control 23 28.1 ± 0.4	Experimental 1 Nonnutritive sucking Sucking on a pacifier Procedure, 15-min, 1x/day, 1x/day, 5x/week, during gavage feeds until independent oral feeds achieved. Experimental 2 Swallow exercises Direct swallow training Swallow exercises with a bolus of formula 0.02–0.2 ml every 30 secs Procedure, same as above. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 Nonnutritive sucking 21 ± 2 vs Experimental 2 swallow exercises 15 ± 2 vs Control 19 ± 2 L p = 0.019
Olfactory
Davidson et al., 2019 USA	RCT Two-group design 1B	N = 33 Experimental N = 17 30± SD not included Control N = 16 31± SD not included	Experimental 1 Olfactory stimulation Mothers own milk placed on cotton tipped applicator and positioned under infant’s nose during gavage feeds. Procedure, 15-min, 1x/day, 4–6x/week, from start of oral feeds to independent oral feeds. Control Sham intervention Water placed on cotton tipped applicator and positioned under infant’s nose during gavage Procedure, same as above.	Experimental 1 13.3 mean days vs Control 13 mean days p = 0.880 When stratified by GA, infants born <31 wk learned to feed sooner than controls (p = 0.05).
Cao Van et al., 2018 Belgium	RCT Two-group design 1B	N = 49 Experimental N = 25 34.6 ± 1.8 2223.4 ± 435.6 Control N = 24 34.4 ± 1.4 2206 ± 383	Experimental 1 Olfactory Stimulation The program involved a scented pen placed under the nose for 10 s prior to each gavage feeding. Control Sham intervention Odorless pen placed under the nose. Procedure, same as above.	Experimental 1 8.1 ± 4.9 vs Control 9.6 ± 5.5 p = 0.326
Auditory
Yildiz & Arikan, 2012 Turkey	RCT Three-group design 1) Auditory stimulation 2) Nonnutritve sucking 3) Control 1B	N = 90 Experimental 1 N = 30 31.23 ± 1.33 1508.33 ± 338.0 Experimental 2 N = 30 31.90 ± 1.29 1468.83 ± 266.2 Control N = 30 31.6 ± 1.57 1495.33 ± 350.5	Experimental 1 Nonnutritive sucking Sucking on pacifier during gavage feeding Procedure, 3x/day, during the duration of a gavage feeding Experimental 2 Auditory stimulation Lullaby music played during gavage feeding Procedure, 3x/day, during the duration of a gavage feeding Control Standard care	Experimental 1 Auditory stimulation 184.27 ± 78.17 (in hours) Experimental 2 Nonnutritive sucking 243.03 ± 123.34 Control 280.30 ± 174.89 p < 0.05
Tactile/Kinesthetic
Fucile et al., 2011 USA	RCT Four-group design 1) Oral stimulation 2) Tactile/kine sthetic stimulation 3) Combined oral and tactile/kinesthetic stimulation 4)Control 1B	N = 75 GA < 33 wk Experimental 1 N = 19 Experimental 2 N = 18 Experimental 3 N = 18 Control N = 20	Experimental 1 Oral stimulation A 15-min program, first 12 min of peri- and intra-oral input and final 3 min of non-nutritive sucking. Developed by Fucile et al. Procedure, 15-min, 2x/day, for 10 days, before gavage feeds. Experimental 2 Tactile/kinesthetic stimulation A 15-min program, first 10 min of stroking the whole and final 5 min of flexion/extension Procedure, 15-min, 2x/day, for 10 days, before gavage feeds. Experimental 3 Combined oral + tactile/kinesthetic stimulation, same as above however each was provided 1x/day for 10 days. Control Sham intervention. A researcher observed infant only. Procedure, same as above.	Experimental 1 Oral stimulation 11.1 ± 0.8 Experimental 2 Tactile/kinesthetic stimulation 11.4 ± 0.8 Experimental 3 Combined 10 ± 0.8 Control 20.7 ± 1.5 p < 0.001 All three experimental groups achieved independent oral feeding sooner than the control, but no difference between the three groups. p < 0.001

Overall, the age range was from 26 to 36 wk postmenstrual ages for provision of the intervention and the programs were administered by health professionals including occupational therapists, physical therapists, and nurses. All 21 articles had a high level of evidence with 17 graded as 1B (RCT) and four graded as level 2B (prospective cohort or low quality RCT). The authors identified five categories of interventions: (i) oral stimulation, defined as stroking of peri-oral structures (cheeks, lips, jaw), stroking of intra-oral structures (tongue, palate, and gums) and/or nonnutritive sucking (NNS); (ii) swallow/gustatory stimulation, defined as provision of direct swallow exercises with or without different fluids, such as formula or breast milk. The swallow exercises involve placing a bolus of 0.05 to 0.2 mL of milk via a syringe directly on the medial-posterior part of the tongue to elicit a swallow. Of note, swallow and gustatory stimulation was included as one theme because both swallow function and gustatory senses are simultaneously stimulated and cannot be isolated; (iii) tactile/kinesthetic stimulation, described as stroking of whole body and limb extension/flexion; (iv) auditory stimulation, defined as exposure to music or parental voices; and (v) olfactory stimulation defined as exposure to different scents such as breast milk odor.

Table 2 provides a synthesis of the effect of each category of intervention on achievement to independent oral feeds. All categories displayed a strong level of evidence because only randomized clinical trials (1B) or prospective cohort or low quality RCT(2B) were included in the scoping review. The large majority of studies focused on oral stimulation with most finding a beneficial outcome on achievement to independent oral feed. The alternate interventions had one to three studies with insubstantial results. The section below describes in category of intervention in more detail.

Table 2. Synopsis of study findings effect on achievement to independent oral feeds.

Intervention (n = number of studies)	Level of evidence	Statistical significance noted in the time to attainment to independent oral feeds
	1B
	2B
Oral stimulation (n = 14)	1B = 10	11
	2B = 4
Swallow/Gustatory stimulation (n = 3)	1B = 3	2
Olfactory stimulation (n = 2)	1B = 2	0
Tactile/Kinesthetic stimulation (n = 1)	1B = 1	1
Auditory stimulation (n = 1)	1B = 1	1

Oral Stimulation

Fourteen studies assessed the effect of an oral stimulation intervention on time to achieve independent oral feeds (Arora et al., 2018; Asadollahpour et al., 2015; Bache et al., 2014; Bala et al., 2016; Boiron et al., 2007; Çelik et al., 2022; Fucile et al., 2002; Ghomi et al., 2019; Lessen, 2011; Lyu et al., 2014; Negi et al., 2022; Rocha et al., 2007; Thakkar et al., 2018; Younesian et al., 2015; Y. Zhang et al., 2014). Studies performed a two- to four-group randomized trial to test a specific oral stimulation protocol by comparing an experimental and control group. Ten of the studies had high level of evidence (1B). Eleven out of the fourteen (78%) studies revealed a statistically significant beneficial effect of oral stimulation on time to achieve independent oral feeds (Arora et al., 2018; Bala et al., 2016; Boiron et al., 2007; Çelik et al., 2022; Fucile et al., 2002; Ghomi et al., 2019; Lyu et al., 2014; Negi et al., 2022; Rocha et al., 2007; Thakkar et al., 2018; Younesian et al., 2015; Y. Zhang et al., 2014). In one study by Lessen et al. (2011) the significance was no longer maintained when birthweight was included as a co-variate in the statistical analysis, and in two studies (Asadollahpour et al., 2015; Bache et al., 2014), there was no statistically significant difference between the experimental and control groups.

Swallow/Gustatory Stimulation

Three studies evaluated the effect of swallow/gustatory stimulation (Heo et al., 2022; Lau & Smith, 2012; Le et al., 2022). All three studies had a three-group randomized study design (level of evidence 1B) which assessed the impact of swallow/gustatory stimulation intervention alone (Lau & Smith, 2012), or in combination with oral stimulation intervention, and a control sham intervention (Heo et al., 2022; Le et al., 2022). Two of the studies observed that the intervention which consisted of swallow/gustatory stimulation alone or in combination with oral stimulation led to faster achievement to independent oral feeds than a control sham intervention (Heo et al., 2022; Lau & Smith, 2012). The study by Le et al. (2022) did not observe a significant difference between swallow/gustatory stimulation alone and oral stimulation experimental groups.

Olfactory Stimulation

Two studies performed a randomized trial (level of evidence 1B) to examine the effect of olfactory stimulation intervention to a sham intervention on achievement of independent oral feeds (Cao Van et al., 2018; Davidson et al., 2019). Both studies did not observe a statistically significant difference between the two groups in achievement to independent oral feeds. However, when gestational age was incorporated in the analyses by Davidson et al. (2019) a statistically significant difference was noted between groups.

Tactile/Kinesthetic Stimulation

One study by Fucile et al. (2011) investigated the effect of a tactile/kinesthetic stimulation intervention on achievement of independent oral feeds. A four-group randomized trial (level of evidence 1B) was performed testing the impact of a single tactile/kinesthetic stimulation, a single oral stimulation intervention, a combined tactile/kinesthetic and oral stimulation, and a control sham intervention. The study results indicated that all three interventions enhance the achievement to independent oral feeds compared to a control sham intervention. However, there was no statistically significant difference between the three experimental interventions (Fucile et al., 2011).

Auditory Stimulation

The study by Yildiz and Arikan (2012) was the only study to assess the effects of auditory stimulation, which consisted of a 2-group randomized trial (level of evidence 1B) testing the exposure to Mozart’s lullabies sonatas during gavage feedings to a control sham intervention. The study observed a significant difference between the experimental and control groups in achievement to independent oral feeds (Yildiz & Arikan, 2012).

Discussion

Oral feeding difficulties in premature infants is highly prevalent and clinically significant as they may have negative consequences on the long-term health of infants, family well-being and health care resource utilization (Jadcherla et al., 2017; Viswanathan & Jadcherla, 2020). Interventions aimed at maintaining rudimentary sucking skills and enhancing maturation of oral feeding skills is paramount. The aim of this scoping review was to evaluate the available literature on the different types of interventions and their effectiveness at facilitating the transition from full tube to independent oral feeds in premature infants. This scoping review revealed five types of intervention: oral stimulation, swallow/gustatory stimulation, olfactory stimulation, tactile/kinesthetic stimulation, and auditory stimulation.

A total of 21 studies were included in this scoping review. Of these, 14 out of the 21 investigated oral stimulation. The large majority of these studies (11/14, 79%) observed a decrease in the time to achievement of independent oral feeds, despite the variances in the oral stimulation intervention between the studies. The study by Lessen (2011), initially found a statistically significant difference between groups which disappeared when including birthweight as a co-variate. The lack of significance may be attributed to the weaker level of evidence (level 2B) because of its small sample size (n = 19) and thus weak power in the study. There was no blinding of the intervention in the two studies that did not observe a statistically significant difference which may have impacted the results. The oral stimulation interventions included studies involved stroking of peri- and intra- oral structures and variations in nonnutritive sucking. These findings provide substantial evidence to support the concept that maturation of sucking may be dependent not only on physiological maturation, but also on learning experiences. As such, training of infants to improve sucking is conceivable (Fucile et al., 2002). The oral stimulation interventions strengthen the oral musculature, improve the functioning of the oral structure to work more efficiently with greater endurance, and as a whole, enhance the maturation of central and peripheral neural structures necessary for adequate sucking skill and coordination of suck, swallow and breathe (Fucile et al., 2002; Fucile et al., 2005; Medoff-Cooper et al., 2015). We observed that the duration of the oral stimulation interventions ranged from 5 min to 15 min. This brings to the forefront the need for a dose response study to identify the most effective duration in decreasing the period of transition from full tube to independent oral feeds in premature infants.

The second most common intervention was gustatory/swallow stimulation which was investigated by three studies using a three-group randomized trial consisting of swallow exercises alone, swallow exercises combined with an oral stimulation intervention, and a control sham intervention (Heo et al., 2022; Lau & Smith, 2012; Le et al., 2022). Notably, all three studies found that swallow exercises alone or combined with an oral stimulation intervention was the most effective in facilitating the transition to independent oral feeds compared to control sham intervention. The oral feeding process consists of the oral preparatory, pharyngeal and esophageal phases involved in the formation of the bolus and its transport to the stomach through the pharynx and esophagus, respectively (Lau & Smith, 2012; van den Engel-Hoek et al., 2017; Viswanathan & Jadcherla, 2020). The swallowing process is reflexive, and dependent on the activation of spatially and temporally overlapping muscle components. The swallow exercises are intended to enhance the pharyngeal phase of swallow. The oral stimulation is intended to increase the strength and functioning of the oral musculature involved in the oral preparatory phase (Lau & Smith, 2012; van den Engel-Hoek et al., 2017; Viswanathan & Jadcherla, 2020). The findings from this scoping review suggest that enhancing the oral musculature involved in the oral preparation and propelling of the bolus to the pharynx to initiate a swallow along with swallow exercises have a synergistic effect on sucking skills and coordination of suck, swallow and breathe. However, the limited number of studies highlights the need for further research to delineate the effectiveness of swallow/gustatory stimulation alone or in combination with oral stimulation prior to implementation in clinical practice.

Very few studies focused on alternate input, specifically olfactory, tactile/kinesthetic, or auditory stimulation. The evidence on provision of these inputs to enhance achievement of independent oral feeds is weak because the quantity of available data is low (only 1 to 3 studies available) rather than quality, as all studies had a high level of evidence (1B). This review identified two studies that assessed olfactory stimulation with conflicting results (Cao Van et al., 2018; Davidson et al., 2019). One study tested tactile/kinesthetic stimulation (Fucile et al., 2011) and another tested auditory stimulation (Yildiz & Arikan, 2012), and a significant effect on achievement to independent oral feeds was observed with both types of intervention. What these findings suggest, is that stimulation input which targets the trunk/limbs or auditory system, as in these studies, may have distributed effects that go beyond the target system to enhance oral feeding performance (Fucile et al., 2012). However, there is not enough evidence on these alternate forms of interventions to lead to practice. This review brings forth some evidence that alternate forms, beyond the oral structures, of sensory stimulation can enhance oral feeding skills as it is understood that achieving independent oral feeding is a multisystem process that involves not only oral system, but many other systems such as behavioral state organization, postural control, head/neck and trunk tone, and appropriate cardiorespiratory function (Fucile et al., 2019). Clinicians may use these alternate inputs when infants have limited access to the oral system, such as when infants are intubated or as a complement to oral sensory input to further improve infants’ development of oral feeding skills.

An important purpose of this review was to highlight the impact of interventions that can be used by clinicians to safely enhance oral feeding skills in premature infants. This review demonstrates that oral stimulation has the most evidence with consistent evidence supporting its beneficial effect to facilitate achievement to independent oral feeds; swallow/gustatory stimulation alone or in combination with oral stimulation appears to beneficial as well; and alternate form of interventions (olfactory, tactile/kinesthetic, and auditory) have limited evidence. Future larger and more diverse sample sizes studies are needed to establish the effect of alternated forms of interventions on attainment to full oral feeds in premature infants.

It should be noted that there are several limitations in this scoping review. This review did not include searches in the gray literature, (e.g. online websites). By not screening the gray literature it is possible that some interventions may have been overlooked. There is also a possibility that inadequate search terms and bias of un-blinded reviewers to study objectives may also have influenced results. The review only focused on one outcome, attainment to independent oral feeds because it is a criteria that often delays hospital discharge. However, the authors acknowledge that interventions are centered on improving infants overall oral feeding performance such as, behavioral state regulation, physiological response to feeding and feeding outcomes rather than attainment to independent oral feeds only and these benefits were not covered in this review. The overall study limitations (inclusion/exclusion criteria) were quite restrictive to include premature infants only, therefore these findings are only generalizable to this population.

Conclusion

This scoping review reveals that oral stimulation interventions can be used as an early intervention strategy by health care providers to facilitate achievement to independent oral feeds in premature infants. However, the evidence on the effectiveness of alternate forms of stimulation interventions is limited, and further research is needed to establish their benefit on infant’s oral feeding skills.

Authors’ Contributions

Samiira Omar Sheikh-Mohamed, Hillary Wilson, and Dr. Sandra Fucile were all involved in inception of the research project, study design development, data collection and analysis, and writing of the manuscript.

Disclosure Statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.

Notes on contributors

Samiira Omar Sheikh-Mohamed

Samiira Omar Sheikh-Mohamed is an Occupational Therapist who completed this research study as part of the degree.

Hillary Wilson

Hillary Wilson is an Occupational Therapist who completed this research study as part of the degree.

Sandra Fucile

Sandra Fucile is an Occupational Therapist and Assistant Professor at the School of Rehabilitation Therapy, Queen's University.