Oral Feeding Strategies: Special Series

Early Intervention to Improve Sucking

in Preterm Newborns
A Systematic Review of Quantitative Studies
Angela Grassi*, PhD; Giada Sgherri*, MD; Olena Chorna, MM, CCRP; Viviana Marchi, MD;
Luigi Gagliardi, MD; Francesca Cecchi, PhD; Cecilia Laschi, PhD; Andrea Guzzetta, MD, PhD

ABSTRACT
Background: Premature birth is associated with feeding difficulties due to inadequate coordination of sucking, swal-
lowing, and breathing. Nonnutritive sucking (NNS) and oral stimulation interventions may be effective for oral feeding
promotion, but the mechanisms of the intervention effects need further clarifications.
Purpose: We reviewed preterm infant intervention studies with quantitative outcomes of sucking performance to sum-
marize the evidence of the effect of interventions on specific components of sucking.
Methods: PubMed, CINAHL, MEDLINE, EMBASE, and PSYCOLIST databases were searched for English language pub-
lications through August 2017. Studies were selected if they involved preterm infants, tested experimental interventions
to improve sucking or oral feeding skills, and included outcome as an objective measure of sucking performance. Specific
Medical Subject Headings (MeSH) terms were utilized.
Results: Nineteen studies were included in this review: 15 randomized, 1 quasi-randomized, and 3 crossover randomized
controlled trials. Intervention types were grouped into 6 categories (i) NNS, (ii) NNS with auditory reinforcement, (iii)
sensorimotor stimulation, (iv) oral support, (v) combined training, and (vi) nutritive sucking. Efficiency parameters were
positively influenced by most types of interventions, though appear to be less affected by trainings based on NNS alone.
Implications for Practice: These findings may be useful in the clinical care of infants requiring support to achieve efficient
sucking skills through NNS and oral stimulation interventions.
Implications for Research: Further studies including quantitative measures of sucking performance outcome measures
are needed in order to best understand the needs and provide more tailored interventions to preterm infants.
Key Words: feeding, preterms/prematurity, sucking, training/intervention infant, efficiency, morphology, frequency,
timing parameters

S
ucking is one of the first coordinated muscu- ororhythmic behavior already occurring in utero. It
lar activities in infants, already observable in is organized in bursts consisting of 6 to 12 suck
fetuses as young as 13 weeks.1,2 Similar to cycles that occur at approximately 2 Hz, followed by
other rhythmic actions (eg, locomotion), sucking is pause periods.5,6 Development of nutritive sucking
generally considered to be controlled by an innate (NS) begins later and finalizes at fluid intake. It com-
neural network known as central pattern generator prises expression or the combination of suction and
(CPG).3 In human infants, there are 2 main types of expression for fluid intake.7,8 Suction is the negative
sucking. 4 Nonnutritive sucking (NNS) is an intraoral pressure generated by lowering the tongue
and jaw and closure of the nasopharynx to draw
Author Affiliations: The BioRobotics Institute, Scuola Superiore milk out, while expression is the stripping/compres-
Sant'Anna, Polo Sant'Anna Valdera, Pontedera, Pisa, Italy (Drs Grassi, sion of the nipple between the tongue and the hard
Cecchi, and Laschi); Departments of Translational Research and of New
Surgical and Medical Technologies (Dr Sgherri) and Clinical and
palate to eject milk.9,10
Experimental Medicine (Dr Guzzetta), University of Pisa, Pisa, Italy; Stella To be effective, NS generally requires the infant to
Maris Infant Laboratory for Early Intervention, Department of have mature and functional neural networks and
Developmental Neuroscience, Stella Maris Scientific Institute, Pisa, Italy
(Ms Chorna and Drs Marchi and Guzzetta); and Department of Woman
coordinated swallowing and breathing.11 For the
and Child Health, Ospedale Versilia AUSL 12, Viareggio, Italy (Dr Gagliardi). successful development and function of NS, the
*Angela Grassi and Giada Sgherri are co-first-authors. organization of the suck, swallow, and respiration
This study was conducted at the Department of Developmental must occur at 2 levels. First, each of the 3 compo-
Neuroscience, Stella Maris Scientific Institute, Pisa, Italy.
nents must be well established for their synchronous
The authors declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article. function. Second, this cumulative mechanism func-
Correspondence: Andrea Guzzetta, MD, PhD, Stella Maris Infant tion must be still effective with the introduction of
Laboratory for Early Intervention, Department of Developmental the bolus to support transfer to the stomach.12
Neuroscience, Stella Maris Scientific Institute 331, Viale del Tirreno,
56128 Pisa, Italy ([email protected]).
Because of the immaturity and significant medical
needs of infants hospitalized in the neonatal intensive
Copyright © 2018 by The National Association of Neonatal Nurses
care units, these skills are not well established, espe-
DOI: 10.1097/ANC.0000000000000543 cially in preterm infants, defined as neonate born prior
Advances in Neonatal Care • Vol. 0, No. 0 • pp. 1-13 1

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2 Grassi et al

to 37 weeks of gestation (GA), and can represent an

What This Study Adds
important hurdle in their early development.13 Chronic
lung disease, infections, neurologic disorders, infec- • Further studies on sucking interventions in preterm
infants should include both direct and indirect quanti-
tions, and necrotizing enterocolitis are associated with tative and qualitative outcome parameters to maxi-
feeding dysfunctions and neurodevelopmental out- mize the evidence and increase the impact on clinical
comes in later childhood.14 Infants in all categories of practice. Collecting data on the efficiency, morphol-
prematurity, including extremely preterm (<28 weeks ogy, and frequency parameters may be used to objec-
tively determinate preterm infant's sucking skills.
of GA), very preterm (28 to <32 weeks of GA), moder-
ate (32 to<34 weeks of GA), and late preterm (34 to
< 37 weeks of GA), may require support for the attain-
ment of coordinated sucking for functional and effec- Several studies have demonstrated that early
tive breastfeeding or bottle-feeding.13-15,16 intervention strategies have beneficial effects on the
Recent evidence suggests that GA age at birth oral feeding performance of preterm infants, and
and birth weight are the strongest predictors of the the majority of them used qualitative assessments as
time for the transition from tube feeding to the first the primary outcome measures. A recent systematic
oral feeding and subsequent oral feeding indepen- review of NNS interventions and the effect on the
dence. And while the achievement of oral feeding is physiologic stability of preterm infants showed sig-
typically one of the primary requirements for the nificant decrease in the length of hospital stay and
discharge of a neonate, the initial neonatal inten- facilitation of the transition from gavage or partial
sive care unit discharge to home may take place oral feeds to full oral feeds, with limited information
while infant remains feeding through the feeding on the basic mechanisms underlying the observed
tube. This increases the risk of an increased rate of improvements.21 Similar results of improvements of
emergency department visits and rehospitalisa- some of the feeding/swallowing variables were
tion17 and puts the feeding tube–dependent infants reported in another review article exploring the
at an increased risk of significant neurodevelop- effects of a wider range of interventions, namely,
mental challenges.18 NNS and oral/perioral stimulation.28 Yet, another
Infants who were dependent on an orogastric Cochrane review reported benefits of NNS out-
tube upon discharge were recently reported to have weighing nonoral interventions and standard of care
significantly lower cognitive, communication, and in regard to transition to oral feeding and duration
motor scores on a standard developmental assess- of the initial hospitalization.20
ment at 2 years, independent of infant’s brain injury A number of previous systematic reviews and
and overall illness.18 Therefore, the dependence on meta-analyses have been published with valuable
orogastric technology upon discharge presents information about the types and outcomes of devel-
long-term difficulties for the infant’s neurodevelop- opmental interventions provided to preterm infants
ment and the family overall.17 Up to 40% of infants with oromotor or feeding difficulties, the use of paci-
referred to feeding clinics in early months of life are fiers, and specific intervention protocols. In general,
reported to have been born preterm.14 This is con- their conclusions show that interventions are promis-
sistent with preterm birth often being accompanied ing for enhancing feeding performance in preterm
by a number of medical and neurodevelopmental newborns, although methodological heterogeneity
needs that have long-term developmental conse- and variations in results across studies hamper the
quences, ranging from mild delays in general devel- application and the selection of the most appropriate
opmental that are overcome with supportive reha- intervention across preterm populations.
bilitative services to permanent disorders and However, no review has focused on the quantita-
disabilities. tive categories of suck performance. This informa-
Therefore, numerous studies have focused on tion may be useful in the implementation of early
intervention strategies to facilitate oral feeding of treatment and more individualized strategies of
preterm infants while still hospitalized in the neona- interventions. Therefore, the current review was
tal intensive care unit.19 In particular, NNS via paci- designed to review preterm infant intervention stud-
fier has been consistently proposed as an interven- ies with quantitative outcomes of sucking perfor-
tion to improve sucking in preterms and was found mance to summarize the evidence of the effect of
to decrease length of hospital stay and to facilitate interventions on specific components of sucking
the transition to full oral-/bottle-feeds.20-22 Similarly, including efficiency, morphology, frequency, and
strategies based on sensorimotor inputs (such as timing parameters of preterm neonate feeding. These
cheek/chin support, oral, tactile, kinesthetic, audi- parameters are directly related to the infant nutri-
tory, and vestibular, and/or visual stimulation) were tion capacity and therefore have a significant clinical
utilized in other studies showing beneficial effects on relevance. Furthermore, to fill the gap in knowledge
qualitative aspects of oral feeding performance in of the quantitative parameters of sucking matura-
preterm infants.23-27 tion, this review included only randomized

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 Early Intervention to Improve Sucking in Preterm Newborns 3

controlled trial designs of NS and NNS interven- to improve sucking or oral feeding skills, and (iii)
tions with preterm infants with quantitative out- included quantitative outcome measure based on
comes of sucking performance. objective parameters of sucking performance.
Studies were excluded if they were protocols, not
METHODS in English, did not include preterm infants, or were
any study design other than randomized.
Literature Search
Studies were identified by searching PubMed, Validity Assessment
CINAHL, MEDLINE, EMBASE, and PSYCOLIST The methodological quality of the studies was
databases. The searches were limited to peer- assessed using the Cochrane Collaboration’s tool29
reviewed publications in English and included arti- for assessing risk of bias and the following criteria
cles published through August 2017. References were considered: sequence generation, allocation
were exported into a bibliographic management concealment, blinding of participants, personnel and
database and duplicates were removed. The search outcome assessors, and completeness of outcome
strategy was performed using the following Medical data. Each criterion was judged as “yes,” “no,” or
Subject Headings (MeSH) terms: (“preterm infants” “unclear.” Two review authors separately assessed
or “preterms” or “prematurity newborns”) and each study, and disagreement was resolved by dis-
(“sucking” or “suck” or “oral feeding skills”) and cussion together with the senior author.
(“intervention” or “training”).
RESULTS
Study Selection
Criteria for inclusion in the study were established Description of Studies
prior to the literature search. Inclusion was limited to The PRISMA flow diagram of the review process is
randomized controlled trial designs. Studies were reported in Figure 1. The search, completed in Sep-
selected if they fulfilled the following criteria: (i) tember 2017, yielded 780 articles, and then 59
involved infants born preterm (gestational age at birth duplicates were removed. Two authors indepen-
below 37 weeks), (ii) tested experimental interventions dently reviewed 721 articles on the basis of the titles

FIGURE 1

Records search and inclusion chart. Description: The flowchart outlines the
process of the records search, screening, review, and inclusion. RCT indicates
randomized controlled trial.

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4 Grassi et al

and abstracts, and selected 47 articles. Full texts of parameters were subdivided into 4 groups: (i)
the selected articles were analyzed by 2 reviewers efficiency, (ii) frequency, (iii) morphology, and (iv)
and the eligibility of the study inclusion was assessed duration. They are described both in NS and the NNS.
independently; in case of mismatched opinion, con- Efficiency parameters were defined as those
sensus was reached after discussion. Twenty-eight of strictly related to the infant nutrition capacity,
the 47 articles were excluded on the basis of failure including milk volume measures and parameters
to meet the inclusion criteria. referred to the coordination of sucking and swallow-
In particular, we excluded these studies because 6 ing. Frequency parameters were defined as those
were not randomized controlled trials, 2 were proto- exploring the occurrence of a periodic event per unit
cols, 9 did not include quantitative outcome measures, time (burst, pause, suck, expression, and suction).
1 was a poster, 8 were systematic reviews, and 2 were Some of these parameters describe the whole suck-
meta-analyses. The remaining 19 studies were included ing pattern (the alternation of sucking burst and
in this review: 15 randomized, 1 quasi-randomized, pause) or the single suck cycle (alternation of expres-
and 3 crossover randomized controlled trials.5,7,30-46 sion and suction phases). Morphology parameters
The methodological quality of the selected studies were defined as those describing the shape, size, and
was evaluated as reported in Table 1. All studies had phase distribution of the sucking curves, including
risk of bias in at least 1 of the 4 items. either suction/expression amplitude or pressure.
Most of the studies involved low-risk preterm Finally, duration parameters were defined as those
infants, and 2 studies included preterm infants with exploring the time length of all events related to
either specific respiratory pathology or with low birth sucking (Table 3).
weight.5,41-43 Sample sizes ranged from 11 to 230 pre-
term infants. The types of interventions were grouped Effects of the Different Types of Intervention
into 6 categories on the basis of their features: (i)
NNS, (ii) NNS with auditory reinforcement, (iii) sen- Nonnutritive Sucking
sorimotor stimulation, (iv) oral support (OS), (v) com- Nonnutritive sucking alone was evaluated in 6 stud-
bined training, and (vi) NS. Interventions occurred ies, generally consisting of a brief intervention before
before, during, or after feeding (either by orogastric infant’s feedings. Training modalities were heteroge-
tube or bottle-feeding), or outside of the feeding times. neous and their total duration ranged from 5 days to
Figure 2 summarizes the results of the review by cat- 1 week, performed for 2, 5, or 15 minutes before
egory (efficiency, frequency, morphology, and feedings. Overall, NNS training studies showed
duration). inconsistent effects on quantitative outcome
Very preterm infants were included in 19/19, measures.
extremely preterm were included in 11/19, moderately Four efficiency parameters were identified in 5
preterm were included in 11/19, and late preterm were studies. The parameter reported to have been signifi-
included in 2/19 included studies. Since all of the stud- cantly affected by the training was the formula taken
ies the majority of the included infants were born at at first 5 minutes (1 study). The parameters unaf-
the very preterm GA age category, we did not identify fected by the training were overall transfer (4 stud-
any patterns of the type of training and its effective- ies) and proficiency (2 studies). One parameter,
ness as it relates to the GA age at birth. Table 2 sum- namely, rate of transfer, was affected in 1 study and
marizes the population, intervention/s, and outcome unaffected in another 2. Three frequency parameters
measures of the included studies. were explored in 2 studies. The parameter signifi-
cantly affected by the training was frequency of
Outcome Parameters pauses in NS (1 study). Two parameters, namely,
In accordance with the specific aims of our review, we frequency of bursts in NS and frequency of sucks per
selected all outcome measures consisting of quantita- burst in NS, were affected in 1 study and unaffected
tive parameters. Based on their characteristics, sucking in the other. Only 1 morphology parameter, suction

TABLE 1. Risk of Bias Assessed by the Cochrane Collaboration Toola

Study (see Table 2 for Reference) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19
Adequate sequence generation? X X ✓ ✓ U X U U ✓ ✓ ✓ ✓ X ✓ U U U ✓ ✓
Allocation concealment? U ✓ ✓ ✓ ✓ U U U U U U ✓ U ✓ U X U U ✓
Blinding? All outcomes ✓ ✓ U X X X U ✓ X X U X X ✓ X X ✓ ✓ ✓
Incomplete outcome data ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ ✓ X ✓ U ✓ X X X U
addressed? All outcomes.
a
✓: low risk of bias; X: high risk of bias; U: uncertain risk of bias.

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 Early Intervention to Improve Sucking in Preterm Newborns 5

FIGURE 2

Results of the review by category. EO indicates extraoral; IO, intraoral; MS, multisensory; NNS, nonnutritive
sucking; NS, nutritive sucking; OS, oral support; Overall transfer, % volume taken/volume prescribed; PAL,
pacifier-activated lullaby; PO, perioral; Proficiency, % volume taken within 5’/volume prescribed; Rate of
transfer, volume taken per minute; Suck stability, mean time from expression to swallow; T, time; Volume
loss, volume prescribed-volume taken; z, parameter not significantly affected by training; |, parameter
significantly affected by training.

amplitude, was explored (1 study) and was found to number of feeds per day (frequency parameter),
be affected by the training. Four duration parame- mean pressure in NNS (morphology parameter),
ters were explored in 3 studies. The parameters sig- and feeding duration (duration parameter).
nificantly affected by the training were pause dura-
tion (1 study). The only parameter unaffected by the Sensorimotor Stimulations
training was pause duration in NS (1 study). Three Sensorimotor stimulation programs were explored in
parameters, namely, first burst duration in NS, burst 11 studies, some of which assessed more than 1 train-
duration in NS, and feeding duration, were affected ing type. Sensorimotor stimuli consisted of oral/intra-
in one study and unaffected in another. oral (O/IO), perioral (PO), or extraoral inputs. The
O/IO was generally based on gum and tongue stimu-
NNS With Auditory Reinforcement lation that could be delivered by therapist’s hands or
Nonnutritive sucking with auditory reinforcement via a pacifier. Barlow et al5 applied an intraoral stim-
was explored in 2 studies. They used a pacifier ulus through a specific pacifier, a ‘pulsating nipple’
adapted so that a suck of predetermined strength programmed to mimic the temporal features of a
activated an audio player with lullabies36 or mother’s well-formed NNS burst. The treatment was adminis-
voice.37 Infants were trained for 15 to 20 min/d, in a tered for 3-minute epochs for 3 to 4 times per day for
range of 15 to 45 min before feedings, for 5 days. 10 days. Perioral stimulation programs, instead, were
Nonnutritive sucking with auditory reinforce- variable and composed of stroking and stimulating
ment trainings showed significant effects on all infants’ cheeks and lips. In 3 studies,7,35,38 the perioral
quantitative outcome measures explored. In particu- stimulation was associated with an oral one. Treat-
lar, they were found to be effective on rate of transfer ment duration ranged between 10 and 14 days for
and oral volume intake (efficiency parameters), 12 to 30 minutes per session. Finally, an extraoral

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 6

TABLE 2. Included Studies

Age at Assessment/
Author Population/GA Outcome Type of Training Outcome Measures Design
5
Barlow et al (2008)
1 31 Very Preterm Treatment: Pre (34.84 T: patterned oral somatosensory (1) Total oral compression, (2) non-NNS RCT
infants ± 2.10) Post (38.10 stimulation during gavage feeds compression per minute, (3) burst
Grassi et al

2 groups: treatment ± 2.27) PMA with device: 3 min. Epochs 3-4 cycle per minute, (4) NNS bursts per
(20) GA (29.11 ± Control: Pre (34.67 ± times daily for 10 d. minute, (5) mean cycle per burst, (6)
2.32) or Control (11) 2.65) Post (38.24 ± C: Soothie pacifiers during gavage NNS cycles % total, (7) daily % oral
(29.24 ± 3.10) birth 1.48) PMA feeds feed
GA
2 Barlow et al 160 preterms 23-37 HI: mean 222.1 d Ntrainer pneumatically pulsed (1) Total oral compressions: sum of all RCT
(2014)41 births GA RDS: mean 214.5 d pacifier stimulation during gav- pressure events per minute, (2) NNS
3 groups: 39 HI CLD: mean 188.1 d age feeds, or control sham with cycles: suck compression cycles with
49 respiratory distress Soothie pacifier, 3 times daily cycle periods 1200 ms and occurring
syndrome (RDS), for 10 d within the NNS burst structure per
74 chronic lung dis- minute, (3) number of NNS bursts:
ease (CLD) nipple compression cycles. NNS
performance: (4) mean number NNS
cycles/burst, and (5) NNS pressure
amplitude (cmH2O)
3 Barlow et al 180 extremely pre- 3 times weekly for 4 wk, Ntrainer pulsed orocutaneous (1) Salivary gene expression profiles, RCT
(2017)45 terms: 24-29 births from 30 wk PMA simultaneous or sham with tube (2) number of NNS bursts, (3) NNS
GA feedings 3 times daily for 4 wk cycle events, (4) total oral compres-
2 groups: treatment or sions, and (5) NNS compression
sham control pressure
4 Boiron et al 43 preterms 29-34 Stimulation + Sup- Oral stimulation: 12 min once (1) Maximum pressure for each suck RCT
(2007)38 births GA port: 33.3 PMA daily, 30 min before gavage, for burst (mm Hg), (2) burst duration for
4 groups: Stimulation Stimulation: 33.4 PMA the last 14 consecutive days of each sucking burst, (3) number of bot-
+ support: n = 14 Support: 33.3 PMA the period of gavage. tle feeds taken daily, and (4) quantity
Stimulation, n = 11 Control: 33.1 PMA Oral support twice daily for a of milk ingested per day
Support, n = 10 maximum of 10 min, with at
Control, n = 13 least 1 bottle session between
during the transition period until
autonomous feeding
5 Bernbaum et al 30 preterms (birth Weekly assessment Treatment: oral stimulation: paci- (1) Expression frequency of NNS, (2) RCT
(1983)34 weight <1500 g) 34-38 wk PMA fier during all gavage feeds NNS bursts per minute, (3) Number
2 groups: Treatment Controls: gavage feedings without of NNS cycles per minute, and (4)
and control: mean oral stimulation NNS mean pressure

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31.5 ± 1.3 and 31.5 Sucking patterns classified as organized
± 1.6 birth GA or sporadic
(continues)

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 TABLE 2. Included Studies (Continued)
Age at Assessment/
Author Population/GA Outcome Type of Training Outcome Measures Design
6 Chorna et al 94 preterms 34-36 wk 24 h after the training PAL group: 5 daily 15-min sessions (1) Oral feeding rate, (2) volume of oral RCT
(2014)37 GA period Control: routine NNS sucking intake measured during 24 h after the
2 groups: PAL or last intervention, (3) number of oral
control feedings daily, and (4) suck pressure
measured only in the intervention
group
7 Fucile et al (2005)7 32 preterms 26-29 wk Experimental 36.1 ± Experimental: nonnutritive oral (1) Overall intake (volume taken/volume RCT
birth GA 1.8 PMA stimulation or sham control. prescribed, %), (2) rate of milk trans-
2 groups: experimen- Control: 36.9 ± 1.8 Both started prior to oral feeds, fer (mL/min), (3) sucking frequency,
tal or sham

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PMA once daily for 10 d, 15-30 min (4) amplitudes of suction, and (5)
before a tube feeding expression (mm Hg)
8 Fucile et al (2009)44 30 preterms 26-29 wk Suck assessment The CFVFB: nipple-bottle system (1) Overall transfer (percent volume RCT
birth GA when 1-2 and 6-8 that delivered milk to the nipple of milk taken over the prescribed
2 groups: CFVFB (con- oral feedings per chamber from an open reservoir volume), (2) rate of milk transfer
trolled flow vacuum- day. Mean PMA of that was adjusted such that the (volume transferred per unit time mL/
free bottle system) CFVFB 34.2 ± 0.8, milk level was maintained con- min), (3) frequency of suction (#S/s),
and SB (standard SB group: 34.3 ± 1. tinually at the level if the infant's (4) expression (#E/s), (5) suction
bottle) Postassessment mouth. amplitude (mm Hg), and (6) sucking
CFVFB: 36.8 ± 2 burst duration
PMA, SB: 36.3 ± 1.5
PMA
9 Fucile et al (2011)39 75 preterms, mean Suck assessment O: twice daily stroking of the (1) Proficiency (volume of milk taken RCT
birth GA 29 ± 0.3 wk performed seri- cheeks, lips, gums, and tongue during the first 5 min as a percent-
4 groups: Oral (O), ally, started at mean for 12 min, NNS for 3 min. age of the total), (2) volume transfer
tactile/kinesthetic 33.2-34.2 PMA T⁄K: twice-daily stroking of the (volume consumed as a percentage
(T/K), combined O + head, neck, back, arms, and legs of the prescribed volume), (3) rate of
T/K, and control for 10 min and passive range of transfer (volume of milk consumed
motion to the limbs for 5 min. relative to the duration of the oral
Combined: 15 min of O or T⁄ K each feed session [mL⁄min]), and
once a day, in random order. (4) volume loss
Control: placing her hands in the
incubator without touching
infant for 15 min twice daily
(continues)

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Early Intervention to Improve Sucking in Preterm Newborns
7
 TABLE 2. Included Studies (Continued) 8

Age at Assessment/
Author Population/GA Outcome Type of Training Outcome Measures Design
10 Fucile et al (2012)40 75 preterms, mean When infants taking O: twice-daily stroking of the (1) Suction amplitude, (2) RCT
birth GA 29 ± 0.3 wk 1-2, 3-5, and 6-8 oral cheeks, lips, gums, and tongue expression amplitudes
4 groups: Oral (O), feedings per day for 12 min, NNS for 3 min (mm Hg), (3) suck-swallow ratio, (4)
tactile/kinesthetic T⁄ K twice-daily stroking of the stability of suck-swallow interval
Grassi et al

(T/K), combined O + head, neck, back, arms, and legs

T/K, and control for 10 min and passive range of
motion to the limbs for 5 min
Combined: 15 min of O or T⁄ K each
once a day, in random order.
Control: placing hands in the incu-
bator without touching infant for
15 min twice daily
11 Hill et al (2005)31 156 preterms: 29.98 ± Before intervention, im- 7-d intervention of oral support or (1) Formula taken during the first 5' (2) Quasi-RCT
2.78 to 30.33 ± 2.54 mediately after, and NNS total length of feeding time and nutri-
wk birth GA at 1-wk follow-up. tive sucking patterns (registered by a
3 groups: Oral support The Postnatal Baseline stretch-sensitive gauge WMSG) (3)
(OS), NNS, control at 23.4 ±16.86 d NS number of suck/burst, (4) number
with NNS, at 26.35 of NS bursts, and (5) number of NS
± 16.86 d in the OS pauses
and at 23.81 ± 15.25
d in the controls
12 Hwang et al 19 preterms, mean birth Ranged 32.3-40.3 wk Transition to full oral feeding, (1) Sum feeding duration in minutes, Crossover
(2010)42 GA 28.1 ± 2.6 wk PMA (mean: 5.8 ± participants served as own (2) % of prescribed volume ingested RCT
1.8) controls. A 5-min oral stimula- (mL/min),
tion applied before feedings. (3) sucking frequency, and
Oral stimulation: 3 min of manu- (4) mean volume ingested per suck
al peri- and intraoral stimulation, (mL per suck). Level of alertness
2 min of sucking on a pacifier coded from videotaped observations
based on a modification of the Neo-
natal Behavioral Assessment Scale
13 Lau and Smith 70 very low birth- Feeding monitored Swallowing group: placing a (1) Days from start to independent oral RCT
(2012)30 weight preterm when infant reached milk bolus (0.05-0.2 mL) on the feeding, (2) total
infants 24-33 wk 1-2, 3-5, and 6-8 oral tongue where the bolus rests volume prescribed, (3) volume taken
birth GA feedings per day before entering the pharynx at 5 min, (4) volume taken during
3 groups: swallowing, 15 min⁄d, 5 d weekly entire feed (mL), and (5) duration of
sucking, control Sucking group: active sucking on a oral feeding (min)
pacifier 15 min⁄d, 5 d weekly Parameters indicative of performance:

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Control group: standard care (a) overall transfer (% volume taken
per volume prescribed), (b) proficiency
(PRO, % volume taken at 5 min per vol-
ume prescribed), and (c) rate of transfer

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(RT, mL⁄min) over the entire feeding
(continues)
 TABLE 2. Included Studies (Continued)
Age at Assessment/
Author Population/GA Outcome Type of Training Outcome Measures Design
14 Medoff-Cooper 230 prematures Mean PMA: 9.29 ATVV: 10 min of auditory (female (1) Number of sucks, (2) number of RCT
et al (2015)46 29-34 wk birth GA d/33.89 wk at base- voice), tactile (moderate touch sucks per burst, (3) sucking maturity
2 groups: ATVV (audi- line assessment stroking or massage), and index, and (4) suck pressure
tory, tactile, visual, visual (eye to eye) stimulation,
and vestibular) or followed by 5 min of vestibular
control stimulation (horizontal rocking)
Controls: standard feeding and
nursing care
15 Pickler et al (1996)32 13 preterms, 28-34 wk 1-38 d PMA (mean: Prefeeding NNS: offered the infant Feeding performance: (1) the initiating Crossover
birth GA 17.5 ± 11) a pacifier for 2 min of nutritive sucking, (2) duration of RCT

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Prefeeding NNS or no Control: no prefeeding NNS first nutritive suck burst, (3) duration
prefeeding NNS of the bottle-feeding, (4) the percent-
age of prescribed formula consumed,
(5) behavioral organization (heart
rate and oxygen saturation), and (6)
behavioral state (level of arousal and
wakefulness on the Anderson Behav-
ior State Scale)
16 Pickler and Reyna 10 preterm infants, 33-40 wk PMA (mean: NNS condition was offered for Characteristics of NS (1) number of Crossover
(2004)33 28-31 wk birth GA 36 ± 2.2) at 2 min before bottle-feeding. At suck/bursts, (2) sucks/burst, (3) suck/ RCT
observation another feeding, no NNS was burst length, feeding efficiency, (4)
offered. The 2 feedings occurred percentage of prescribed formula
within 24 h of each other consumed, (5) formula consumed
per minute of feeding, (6) number of
breath bursts, (7) breaths/burst, and
(8) breath burst length
17 Rocha et al (2007)43 98 very low birth- Baseline (when Treatment: sensory-motor-oral (1) Number of feeds per day RCT
weight preterm reached a full enteral stimulation + NNS
infants, 26-32 wk diet (100 kcal/kg/d), Control: gavage tube diet + sham
birth GA postintervention procedure
2 groups: treatment or Sessions were15 min daily for 10 d
sham control
18 Standley (2003)36 32 prematures (poor Assessment: at a PAL: 15- to 20-min trial between (1) Nutritional amount ingested, (2) RCT
feeders) mean birth mean 30.8-d PMA 4 pm and 5 pm, 30-60 min be- length of feeding time, and
GA 31.7 wk fore feed trial (3) feeding rate

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2 groups: Pacifier Control: standard of care
Early Intervention to Improve Sucking in Preterm Newborns

Activated Lullaby
(PAL) or control
(continues)
9
10 Grassi et al

stimulation program implemented by Fucile and col-

Design leagues44 included sensorimotor tactile input to the

Abbreviations: CFVFB, controlled- flow vacuum-free bottle system; GA, gestation age; HI, healthy preterms; NNS, nonnutritive sucking, NS, nutritive sucking; OS, oral stimulation; PMA, postmenstrual
RCT
infants’ head, neck, trunk, and limbs, even in combi-
nation with IO/PO stimuli. The treatment duration
was 12 minutes, twice daily, for 10 days.

prescribed), (5) weight, and (6) length

ferred during entire feeding/volume
Studies in this group showed significant effects of
fer (mL/min), (3) proficiency (intake
(1) Transition time (d), (2) milk trans-

(4) volume transfer (volume trans-

sensorimotor training on the majority of quantita-
first 5 min per volume ordered),

tive outcome measures explored.

Outcome Measures

Seven efficiency parameters were explored in 5

studies and were all found to be significantly affected
by the training, except for the overall transfer and
proficiency that were unaffected in 1 study.35 Seven
frequency parameters were explored in 5 studies and
were all found to be significantly affected by the
training. Four morphology parameters were explored
in 4 studies and were all found to be significantly
of stay

affected by the various sensorimotor trainings with

the exception of mean NNS pressure, which was
unaffected in 1 study.41 A single duration parameter,
mean sucking activity, was explored in one study38
Oral stimulation (OS): stroking the
cheeks, lips, gums, and tongues

and was found to be improved by the training.

NNS: sucking on pacifiers for 5

Oral Support
Type of Training

Oral support was assessed in 2 studies and consisted

Combined: NNS + OS

of cheeks and chin support during feeding sessions.

Studies used different treatment duration and time
min 7-8× daily

distribution.
The efficiency parameters explored, formula
age; RCT, randomized controlled trial; SB, standard bottle; WMSG, Whitney mercury strain gauge (WMSG)
12 min

taken at first 5 minutes in one and oral volume

Control

intake in the other, were significantly affected by the

training. Frequency (4 parameters), morphology
(1 parameter), and duration (4 parameters) were
explored in both studies and were always found to
Age at Assessment/

6 d, at full oral feed

Assessment: at base-
line, after 3 d, after

be significantly affected by the training.

Outcome

Combined Training
Seven studies combined sensorimotor stimulation
with either NNS (5 studies) or OS (1 study) or with
other stimuli (1 study).
Nine efficiency parameters were explored in 5 stud-
ies and were all found to be significantly affected by
stimulation, NNS +

the training. The exceptions were overall transfer,

TABLE 2. Included Studies (Continued)

29-34 wk birth GA
4 groups: NNS, oral
Zhang et al (2014)35 120 preterm infants
Population/GA

unaffected in 2 studies, and mean volume per suck and

rate of transfer, unaffected in 1 study. Three frequency
OS, control

parameters were explored in 4 studies. Frequency of

sucks per burst was affected in 1 study.46 Frequency of
sucks per minute was unaffected (1 study) and fre-
quency of feeds per day was unaffected in one and
unaffected in the other study. Three morphology
parameters were explored in 3 studies and were all
found to be significantly affected by the different types
of trainings. Two duration parameters were explored
Author

in 2 studies. Mean sucking activity was affected (1

study) and feeding duration was unaffected (1 study).

Nutritive Sucking
Two studies applied an NS intervention.30,44-46 The
19

swallowing program consisted of placing a milk

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 Early Intervention to Improve Sucking in Preterm Newborns 11

TABLE 3. Assessment Parameters Classification

Parameters Classification Definition for the Purpose of This Review
Efficiency Infant nutrition capacity: milk volume and sucking and swallowing coordination
Frequency Periodic event per unit of time: burst, pause, suck, expression, and suction
Describe the entire progression of the sucking pattern (eg, sucking burst and pause)
or a single suck cycle (eg, expression and suction)
Morphology Shape, size, and phase distribution of sucking curves
Includes either suction/expression amplitude or pressure
Duration Length of time of all events related to sucking

bolus on the tongue to facilitate swallow mecha- outcome measures are not comparable with the objec-
nisms for 15 minutes for 5 days. The intervention tive sucking parameters explored in our review, as
proposed by Fucile et al44 was based on a particular most of them represent general clinical variables.
device, a controlled flow vacuum-free bottle system, Moreover, clinical quantitative variables, such as
capable to maintain milk continually at the level of weight gain, energy intake, oxygen saturation, or
the infant’s mouth. The experimental group received intestinal transit time, were not found to be affected
feeding session with this device for 20 minutes. by the training.
Both of the studies demonstrated a good effect on One of the proposed reasons for the limited effect
efficiency outcome parameters, in particular, in of NNS-only trainings on sucking parameters is
overall transfer and rate of transfer. The swallow habituation to the teat.47 In this view, the positive
program also demonstrated an effect on proficiency effect of NNS on sucking in the trained infant gradu-
outcomes. Fucile and colleagues44 also reported sig- ally fades out and a novel stimulus is necessary to
nificant differences between experimental and con- revitalize the sucking behavior. This interpretation
trol groups in frequency outcomes (suction fre- aligns with many studies in which NNS was coupled
quency and expression frequency) and in feeding with sensorimotor reinforcement (ie, sensorimotor
duration. However, no differences were found in stimulation, OS) and showed significant effects of
suction amplitude and NS burst duration. training on sucking parameters. In those studies, the
reinforcement provided by the sensory stimulation,
DISCUSSION AND CONCLUSIONS which was human-mediated in the great majority of
the cases, is likely to be responsible for the persis-
The main aim of this systematic review was to deter- tence of the positive effects on sucking patterns. This
mine the effects of early intervention on quantitative is also confirmed by the results obtained with inter-
parameters of sucking in preterm infants as reported ventions based on NNS with auditory reinforcement.
by randomized controlled designs studies. In gen- Music or mother’s voice was used as a contingent
eral, the results demonstrate that most types of inter- reward to promote NNS during the intervention
ventions aimed at improving sucking in preterm sessions.
infants yield significant effects on quantitative Following NNS, which was the most common
parameters of sucking, with the exception of train- intervention in our review (13/19 studies), senso-
ings based exclusively on NNS. The studies using rimotor stimulation was the second most common
NNS-only training report inconsistent results. Of intervention, applied in 11 out of 19 studies. Most
the 12 different outcome parameters explored in sensorimotor stimulation programs showed to posi-
those studies, 3 were positively affected by training, tively affect sucking performance. This applied to all
3 were not affected by training, and the remaining 4 domains explored and, in particular, to morphol-
6 showed inconsistent results among studies. ogy and frequency. This finding is consistent with
It is of interest that the types of parameters most another recent review of oral motor interventions
frequently found to be unaffected by the NNS-only with preterm-born infants that highlighted quantita-
training were the efficiency parameters, which are tive parameters of oral feeding success.48 The senso-
considered to be most directly related to the infant rimotor stimulation seemed to be effective irrespec-
nutrition capacity and therefore may have the highest tive of the stimulated region, that is, intra-, peri-, or
clinical relevance. Our findings might appear in con- extraoral. This might suggest that benefits could be
flict with other reviews, which found significant related to a broader effect of the intervention on the
reduction of premature infants’ length of hospital stay infant’s state regulation rather than a direct effect on
and improved bottle-feeding performance and transi- the coordination of sucking. Also, a critical role is
tion from tube to bottle as potential positive clinical played by the adult-infant relationship, as the senso-
outcomes of NNS training.21-28 However, these rimotor stimulation involved a human caregiver. It

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12 Grassi et al

Summary of Recommendations for Clinical Practice and Research

What we know: • A variety of interventions are effective in enhancing quantitative aspects of
sucking. Efficiency parameters are the most frequently explored, as they are
directly related to the infant nutrition capacity and therefore have the highest
clinical relevance.
• Efficiency parameters are positively influenced by most types of interventions,
although less affected by NNS training only.
What needs to be studied: • Further characterization of the most useful treatments to improve sucking skills,
in terms of treatment features, duration, intensity, and type of administration.
• Tailored approaches based on individual sucking pattern and infant clinical
comorbidities.
What can we do today: • Include quantitative parameters including efficiency, morphology, and frequen-
cy into clinical sucking assessments.
• Take efficiency, morphology, and frequency parameters of sucking into consid-
eration when making decisions about the most appropriate intervention for the
patient.

is noteworthy, however, that the training was also this work. Most institutions caring for hospitalized
effective in the 3 studies adopting a mechanical infants provide or have information about the com-
device to provide the intraoral stimulation.5,41,45 munity source of supportive and rehabilitative ser-
Two of the 11 studies using sensorimotor stimula- vices, including lactation specialists, speech-lan-
tion, either alone or in combination, showed pre- guage pathologists, occupational therapists, and
dominantly nonsignificant results. Hwang et al42 other professionals. These services assist mothers
found no effects of combined training (PO/IO + and primary caregivers in informed decision making
NNS) in efficiency, frequency, and time but reported and provide information and support to ensure suc-
an increase of formula intake in the first 5 minutes cessful feeding methods for their infants.
of a feeding as a result of the training intervention. In conclusion, the evidence indicates that a variety
This apparently conflicting finding may be due to of interventions, based on different principles and
the small sample size (n = 16) and heterogeneous methodologies, are effective in enhancing quantita-
infant clinical characteristics. Nonsignificant results tive aspects of sucking. Efficiency parameters are the
were also reported by Rocha and colleagues43 most frequently explored, as they are directly related
although their study explored only 1 quantitative to the infant nutrition capacity and therefore present
parameter (the number of feeds per day), and the the highest clinical relevance. They are positively
quality of the study was low.43 influenced by most types of intervention, though are
Both studies31-38 assessing the effects of OS showed less affected by NNS training only. Frequency, mor-
improvements in all areas of sucking performance, phology, and efficiency parameters outline some of
both when the training was used in isolation and when the mechanisms of functional sucking but are infre-
it was combined with oral stimulation. Oral support quently investigated. Future studies may benefit
seems to provide the necessary stability for the jaw and from the concurrent exploration of the different
to assist the infants in maintaining a more organized types of outcome measures. This could serve as a
sucking pattern. Also, NS studies generally report posi- support for a better tailored therapeutic approach
tive effects on sucking performance, although the small consisting of the selection of more personalized
number of studies and the different types of interven- interventions based on a pretraining profiling of the
tions do not allow for definitive conclusions. specific sucking components that are compromised
Several limitations need to be considered in the or weakened.
interpretation of the results of this review, princi-
pally related to the heterogeneity of the reviewed
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