The Association between Sucking Behavior in Preterm Infants

and Neurodevelopmental Outcomes at 2 Years of Age

Mechteld I. Wolthuis-Stigter, MSc1, Margreet R. Luinge, PhD1, Saakje P. da Costa, PhD1, Wim P. Krijnen, PhD1,
Cees P. van der Schans, PhD1,2, and Arend F. Bos, MD, PhD3

Objective To evaluate whether a specific period after birth (in weeks postmenstrual age [PMA]) and specific el-
ements of sucking are associated with abnormal neurodevelopmental outcomes at age 2 years using a longitudinal
approach.
Study design Fifty-two preterm infants participated in this longitudinal cohort study (mean gestational age,
29.5 weeks; mean birth weight, 1197 g). We assessed the infants’ sucking patterns at 37-50 weeks PMA using
the Neonatal Oral-Motor Assessment Scale. At age 2 years, based on a neurologic examination and the Dutch
version of the Bayley Scales of Infant and Toddler Development, Second Edition, we categorized the children as
developing normally (n = 39) or abnormally (n = 13). ORs, including 95% CIs, were calculated to ascertain the
risk of abnormal neurodevelopmental outcomes.
Results The inability to sustain sucking at 46 weeks PMA (OR, 6.25; 95% CI, 1.29-30.35) and the absence of a
mature sucking pattern at 44 weeks PMA (OR, 6.30; 95% CI, 1.40-28.32) significantly increased the odds of
abnormal neurodevelopmental outcomes at age 2 years. The ORs of the Neonatal Oral-Motor Assessment Scale
items assessing rhythmic jaw movements, rhythmic tongue movements, and coordination among sucking, swal-
lowing, and respiration were high shortly after term, but failed to reach significance.
Conclusion Specific elements of sucking at 4-6 weeks postterm are associated with abnormal neurodevelop-
mental outcomes in preterm infants at age 2 years. This period might be a sensitive time of infant development
in which sucking behavior is an early marker of abnormal developmental outcomes. This finding may offer oppor-
tunities for early intervention. (J Pediatr 2015;166:26-30).

P
reterm infants have more developmental difficulties at school age compared with full-term infants.1 One challenge
for these children is to master the skills required for oral feeding. Preterm infants have more difficulty coordinating
sucking, swallowing, and breathing, and in some cases the tongue and jaw movements are inadequate as well.2-5
Although several studies have suggested that inadequate sucking behavior in preterm infants may serve as a marker of
abnormal development,6-8 few studies have investigated the direct association between sucking behavior and neurodevelop-
mental outcomes.9-11
The present study is part of a prospective, longitudinal study concerning the development of sucking behavior of 65 preterm
infants in relation to neurodevelopment.2,12 In this study, we first addressed the question whether a specific period, expressed in
weeks’ postmenstrual age (PMA), may be associated with abnormal neurologic development. Insight into the development of
sucking patterns between 37 and 50 weeks PMA will contribute to our understanding of the association between sucking pat-
terns and neurodevelopmental outcomes. We then focused on investigating whether specific elements of sucking patterns are
associated with abnormal neurologic development. In addition to the overall diagnosis of the Neonatal Oral-Motor Assessment
Scale (NOMAS),4 investigating the individual items on the scale afforded a more detailed understanding of the association be-
tween specific elements of sucking patterns and neurodevelopmental outcomes at age 2 years. In short, our aim was to evaluate
the hypothesis that a specific period after birth, expressed in weeks of PMA, and specific elements of sucking, as assessed by
items of the NOMAS, are associated with abnormal neurodevelopmental outcomes.

Methods
From the 1Research and Innovation Group Health Care
This study was part of a prospective, longitudinal study on the developmental and Nursing, Hanze University of Applied Sciences; and
2
course of sucking patterns in 65 preterm infants in relation to neurodevelopmental Department of Rehabilitation Medicine, Center for
Rehabilitation, and 3Department of Pediatrics and
Neonatology, Beatrix Children’s Hospital, University
Medical Center Groningen, University of Groningen,
Groningen, The Netherlands
BPD Bronchopulmonary dysplasia
Funded by the Regional Attention and Action for the
MDI Mental Developmental Index Circulation of Knowledge scheme, which is managed by
NOMAS Neonatal Oral-Motor Assessment Scale the Dutch Foundation of Innovation Alliance (NVG-7-
2011-3-7Int). The authors declare no conflicts of interest.
PDI Psychomotor Developmental Index
PMA Postmenstrual age 0022-3476/$ - see front matter. Copyright ª 2015 Elsevier Inc.
SGA Small for gestational age All rights reserved.
http://dx.doi.org/10.1016/j.jpeds.2014.09.007

26

outcomes.2,12 The focus of the original study was on 2 groups:
infants who were small for gestational age (SGA)2 and infants
with bronchopulmonary dysplasia (BPD).12 Preterm infants
without these conditions were included as controls. All of
the infants had been admitted to University Medical Center
Groningen or to Martini Hospital Groningen shortly after
birth. Recruitment of infants extended from 2004 until the
end of 2006, with follow-up between 2006 and 2009. The
NOMAS was used to assess sucking patterns longitudinally
from 37 to 50 weeks PMA. The Medical Ethics Review Com-
mittee of University Medical Center Groningen approved
the study, and written informed consent was obtained from
the parents of all infants participating in the study.
Fifty-two of 65 preterm infants were included in the
follow-up study. Of the 13 infants not included, 11 infants’
parents had declined the invitation to participate in the
follow-up study or had not been contacted in time, 1 infant
was excluded owing to congenital defects that manifested af-
ter inclusion, and 1 infant had died. Owing to the original
study design the study group consisted of a relatively large
proportion of infants with BPD (n = 18; 35%) and SGA in-
fants (n = 12; 23%).
NOMAS
Sucking behavior was assessed using the NOMAS, an
observational method consisting of 28 items that assess
sucking of newborn infants. The NOMAS is a noninvasive
and user-friendly tool for assessing both nutritive and
nonnutritive sucking in both breastfed and bottle-fed in-
fants.13 da Costa and van der Schans14 assessed the intra-
rater agreement as “fair” to “almost perfect” and interrater
reliability as “moderate” to “substantial.” To strengthen
the reliability of the NOMAS, the video recordings (see
below) were assessed independently by various pairs
among 4 certified assessors.4,15 In cases of disagreement
about an episode in the recordings, the particular
recording was discussed among all 4 assessors until
consensus was reached.
Assessment resulted in 1 of 3 possible diagnoses: normal
sucking pattern, disorganized sucking pattern, or dysfunc-
tional sucking pattern. A normal sucking pattern is charac-
terized by rhythmic movements of the jaw and tongue and
appropriate coordination between sucking, swallowing, and
breathing. If the jaw and tongue movements are arrhythmic,
the sucking pattern is classified as disorganized. Infants
whose jaw and tongue movements are abnormal and inter-
fere with sucking are classified as having a dysfunctional
sucking pattern.
NOMAS Recordings and Analyses
Between 37 and 40 weeks PMA, weekly video recordings were
made of the first 2 minutes of nutritive sucking; between 40
and 50 weeks PMA, these recordings were made every
2 weeks. The recordings were assessed independently by
various pairs among the 4 certified assessors.2,12 These asses-
sors were Dutch speech and language therapists, as described
in the NOMAS literature.4,15 We defined the scores on the
Vol. 166, No. 1  January 2015
NOMAS items as either positive (yes = 1) or negative
(no = 0). A positive score was awarded if the infant was
seen to perform a specific element of sucking and swallowing
(eg, rhythmic jaw excursions), whereas a negative score was
awarded if this element of sucking and swallowing was not
performed adequately. Sometimes 2 separate items on the
NOMAS represent the same element of sucking and swallow-
ing but are formulated as opposites (inconsistent vs consis-
tent, rhythmic vs arrhythmic). For the purpose of
investigating whether the infants were or were not able to
perform a specific element of sucking and swallowing, the
scores on these opposite items were combined.
Follow-Up at Age 2 Years
At 27 months (corrected age), we administered the Bayley
Scales of Infant Development, Second Edition, Dutch
version16 to assess the children’s mental and motor develop-
ment. Scores were obtained on the Mental Developmental
Index (MDI) and the Psychomotor Developmental Index
(PDI). We also performed a neurologic examination
following Touwen’s method17 to assess neurologic outcomes
at age 2 years. Based on the results of the neurologic exami-
nation and the scores on the Bayley Scales of Infant Develop-
ment, Second Edition, Dutch version, the 52 children were
divided into 2 groups: normal development and abnormal
development. A child was assigned to the abnormal develop-
ment group if his or her neurologic examination was
abnormal or if he or she had an MDI or PDI score <85.
Statistical Analyses
Analyses were performed using the statistical software pack-
age SPSS for Windows, version 17.0 (SPSS, Chicago, Illinois).
First, the data were analyzed at the level of the diagnoses. The
proportions of infants with normal sucking behavior and
those with abnormal sucking behavior (ie, a disorganized
or dysfunctional sucking pattern) were determined for each
group and for each measurement. ORs and 95% CIs were
calculated to determine the risk of abnormal sucking patterns
on subsequent abnormal neurologic development. Second,
NOMAS data were analyzed at the level of the items. Each
item’s OR and 95% CI were calculated to establish the risk
of subsequent abnormal neurologic development.
Whether differences in sucking patterns between the
normal development and abnormal development groups
were related to potential confounders was investigated using
the independent-samples t test and the Pearson c2 test.
Gestational age, birth weight, and variances in the distribu-
tion of appropriate for gestational age infants, SGA infants,
and infants with BPD were considered potential con-
founders. Statistical significance was predetermined at
P < .05.
Results
Fifty-two preterm infants participated in the follow-up study.
At age 2 years, 39 infants were classified as developing nor-
mally and 13 infants were classified as developing abnormally
27
THE JOURNAL OF PEDIATRICS  www.jpeds.com
Table I. Characteristics of the preterm infants (n = 52)
Characteristics Total
Number 52
Males/females, n 27/25
Gestational age, wk, mean (range) 29.5 (24.9-35.7)
Birth weight, g, mean (range) 1197 (560-2150)
SGA, n (%) 12 (23)
BPD, n (%) 18 (35)
SGA + BPD, n (%) 3 (6)
No SGA, no BPD, n (%) 25 (48)
(Table I). Of those 13 infants, 3 infants had cerebral palsy (2
unilateral spastic, 1 bilateral spastic; Gross Motor Function
Classification System 1, 2, and 4, respectively), 6 had mild
neurologic abnormalities on Touwen examination, 3 had
developmental delay without neurologic abnormalities (MDI
<85, 1 infant MDI <85 and PDI <85), and 1 infant had
developmental delay (PDI <85), but he did not undergo
neurologic testing. No significant between-group differences
were found in terms of gestational age (P = .91), birth
weight (P = .17), SGA (P = .25), or BPD (P = 1.00).
NOMAS Diagnoses
The numbers of infants in the 2 groups assessed each week be-
tween 37 and 50 weeks PMA are presented in Table II. The
developmental course of sucking patterns, depicted in
Figure 1, shows the differences between the 2 groups during
the early postterm period, 44-46 weeks PMA. Between 44
and 46 weeks PMA, the proportion of infants with normal
sucking behavior was smaller in the abnormal development
group compared with the normal development group. The
risk of abnormal neurodevelopmental outcomes is greater in
infants who exhibited an abnormal sucking pattern at
44 weeks PMA (OR, 6.82; 95% CI, 0.79-58.99). At 46 weeks
PMA, the OR was 7.90 (95% CI, 0.91-68.75).
NOMAS Items
Our analysis revealed that essentially none of the infants had
dysfunctional jaw and tongue movements. For the sake of
clarity, these items are not presented graphically. The differ-
ences between the 2 groups during the early postterm period
(44-46 weeks PMA) were apparent for a consistent degree of
jaw depression, rhythmic jaw movements, and mature suck-
ing beyond appropriate age (ie, full term) (Figure 2; available
at www.jpeds.com).
The differences between the 2 groups during the early post-
term period (44-46 weeks PMA) were also apparent for
rhythmic tongue movements, the ability to sustain sucking,
and the coordination of sucking, swallowing, and respiration
(Figure 3; available at www.jpeds.com).
The inability to sustain sucking at 46 weeks PMA and the
absence of mature sucking at 44 weeks PMA significantly
increased the odds of abnormal neurodevelopmental out-
comes at age 2 years (Table III). For the items relating to
rhythmic jaw movements, rhythmic tongue movements, and
the coordination of sucking, swallowing, and respiration, we
28
Vol. 166, No. 1
Normal development Abnormal development
39 13
20/19 7/6
29.5 (24.9-35.0) 29.4 (26.0-35.7)
1231 (560-2150) 1096 (750-1460)
7 (18) 5 (39)
13 (33) 5 (39)
2 (5) 1 (8)
21 (54) 4 (31)
also found elevated ORs regarding neurodevelopmental
outcomes, albeit without statistical significance.
Discussion
This study demonstrates that both a specific period and spe-
cific elements of sucking skills were associated with abnormal
neurologic development at age 2 years in this heterogeneous
group of preterm infants. In the event of persistent abnormal
sucking patterns at 4-6 weeks postterm, a detailed inspection
of specific items of the NOMAS is important, because these
specific items may serve as early indicators of abnormal neu-
rodevelopmental outcomes.
In the present study, the early postterm period differenti-
ated between normal and abnormal development. This im-
plies that the period of 4-6 weeks after term might be
viewed as a sensitive period in infant development during
which sucking behavior could serve as an early marker of
abnormal developmental outcomes. A study of cardiorespi-
ratory events reported a similar finding; compared with
healthy controls, preterm infants were at increased risk of
cardiorespiratory events only up to 43 weeks PMA.18
Interestingly, at 8 weeks after term and beyond, sucking pat-
terns no longer differentiated between normal and abnormal
development. This is consistent with the idea that the end of
the second month after term can be considered a period of ma-
jor transformation of the nervous system.19 During this trans-
formation, many neural functions (eg, postural control,
control of visual attention, sucking pattern, social smiling
and pleasure vocalizations, motor behavior) change within a
relatively short period of several weeks.19 Aberrant features
of these neural functions have different associations with later
neurodevelopment, depending on whether they occur before
or after this transformation. If the quality of general move-
ments is impaired before but normalizes after this transforma-
tion, poorer IQ scores are seen in very preterm children at
school age compared with children in whom general move-
ments had normalized before the transformation.20 This is
in line with our findings regarding the normalization of suck-
ing patterns after the period of this major neural transforma-
tion. The abnormal features of sucking patterns at 4-6 weeks
after term reflect damage of neural structures involved in neu-
rodevelopmental outcomes at around age 2 years.
In terms of the observed association between sucking
behavior and neurodevelopmental outcomes, our results are
Wolthuis-Stigter et al
January 2015 ORIGINAL ARTICLES

Table II. Number of infants assessed using the NOMAS Table III. ORs and 95% CIs for abnormal
at 37-50 weeks PMA neurodevelopmental outcomes at age 2 years, according
Normal development Abnormal development to sucking behaviors at 44 and 46 weeks PMA
Week (n = 39), n (n = 13), n 44 weeks PMA, 46 weeks PMA,
37 30 10 NOMAS Items OR (95% CI) OR (95% CI)
38 36 11 Arrhythmic jaw movements 6.67 (0.77-58.04) 7.90 (0.91-68.75)
39 35 12 Immature suck beyond 6.30* (1.40-28.32) 3.66 (0.88-15.19)
40 35 10 appropriate age
42 37 11 Arrhythmic tongue movements 6.36 (0.73-55.30) 7.90 (0.91-68.75)
44 37 11 Unable to sustain suck 1.83 (0.29-11.67) 6.25* (1.29-30.35)
46 34 11 Incoordination of suck, swallow, 3.89 (0.48-31.52) 3.56 (0.44-28.89)
48 36 10 respiration
50 34 10
*Significantly increased odds of abnormal neurologic development outcomes.

consistent with previous studies, but less so with regard to the
time frame earlier than 4-6 weeks postterm. Variations in
study design (eg, characteristics of the study groups, how suck-
ing behavior was assessed and at what age, age of follow-up at
which neurodevelopmental outcomes was determined) could
possibly explain this discrepancy. Medoff-Cooper et al9 evalu-
ated a 5-minute sucking test at term equivalent age as opposed
to multiple assessments of sucking behavior up to the early
postterm period in our study, and reported on both mental
and psychomotor development at 12 months vs 2 years in
our study. Tsai et al10 also assessed preterm infants at weekly
intervals with the NOMAS as we did, but used the NOMAS
diagnosis at 37 weeks to allocate infants to 1 of 2 groups,
and all infants with persistent disorganized sucking patterns
achieved normal sucking patterns before 42 weeks PMA. We
did not observe this in the present study; disorganized sucking
patterns persisted after 42 weeks PMA, to a greater degree in
the abnormal development group compared with the normal
development group. The fact that our study group included a
relatively large proportion of infants with BPD and SGA in-
Figure 1. The proportion of infants with normal sucking pat-
terns, assessed at 37-50 weeks PMA.
The Association between Sucking Behavior in Preterm Infants and Neurodevelopmental Outcomes at 2 Years of Age
fants might have contributed to these differences. Finally, in
a study by Mizuno and Ueda,11 improvement of feeding skills
between 1 and 2 weeks after oral feeding had commenced
reportedly resulted in better neurodevelopmental outcomes
at 18 months. The mean gestational age of the infants in that
study was 37.8 weeks (range, 35.1-42.7 weeks), considerably
older than that in the present study and the aforementioned
studies. This also might explain the different findings with re-
gard to the time frame.
Analysis of separate items on the NOMAS demonstrated
that only a few specific elements of sucking patterns were
associated with abnormal neurologic development, and other
elements of the sucking patterns were not associated with
neurodevelopmental outcome at all. Arrhythmic jaw move-
ments, arrhythmic tongue movements, the coordination of
sucking, swallowing, and respiration, the inability to sustain
the sucking pattern, and the absence of a mature sucking
pattern beyond appropriate age increased the odds of
abnormal neurodevelopmental outcomes at age 2 years,
although the associations of the first 3 elements failed to
reach statistical significance.
We assume that a lack of muscle strength and/or endurance
precipitated the inability to sustain sucking. In these infants,
we observed appropriate sucking for brief periods, but the
inability to sustain it for the full 2 minutes. Our results demon-
strate that this inability is associated with abnormal develop-
mental outcomes. Nieuwenhuis et al21 analyzed sucking in
detail in the same cohort of preterm infants as ours, and found
that coordinated sucking, swallowing, and respiration are spe-
cifically related to the quality of general movements of preterm
infants at age 3 months. We did not confirm this finding for
neurodevelopmental outcomes at age 2 years, but that might
be related to our small sample size. Our finding of an associa-
tion between the absence of a mature sucking pattern beyond
appropriate age and later abnormal developmental outcomes
underscores the importance of this early postterm period for
detecting possible abnormal developmental outcomes. How
and at what age after term sucking is assessed is clearly more
important than whether specific elements of sucking are
abnormal, given that the absence of a mature sucking pattern
is obviously a general item of the NOMAS.
Using the NOMAS to assess sucking skills brings both
strengths and limitations to the present study. The
29
THE JOURNAL OF PEDIATRICS  www.jpeds.com
strength of this study lies in its longitudinal and detailed
approach to assessing sucking up to 10 weeks postterm.
The NOMAS is a user-friendly and noninvasive assessment
tool, making it possible to monitor the development of
sucking skills in breast-fed and bottle-fed infants over rela-
tively long periods. Parts of the NOMAS are subjective and
open to individual judgment of the assessor, however. We
were aware of the moderate to fair interindividual and in-
traindividual reliability, and addressed this by using mul-
tiple certified assessors and by conducting a consensus
procedure.
Limitations of the present study also include the small sizes
of the study groups, resulting in the relatively wide 95% CIs
of the ORs. Of note, the abnormal development group was
only one-third the size of the normal development group.
Other limitations include the heterogeneous group of chil-
dren with abnormal developmental outcomes, and the rela-
tively large proportions of children with BPD and children
who were SGA.
We conclude by stating that to identify preterm infants at
risk for abnormal neurodevelopmental outcomes, sucking
behavior should be assessed during the early postterm period.
Specific sucking elements, such as rhythmic jaw and tongue
movements; coordination of sucking, swallowing, and respi-
ration; ability to sustain sucking; and persistence of an imma-
ture sucking pattern beyond appropriate age (ie, full term)
might identify abnormal neurologic development and merits
further study. n
We thank T. van Wulfften Palthe, PhD (professional translator), for
correcting the English in the manuscript.
Submitted for publication Mar 20, 2014; last revision received Jul 21, 2014;
accepted Sep 5, 2014.
Reprint requests: Mechteld I. Wolthuis-Stigter, MSc, Research and Innovation
Group Health Care and Nursing, Hanze University of Applied Sciences, PO
Box 3109, 9701 DC Groningen, The Netherlands. E-mail: m.i.wolthuis@pl.
hanze.nl
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Figure 2. A, Developmental course of items relating to jaw

movements in the preterm infants showing normal neurologic
development. B, Developmental course of items relating to
jaw movements in the preterm infants showing abnormal
neurologic development.
Figure 3. A, Developmental course of items relating to
tongue movements in the preterm infants showing normal
neurologic development. B, Developmental course of items
relating to tongue movements in the preterm infants showing
abnormal neurologic development.

The Association between Sucking Behavior in Preterm Infants and Neurodevelopmental Outcomes at 2 Years of Age 30.e1