Content uploaded by Bob R.J.H. Logjes
Author content
All content in this area was uploaded by Bob R.J.H. Logjes on Oct 05, 2023
Content may be subject to copyright.
Long-term speech outcome in patients with Robin sequence after cleft
palate repair and tongue-lip adhesion: A 21-year retrospective
analysis
Robrecht J.H. Logjes
a
,
b
,
1
,
*
, Joline F. Mermans
a
,
1
, Marieke J. Coerts
c
,
Birgit I. Lissenberg-Witte
d
, Corstiaan C. Breugem
e
, J. Peter W. Don Griot
a
a
Department of Plastic, Reconstructive, and Handsurgery, Amsterdam UMC, Location VU, PO box 7057, 1007 MB, Amsterdam, the Netherlands
b
Department of Speech and Language Pathology, Amsterdam UMC, Amsterdam, the Netherlands
c
ENT Department, Department of Epidemiology &Data Science, Amsterdam UMC, De Boelelaan 1118, 1081 HZ, 1007 MB, Amsterdam, the Netherlands
d
Department of Epidemiology &Data Science, Amsterdam UMC, Vrije Universiteit Amsterdam, De Boelelaan 1117, 1081 HV, Amsterdam, the Netherlands
e
Department of Plastic, Reconstructive, and Handsurgery, Amsterdam UMC, Meibergdreef 9, 1105 AZ, Amsterdam, the Netherlands
article info
Article history:
Paper received 5 June 2021
Received in revised form
21 October 2022
Accepted 22 January 2023
Available online 2 February 2023
Handling Editor: Prof. Emeka Nkenke
This manuscript was presented at: Euro-
pean Cleft-Palate Craniofacial Association
Congress in Utrecht, The Netherlands, 15th
June 2019, - 77th Annual meeting of Amer-
ican Cleft Palate-Craniofacial Association,
Portland, USA, 31st March e4th April 2020
(cancelled last minute due to Covid-19
pandemic), - 35th Annual meeting Dutch
Cleft-Palate Craniofacial Association
Congress in Zwolle, The Netherlands, 21th
November 2020, - 78th Annual virtual
meeting of American Cleft Palate-
Craniofacial Association, 29th April e1st
May 2021.
Keywords:
Robin sequence
Cleft palate repair
Tongue-lip adhesion
Speech
Velopharyngeal insufficiency
Articulation
abstract
The purpose of this study was to assess the effect of tonguelip adhesion (TLA) on the long-term speech
and articulation outcomes of patients with Robin sequence (RS) after cleft palate repair. Outcomes were
compared to those in patients with RS who required positioning alone and to patients with isolated cleft
palate (ICP).
All consecutive patients with RS (with or without TLA) versus isolated cleft palate (ICP) who un-
derwent cleft palate repair were retrospectively reviewed. Speech and articulation included all assess-
ments between the age of 3e6 years. Secondary speech operations, velopharyngeal insufficiency (VPI),
hypernasality, and articulation errors by cleft-type characteristics (CTC), including 4 categories (passive),
non-oral, anterior-oral, and posterior-oral. A total of 41 RS patients and 61 ICP patients underwent repair
with sufficient follow-up. Of them, 23 patients underwent a TLA at median age of 12 days. Rates of
hypernasality (p ¼0.004), secondary speech operations (p ¼0.004), and posterior oral CTC (p ¼0.042)
were higher in RS compared to ICP. Isolated RS had speech outcomes similar to those of ICP; however,
syndromic RS patients needed more secondary speech operations compared to isolated RS (p ¼0.043).
TLA-RS patients did not demonstrate differences in speech outcomes or any CTCs (all p >0.05) compared
to nonTLA-RS patients, except for the anterior oral CTC (74% TLA-RS vs 28% nonTLA-RS, p ¼0.005).
Within the limitations of the study, it seem that TLA does not affect long-term velopharyngeal
function in patients with RS. However, TLA-RS patients demonstrated higher rates of anterior-oral CTC,
which might be related to a different positioning of the tongue after TLA. Every effort should be taken to
treat patients with RS conservatively instead of with TLA because of this demonstrated a negative effect
on one type of articulation error. However, if conservative therapy fails, a TLA is still a valuable adjunct in
the treatment of RS, and cleft speech pathologists who treat such patients should be more aware of this
phenomenon in order to improve long-term articulation outcomes.
©2023 Published by Elsevier Ltd on behalf of European Association for Cranio-Maxillo-Facial Surgery.
1. Introduction
Robin sequence (RS) is a congenital anomaly in newborns that
was clinically defined in 1923 by the triad of micrognathia, glos-
soptosis, and upper airway obstruction (UAO) (Robin, 1923). RS may
*Corresponding author.
E-mail addresses: r.j.h.logjes@gmail.com (R.J.H. Logjes), j.mermans@
amsterdamumc.nl (J.F. Mermans), mj.coerts@amsterdamumc.nl (M.J. Coerts), c.c.
breugem@amsterdamumc.nl (C.C. Breugem), DonGriot@amsterdamumc.nl
(J.P.W. Don Griot).
1
Shared first authors.
Contents lists available at ScienceDirect
Journal of Cranio-Maxillo-Facial Surgery
journal homepage: www.jcmfs.com
https://doi.org/10.1016/j.jcms.2023.01.012
1010-5182/©2023 Published by Elsevier Ltd on behalf of European Association for Cranio-Maxillo-Facial Surgery.
Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
occur in isolation, as part of a syndrome (e.g., Stickler syndrome or
TreacherCollins syndrome), or with additional anomalies or
chromosomal defects but without a (yet) identified associated
syndrome, classified as “RS-plus”(Tan et al., 2013;Basart et al.,
2015;Breugem et al., 2016;Xu et al., 2016;Logjes et al., 2018).
Cleft palate was added as an associated malformation, but is not
considered a prerequisite for the diagnosis (Robin, 1923;Breugem
et al., 2016).
Diagnostic criteria and treatments for RS vary widely among
centers (Breugem et al., 2016;Logjes et al., 2021). If there is evi-
dence of UAO that is not successfully managed by positioning alone,
numerous operations such as mandibular distraction (MDO) or
tonguelip adhesion (TLA) could be performed (Van Lieshout et al.,
2016). At the Amsterdam Medical Center location VUmc, if there is
evidence of UAO that is not successfully managed by positioning
alone or by positioning and nasogastric feeding, a TLA is performed
(Bijnen et al., 2009;Mermans et al., 2018).
TLA, first advocated by Shukowsky in 1911, is usually performed
in the first few weeks of life and involves surgically tethering the
tongue forward to the lower lip, relieving UAO caused by micro-
gnathia and glossoptosis (Viezel-Mathieu et al., 2016). The pro-
cedure is usually reversed between 9 and 12 months of age at the
time of palate repair (Bijnen et al., 2009).
The period from birth to 30 months of age includes critical
phases in the acquisition of speech and language (Hasenstab,1982).
Patients with a cleft palate might develop difficulty with speech
and language development due to velopharyngeal insufficiency
(VPI) that can result in hypernasality in speech and multiple
articulation disorders (Hasenstab, 1982;John et al., 2006;Spruijt
et al., 2018). In addition, patients with RS and severe UAO who
undergo TLA might develop extra difficulties in speech and or
articulation development. The tongue and lip are affected by TLA,
and these articulators are vital in the production of early devel-
oping speech sounds (LeBlanc and Golding-Kushner, 1992).
TLA is commonly used with current practice in Europe and
United States, ranging from 20% to 27% if surgical intervention is
indicated (Scott and Mader, 2014,Van Lieshout et al., 2015;Resnick
et al., 2018). The long-term effect on speech and articulation out-
comes after TLA and subsequently cleft palate repair is unknown. In
order to improve care, this information would be of great value in
counseling families of patients with RS, and for physicians and cleft
speech pathologist involved in the care of patients with RS. It was
the aim of this study to assess the effect of TLA on the long-term
speech and articulation outcomes of patients with RS after cleft
palate repair.
2. Materials and methods
For this study, approval by the institutional review board was
obtained (number: FWA00017598). A retrospective chart review
was performed of all consecutive patients with RS that underwent a
Von Langenbeck repair with intravelar veloplasty between 1993
and 2014 and compared to patients with ICP. RS was defined as
micrognathia, glossoptosis and UAO (Bijnen et al., 2009;Mermans
et al., 2018).
In patients with isolated RS or isolated ICP, there was clear
documentation of no associated syndrome or any other congenital
anomalies after genetic evaluation. All patients received treatment
by the multidisciplinary cleft team. This included evaluation by a
pediatrician and early genetic screening by a clinical geneticist to
investigate for a possible underlying syndrome or for additional
anomalies or chromosomal defects but without a (yet) identified
associated syndrome (RS plus), referred to as “syndromic RS.”If no
syndrome was found, we refer to these patients as those with
“isolated RS.”
A more detailed description of the TLA procedure performed for
UAO is reported separately by one of the senior surgeons (J.P.D.G.)
(Bijnen et al., 2009).
Cleft palate repair was performed between 9 and 12 months of
age, and in patients with RS plus TLA, the takedown was usually
performed at the same time. If performed preoperatively, cleft
palate anatomy did not allow one-stage closure of the hard and soft
palate, and delayed repair of the hard palate was performed at a
later stage, referred to as “remaining anterior cleft”in this article.
Fistula was defined in patients who underwent a primary total cleft
palate repair and later developed an oronasal fistula.
Data retrieved included date of birth, sex, cleft palate type (soft
palate only or soft and hard palate), associated syndromes with RS,
age at TLA (in days), age at cleft palate repair (in months), fistula,
the need for a secondary speech operation to resolve VPI, the age at
time of secondary speech operation (in years) if applicable, and
perceptual speech outcomes. This included binary speech out-
comes (present or absent), without grading by a quantitative scale,
for VPI, hypernasality, and articulation errors.
2.1. Perceptual speech assessment
The senior craniofacial speech pathologist of the multidisci-
plinary cleft team assesses speech outcomes at different ages using
the Dutch cleft speech evaluation test (DCSET) (Spruijt et al., 2018;
Meijer, 2003). During these perceptual speech assessments
hypernasality and articulation errors are assessed live, based on a
short sample of connected speech or separate words, and are
classified. In the present retrospective analysis, all perceptual
speech assessments between the ages of 3 and 6 years were
included. Medical charts were reviewed by the third author (M.J.C),
who has more than 20 years of experience with assessment of
speech of children with cleft lip and palate. The diagnosisof VPI as a
binary outcome was made if hypernasality and/or one of the pas-
sive cleft articulation errors was present during one of these
assessments.
Patients with cleft palate can demonstrate consonant errors in
articulation, the so-called “cleft type characteristics”(John et al.,
2006). These consonant errors can be categorized based on the
nature of the error, primarily in relation to the place of articulation
in the oral cavity or pharynx. Therefore, these cleft-type charac-
teristics (CTC) were classified into 4 categories: (1) anterior oral
(retraction, palatalization, lateralization, inter/addentality, front-
ing); (2) posterior oral (backing); (3) non-oral (glottal realization,
glottal endorsement, pharyngeal fricative, active nasal fricative);
and (4) passive (nasal emission, nasal turbulence, nasal realization).
All 4 of these different CTC categories were assessed as binary
outcome (present or absent).
Besides hypernasality, passive and nonoral articulation errors
are indicators directly related to VPI, whereas the anterior-oral and
posterior oral CTC in speech can also have causes other than VPI
related to different oral morphology. These causes can include a
fistula, dental issues and/or tongue problems such as a misplaced
tongue placement or a hypotonic or reduced mobile tongue muscle
due to a short frenulum.
In patients with a fistula or a remaining cleft of the anterior hard
palate at time of speech evaluation, nasal air loss due to VPI was
distinguished from nasal air loss due to a fistula by temporary fis-
tula closure of the fistula during the perceptual speech assessment
of the senior cleft speech pathologist. In patients with significant
nasal air loss due to inadequate velopharyngeal function, another
speech operation in the form of a pharyngeal flap was performed to
resolve VPI.
Exclusion criteria were as follows: patients with severe mental
retardation, as this could influence speech development and
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
210
outcome; patients who were not assessed by the multidisciplinary
cleft team pre- and postoperatively; patients who did not have
speech assessments available between the age of 3 and 6 years;
patients in whom phonology was not completely developed by the
time of speech assessment; and patients with a submucous cleft
palate.
2.2. Statistical analysis
Data were collected in Excel (Microsoft Corporation) and
analyzed using IBM SPSS version 25.0 (IBM Corporation). To
compare the main outcomes between groups, contingency tables
(with corresponding
c
2
test or Fisher exact test) were used for the
categorical variables. For normally distributed variables, the
independent-samples t-test and for nonnormally distributed
variables the MannWhitney Utest was used. All data are given as
frequency (percentage), mean ±standard deviation (SD) or median
(interquartile range [IQR]) in the case of categorical data, normal
data, and non-normal continuous data, respectively.
If the type of cleft or the presence of a remaining anterior cleft
differed significantly between groups being compared, we tested
their association with the speech and articulation outcomes. In case
of a significant association, we performed additional multivariable
logistic regression analysis to correct for this difference when
comparing groups. A p value of <0.05 was considered statistically
significant.
3. Results
3.1. Patient characteristics
After exclusion, a total of 41 consecutive patients with RS and 61
patients with ICP who required cleft palate repair, at median ages of
9.3 and 9.4 months (p ¼0.79), respectively, were selected. Patient
characteristics are presented in Table 1. The senior author (J.P.D.G.)
performed the majority of the cleft palate repairs (n ¼63, 21 RS vs
42 ICP), followed by two other cleft surgeons (n ¼22, 13 RS vs 9 ICP)
and (n ¼17, 7 RS vs.10 ICP) (p ¼0.11). Cleft palate characteristics
included the following: soft palate only in 24% of patients with RS
vs 59% of patients with ICP, and soft plus hard palate in 76% of
patients with RS vs 41% patients with ICP (p ¼0.001).
Of the 41 patients with RS, 23 underwent a TLA and the
remaining 18 underwent prone positioning (Table 1). The median
age for TLA was 12 days, and the majority of patients (21 of 23) had
TLA release during cleft palate repair (Table 1).
A total of 23 patients with RS had a syndromic diagnosis versus
18 isolated patients with RS. There was no difference in age at time
of repair (9.4 vs 9.2 months, respectively, p ¼0.207) (Table 1). Ten
of the 18 isolated patients with RS underwent TLA, versus 13 of the
23 syndromic patients with RS (p ¼0.951).
3.2. Surgical outcomes
Surgical outcomes are demonstrated in Table 2 and Fig. 1. Pa-
tients with RS required significantly more delayed closures of the
remaining anterior cleft of the hard palate (24%) compared to pa-
tients with ICP (8%) (p ¼0.024). Fistula after primary closure of the
total cleft palate that needed surgical repair occurred in 3 with RS
and 3 patients with ICP (p ¼0.61). Patients with RS needed more
secondary speech operations to resolve VPI (51%) compared to
patients with ICP (23%) (p ¼0.004). In the RS group, patients with
syndromic RS underwent significant more secondary speech op-
erations to resolve VPI (61%) compared to patients with isolated RS
(33%) (p ¼0.043). No difference was observed in secondary speech
operations between isolated RS versus ICP (23% vs 33%, p ¼0.37)
and between TLA-RS vs nonTLA-RS (57% vs 44%, p ¼0.54).
3.3. Speech outcomes
The median age at time of all speech evaluations was 4.5 years
(range: 3.0e6.3 years) in the RS group versus 4.6 years (range:
3.3e6.3 years) in the ICP group (p ¼0.58). The mean number of
speech evaluations was 2.51 (SD ±0.90) in patients with RS versus
2.15 (SD ±0.77) in patients with ICP (p ¼0.031).
3.4. Patients with RS (n ¼41) vs patients with ICP (n ¼61)
Patients with RS demonstrated higher rates of hypernasality
(p ¼0.004) than patients with ICP, with 59% (24 of 41) vs 30% (18 of
61) respectively (Table 3,Fig. 1). When comparing the CTC rates
between the two groups, the RS group had more posterior oral
speech CTC than the ICP group, with 34% (14 of 41) vs 16% (10 of 61)
Table 1
Patient characteristics.
RS (%) ICP (%) P-value
No. Patients 41 61
Male: female ratio 17:24 (41:59) 24:37 (39:61) 0.831
Type cleft palate 0.001
Soft palate 10 (24) 36 (59)
Soft þhard palate 31 (76) 25 (41)
Median age at CP-repair in months (range) 9.3 (8.3e42.5) 9.4 (8.3e31.7) 0.79
Type of RS Syndromic RS(%) Isolated (%) P-Value
23 (56) 18 (44)
6 Stickler syndrome (26)
1 Fragile X- syndrome (4)
1 Carbohydrate deficient glycoprotein syndrome (4)
1 Van den Ende-Gupta syndrome (4)
1 Trichorhinophalangeal syndrome (4)
1 22q11.2 deletion syndrome (4)
12 Other associated anomalies or chromosomal abnormalities (RS-plus) (52)
Age at CP repair in months (range) 9.4 (8.5e24.5) 9.2 (8.3e10.6) 0.207
Total RS group
Treatment for UAO TLA (%) Prone positioning (%)
Time TLA in days (range) 23 (56) 18 (44)
12 (2e100)
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
211
(p ¼0.042). There were no differences in VPI, passive, anterior-oral,
or non-oral CTC rates (Table 3,Fig. 1).
There was a lower rate of hypernasality in the soft palateonly
cleft group, with 17% (8 of 46), compared to the soft and hard palate
cleft group with 61% (34 of 56) (p <0.001), and in the non-anterior
Table 2
Surgical outcomes.
RS (%) ICP (%) p- value
Delayed closure hard palate required 10 (24) 5 (8) 0.024
Delayed closure hard palate performed 8 2
Timing closure (median years (IQR)) 8.2 (3.6e10.0) 7.8 &8.5 (N/A)
Fistula 3 (7) 3 (5) 0.614
Fistula repair 3 2
Timing repair (median years (IQR)) 6.2 (3.2e9.7) 6.0 &6.3
Secondary speech surgery 21 (51) 14 (23) 0.004
I-RS (%) S-RS (%)
6 (33) 15 (61) 0.043
TLA No TLA
13 (57) 8 (44) 0.54
Pharyngeal flap 20 14
Age (median years (IQR)) 3.9 (3.2e7.4) 4.3 (2.9e10.2)
Redo palate 1
Age (year) 18.5
Fig. 1. Speech outcomes RS vs ICP, isolated RS and syndromic RS. RS: Robin sequence, ICP: isolated clef t palate, S-RS: Syndromic RS, I-RS: Isolated RS, VPI: velopharyngeal
insufficiency.
Table 3
Speech and articulation outcomes.
Patients RS (%) ICP (%) p-value corrected p-values TLA-RS (%) non-TLA-RS (%) p-value
VPI 73 62 0.26 0.74 (0.021*&1.0**)78 67 0.49
secondary speech operations 51 23 0.004 0.035 (0.23*&0.210**)57 44 0.54
hypernasality 59 30 0.004 0.16 (0.002*&0.070**) 65 50 0.36
CTC
passive 51 57 0.54 0.15 (0.006**)52 50 1.0
non-oral 24 25 0.98 0.71 (0.13**)26 22 1.0
anterior oral 54 41 0.21 0.43 (0.046**)74 28 0.005
posterior oral 34 16 0.042 0.21 (0.001**) 30 39 0.74
When comparing the RS-group vs. the ICP group the variables type of cleft palate &anterior cleft palate were both significantly different and demonstrated an association with
the outcomes VPI, hypernasality and secondary speech operations, and therefore the corrected p-value was calculated to correct for these 2 possible confounders.
*p-value for type of cleft palate in corrected model.
**p-value for the presence of an anterior cleft in corrected model.
When comparing the RS group vs. ICP group the variable anterior cleft palate was significantly different and demonstrated an association with the outcomes passive, non-oral,
anterior oral and posterior oral articulation groups, and therefore the correct p-value only included correction for the presence of an anterior cleft, to correct for this possible
confounder.
For the comparison TLA-RS vs. non-TLA-RS, none of the variables was significantly different between these two groups.
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
212
cleft group with 35% (30 of 87) compared to the remaining anterior
cleft group with 80% (12 of 15) (p ¼0.001). After correction for type
of cleft and the presence of a remaining anterior cleft using
multivariable logistic regression, there was no significant difference
in hypernasality (p ¼0.16). For the articulation outcomes, only
correction for the presence of a remaining anterior cleft was
necessary, and resulted in a non-significant difference in posterior
oral CTC rates between RS and ICP (p ¼0.21) (Table 3).
3.5. Syndromic patients with RS (n ¼23) vs isolated patients with
RS (n ¼18)
No difference was found for VPI or hypernasality rates between
the isolated and syndromic patients with RS (p ¼0.41, p ¼0.33,
respectively) (Fig. 1). However, syndromic patients with RS un-
derwent more secondary speech operations to resolve VPI (61%)
compared to isolated patients with RS (33%) (p ¼0.043).
3.6. Isolated patients with RS (n ¼18) vs patients with ICP (n ¼61)
There was no difference in VPI rates between isolated RS and ICP
(p ¼0.74), with 67% (12 of 18) compared to 62% (38 of 61), or in
hypernasality (p ¼0.11) or required secondary speech surgery
(p ¼0.37) (Fig. 1).
3.7. NonTLA-RS (n ¼18) vs TLA-RS (n ¼23)
The TLA-RS group had more anterior oral CTC with 74% (17 of 23)
compared to 28% (5 of 18) in the nonTLA-RS group (p ¼0.005).
There were no differences in rates of VPI (p ¼0.49), hypernasality
(p ¼0.36), secondary speech operations (p ¼0.54), and passive,
non-oral or posterior oral CTCs (Table 3,Fig. 2).
When examining the different errors in the anterior-oral CTC
group, lateralization, inter- or addentality and fronting demon-
strated higher rates in the TLA group; however, only retraction
neared statistical significance (35% TLA-RS vs 6% nonTLA-RS,
p¼0.054) (Fig. 3).
3.8. Isolated nonTLA-RS patients (n ¼8) compared to isolated
TLA-RS patients (n ¼10)
No difference was found for VPI (p ¼1.00), hypernasality scores
(p ¼0.64), secondary speech surgery (p ¼0.64), or any of the 4
different CTC categories. Nevertheless, a higher rate of anterior-oral
CTC was seen in the isolated TLA-RS patients, with 70% (7 of 10),
compared to 25% (2 of 8) in the isolated nonTLA-RS patients
(p ¼0.15) (Fig. 3). Since a total of 18 patients could be included in
this analysis, it should be stated that this analysis is underpowered.
4. Discussion
This study was initiated to assess the long-term effect of TLA on
the long-term speech and articulation outcomes of patients with RS
after cleft palate repair. To achieve this, outcomes were retrospec-
tively compared with a nonTLA-RS group and with an ICP group.
This made it possible to comprehensively study the effects of TLA
on long-term speech outcomes that included assessments of
hypernasality and articulation by different groups of CTC (John
et al., 2006).
The present study showed that TLA-RS patients have more
anterior-oral CTC (74%), compared to nonTLA-RS patients (28%)
(p ¼0.003) (Fig. 2). LeBlanc et al. suggested that TLA seemed to
disrupt early speech development by delaying sound production,
but after detachment this development accelerated and TLA-RS
patients seemed to “catch-up”(LeBlanc and Golding-Kushner,
1992). However, the authors observed compensatory adaptations
in lingual posturing that were maintained after TLA release and that
affected the production of lingua-alveolar phonemes in more than
half of the patients with RS up to 18 months after TLA release.
Although visual distortion in speech was observed by the use of the
tongue blade instead of the tongue tip, the production of these
lingua-alveolar sounds was judged to be accurate perceptually
(LeBlanc and Golding-Kushner, 1992). The results of the present
study provide longer follow-up when compared to the study by
LeBlanc et al., and could be explained by the effect of the TLA, since
the anterior oral CTC are associated with the placement of the
tongue. Possible causes of this altered tongue placement after TLA
could be scarring, neural injury caused by the pull-out suture
Fig. 2. Speech and articulation outcomes TLA-RS vs nonTLA-RS. RS: Robin sequence, ICP: isolated cleft palate, VPI: velopharyngeal insufficiency, CTC: cleft type characteristics,
TLA: tongue-lip adhesion.
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
213
(dysphagia), long-term positioning of the tongue in a lower ante-
rior position, or altered motoric brain innervation.
When looking more specifically in the different errors of the
anterior-oral group, lateralization, inter- or addentality and front-
ing demonstrated higher rates in the TLA-RS group; however, only
retraction neared statistical significance (p ¼0.054) (Fig. 3). Cleft
speech pathologists who work with this population should be
aware of the potential lingual articulation errors with patients who
present with a history of TLA.
No differences were found between TLA-RS patients and non-
TLA-RS patients on long-term speech outcomes. This is in line
with previous research that investigated VPI outcomes in patients
with RS and a TLA for airway compromise (Stransky et al., 2013;
Logjes et al., 2021). This can be interpreted in two ways: the
severity of UAO on itself does not correlate with long-term speech
outcomes, or the effect of the surgical procedure TLA does not affect
long-term velopharyngeal function. However, the indication to
perform a TLA was not based purely on objective PSG data in all
patients but rather on clinical assessment as well (Mermans et al.,
2018). Sometimes, in severe clinical cases, a TLA was performed
after the patient needed to be intubated because of severe UAO.
Therefore, the present data suggest, as expected, that the surgical
procedure TLA does not affect long-term velopharyngeal function.
The passive (nasal emission, nasal turbulence, nasal realization)
and nonoral (glottal realization, glottal endorsement, pharyngeal
fricative and active nasal fricative) CTC are errors that are indicators
directly related to VPI. The finding that TLA does not affect long-
term velopharyngeal function is confirmed by the demonstrated
rates: passive CTC 52% TLA-RS vs 50% nonTLA-RS (p ¼1.00) and
nonoral CTC 26% TLA-RS vs 22% nonTLA-RS (p ¼1.00).
Furthermore, the overall findings in the present study suggest
that surgical and speech outcomes are significantly worse for pa-
tients with RS compared to patients with ICP. Patients with RS
require more delayed closure of the hard palate (24% RS vs 8% ICP,
p¼0.024) and secondary speech surgery for VPI (51% RS vs 23% ICP,
p¼0.004). Also, patients with RS had worse hypernasality scores
Fig. 3. Anterior oral CTC TLA-RS vs nonTLA-RS and TLA-isolated-RS vs nonTLA-isolated RS. RS: Robin sequence, CTC: cleft type characteristics, TLA: tongue-lip adhesion, I-RS:
Isolated RS, VPI: velopharyngeal insufficiency.
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
214
(59% RS vs 30% ICP, p ¼0.004) and worse posterior-oral CTC, in
specific backing (34% RS vs 16% ICP, p ¼0.042), compared to the ICP
group.
Comparison of the present findings with other published
studies is challenging because of the variability of the comparison
groups and outcome measures used. To date, several studies have
investigated speech outcomes in patients with RS (Lehman et al.,
1995;Witt et al., 1997;Khosla et al., 2008;deBuys Roessingh
et al., 2008;Goudy et al., 2011;Patel et al., 2012;Stransky et al.,
2013;Black and Gampper, 2014;Basta et al., 2014;Filip et al.,
2015;Hardwicke et al., 2016;Morice et al., 2018;Kocaaslan et al.,
2020;Gustafsson et al., 2020;Logjes et al., 2021;Schwaiger et al.,
2021). However, these studies have reported both similar and
contrasting results on speech outcomes. Two prior speech out-
comes studies investigated speech outcomes and different articu-
lations errors in patients with RS vs patients with ICP (Hardwicke
et al., 2016;Logjes et al., 2021). Hardwicke et al. found worse
speech outcomes in patients with RS, with significantly more VPI,
hypernasality, higher rates of posterior-oral and non-oral CTC and
no differences in anterior-oral or passive CTC (Hardwicke et al.,
2016). Logjes et al. investigated the passive and non-oral CTC and
found, besides higher VPI rates, significant higher rates of non-oral
CTC in patients with RS, which, as previously stated, is an indicator
directly related to VPI (Logjes et al., 2021). We found significant
higher rates of the posterior-oral CTC in patients with RS, which is
in line with Hardwicke et al. (2016), but does not directly correlate
with VPI.
In this study, after statistical correction for cleft-type and/or
presence of anterior cleft, no statistical significant difference was
found between RS and ICP for hypernasality (p ¼0.16) or posterior
oral CTC (p ¼0.21) (Table 3). This could suggest that the severity of
the cleft plays a major role (p ¼0.002) and the presence of an
anterior cleft a minor role (p ¼0.070) in defining the difference in
hypernasality and not the RS sequence. Logjes et al. investigated
predictors for VPI in patients with RS by multivariable logistic
regression analysis, and found, despite the different cleft palate
etiology, no increased odds for VPI in isolated patients with RS
compared to patients with ICP. The only independent predictor for
VPI was a more severe and wider cleft palate anatomy when con-
trolling for different variables (Logjes et al., 2021).
.
Other studies
have demonstrated cleft palate width to be an independent pre-
dictor for VPI in cleft lip and/or palate patients (Lam et al., 2012;
Mahoney et al., 2013;Leclerc et al., 2014;Lee et al., 2015;Yuan et al.,
2016;Wu et al., 2017;Botticelli et al., 2020). Patients with RS often
have a U-shaped cleft palate caused by the superiorly and poste-
riorly displaced tongue. A wider and more severe cleft palate might
result in an impaired embryological development of the soft palate
muscles compared to that if patients with a smaller and less severe
cleft palate. After clef t palate repair, these factors may all contribute
to a shorter and less mobile velum (Logjes et al., 2018,2021).
Previous cited studies found VPI rates ranging from 0% to 58% in
patients with RS (Lehman et al., 1995;Witt et al., 1997;Khosla et al.,
2008;deBuys Roessingh et al., 2008;Goudy et al., 2011;Patel et al.,
2012;Stransky et al., 2013;Black and Gampper 2014;Basta et al.,
2014;Filip et al., 2015;Hardwicke et al., 2016;Morice et al., 2018;
Kocaaslan et al., 2020;Gustafsson et al., 2020;Logjes et al., 2021;
Schwaiger et al., 2021). The present study demonstrated higher
rates of VPI in the RS group (73%) and in the ICP group (63%)
compared to the literature. This can be explained by the outcome
diagnosis of VPI as binary outcome was made if hypernasality and/
or one of the cleft articulation errors was present during one of the
multiple assessments per individual patient. VPI was not assessed
on a quantitative scale, ranging from mild to severe, and therefore,
for example, patients who demonstrated no hypernasality but one
single articulation error in the non-oral or passive groups were
diagnosed with the presence of VPI. When looking at the presence
of hypernasality (59% RS vs 30% ICP, p ¼0.003) and the need for
secondary speech operation (51% RS vs 23% ICP, p ¼0.003), these
rates are in line with the current literature.
Finally, non-surgical treatment for airway compromise in pa-
tients with RS, such as the pre-epiglottal baton plate approach with
velar extension, might replace most other forms of surgical treat-
ment such as TLA if applied by a comprehensive cleft team in the
future (Bacher et al., 2011). This pre-epiglottal baton plate treat-
ment has demonstrated excellent long-term results in many
treatment aspects in patients with RS (breathing, sleep apnea,
speech) and could help to avoid articulation errors in patients with
RS in the future (Poets et al., 2019).
The present study is limited by its retrospective design and the
completeness of the data that is determined by the level of accuracy
of the previously reported medical files.
Therefore, we could retrieve only the severity of the cleft palate
and not the exact length and width of the cleft. A recent study
demonstrated that a wider cleft palate significantly correlates with
a higher Veau classification (Wu et al., 2017). We assume that this is
also applicable for the RS and ICP cohort in the present study.
Regarding the surgical outcome of occurrence of fistula, we
included only patients who had sufficient speech follow-up from
the age of 3 years or older. Therefore, the present study might be
subject to selection bias. The speech outcomes were assessed by a
two-level scale: present or absent. In statistics, as applied to
perceptual judgments, we learn that the fewer the rankings on a
rating scale, the more valid and reliable the outcomes will be. The
present study reported used perceptual speech analysis that was
recently converted to a universal score for international compari-
son (Spruijt et al., 2018;Meijer, 2003).
Perceptual speech evaluation by speech pathologists is subject
to inter- and intrarater variability (Spruijt et al., 2018). In this study,
a total of six craniofacial speech pathologists assessed perceptual
speech evaluations in our cohort of patients. However, this was not
evaluated by audio and/or video recordings, making a calculation of
the inter- and intrarater reliability impossible. In addition, speech
outcomes can differ with age; however, age at speech assessment
was not controlled for in our included speech assessments from age
3e6 years.
Despite these limitations, the present study demonstrates new
insights into the long-term speech and articulation outcomes in
patients with RS who undergo a TLA.
5. Conclusion
Within the limitations of the study, it seem that TLA does not
affect long-term velopharyngeal function in patients with RS.
However, TLA-RS patients demonstrated higher rates of anterior-
oral CTC, which might be related to a different positioning of the
tongue after TLA. Every effort should be taken to treat patients with
RS conservatively instead of with TLA because of this demonstrated
a negative effect on one type of articulation error. However, if
conservative therapy fails, a TLA is still a valuable adjunct in the
treatment of RS, and cleft speech pathologists who treat such pa-
tients should be more aware of this phenomenon in order to
improve long-term articulation outcomes.
Funding
This research did not receive any funding.
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
215
Medical ethical board approval
This study was approved by the medical ethical board of the
Amsterdam University Medical Centers, Location VU, The
Netherlands (FWA00017598).
Declaration of competing interest
None of the authors report any conflicts of interest. None of the
authors have a financial interest in any of the products, devices, or
drugs mentioned in this article.
References
Bacher, M., Sautermeister, J., Urschitz, M.S., Buchenau, W., Arand, J., Poets, C.F., 2011.
An oral appliance with velar extension for treatment of obstructive sleep apnea
in infants with pierre Robin sequence. Cleft Palate Craniofac J 48, 331e336.
Basart, H., Paes, E.C., Maas, S.M., van den Boogaard, M.J.H., van Hagen, J.M.,
Breugem, C.C., Cobben, J.M., 2015. Etiology and pathogenesis of Robin sequence
in a large Dutch cohort. Am. J. Med. Genet. 167A, 1983e1992.
Basta, M.N., Silvestre, J., Stransky, C., Solot, C., Cohen, M., McDonald-McGinn, D.,
Zackai, E., 2014. A 35-year experience with syndromic cleft palate repair:
operative outcomes and long-term speech function. Ann. Plast. Surg. 73,
130e135.
Bijnen, C.L., Griot Jpw, Don, Mulder, W.J., Haumann, T.J., Van Hagen, A.J., 2009.
Tongue-lip adhesion in the treatment of pierre Robin sequence. J. Craniofac.
Surg. 20, 315e320.
Black, J.S., Gampper, T.J., 2014. Transverse mucoperiosteal flap inset by rotation for
cleft palate repair: technique and outcomes. Ann. Plast. Surg. 72, 90e93.
Botticelli, S., Kuseler, A., Molsted, K., Andersen, H.S., Boers, M., Shoeps, A.,
Emborg, B.K., 2020. Influence of infant cleft dimensions on velopharyngeal
function in 5-year-old Danish children born with unilateral cleft lip and palate.
Cleft Palate Craniofac J 57, 420e429.
Breugem, C.C., Evans, K.N., Poets, C.F., Suri, S., Picard, A., Filip, C., Paes, E.C., 2016.
Best practices for the diagnosis and evaluation of infants with Robin sequence:
a clinical consensus report. JAMA Pediatr. 170, 894e902.
Buys Roessingh, A.S., Herzog, G., Cherpillod, J., Trichet-Zbinden, C., Hohlfeld, J.,
2008. Speech prognosis and need of pharyngeal flap for non syndromic vs
syndromic pierre Robin sequence. J. Pediatr. Surg. 43, 668e674.
Filip, C., Feragen, K.B., Lemvik, J.S., Lindberg, N., Andersson, E.M., Rashidi, M.,
Matzen, M., Hogevold, H.E., 2015. Multidisciplinary aspects of 104 patients with
pierre Robin sequence. Cleft Palate Craniofac J 52, 732e74 2.
Goudy, S., Ingraham, C., Canady, J., 2011. The occurrence of velopharyngeal insuf-
ficiency in pierre Robin sequence patients. Int. J. Pediatr. Otorhinolaryngol. 75,
1252e1254.
Gustafsson, C., Vuola, P., Leikola, J., Heli€
ovaara, A., 2020. Pierre Robin sequence:
incidence of speech-correcting surgeries and fistula formation. Cleft Palate
Craniofac J 57, 344e351.
Hardwicke, J.T., Richards, H., Cafferky, L., Underwood, I., Horst, B., Slator, R., 2016.
Outcomes of cleft palate repair in patients with pierre Robin sequence: a
matched case-control study. Plast. Reconstr. Surg. 137, 927e935.
Hasenstab, M.S., 1982. Language Acquisition in Infancy: A Basis for Assessment
through Observation, vol. 3, 14 27.
John, A., Sell, D., Sweeney, T., Harding-Bell, A., Williams, A., 2006. The cleft audit
protocol for speech-augmented: a validated and reliable measure for auditing
cleft speech. Cleft Palate Craniofac J 43, 272e288.
Khosla, R.K., Mabry, K., Castiglione, C.L., 2008. Clinical outcomes of the furlow Z-
plasty for primary cleft palate repair. Cleft Palate Craniofac J 45, 501e510.
Kocaaslan, F.N.D., Sendur, S., Koçak, I., Çelebiler,
€
O., 2020. The comparison of pierre
Robin sequence and non-syndromic cleft palate. J. Craniofac. Surg. 31, 226e229.
Lam, D.J., Chiu, L.L., Sie, K.C.Y., Perkins, J.A., 2012. Impact of cleft width in clefts of
secondary palate on the risk of velopharyngeal insufficiency. Arch. Facial Plast.
Surg. 14, 360e364.
LeBlanc, S.M., Golding-kushner, K.J., 1992. effect of glossopexy on speech sound
production in Robin sequence. Cleft Palate Craniofac J 29, 239e245.
Leclerc, J.E., Godbout, A., Arteau-Gauthier, I., Lacour, S., Abel, K., McConnell, E.M.,
2014. We can predict postpalatoplasty velopharyngeal insufficiency in cleft
palate patients. Laryngoscope 124, 561e569.
Lee, J.S., Kim, J.B., Lee, J.W., Yang, J.D., Chung, H.Y., Cho, B.C., Choi, K.Y., 2015. Factors
prognostic for phonetic development after cleft palate repair. J. Cranio-Maxillo-
Fac. Surg. 43, 1602e1607.
Lehman, J.A., Fishman, J.R., Neiman, G.S., 1995. Treatment of cleft palate associated
with Robin sequence: appraisal of risk factors. Cleft Palate Craniofac J 32 (25
29).
van Lieshout, M.J., Joosten, K.F.M., Mathijssen, I.M.J., Koudstaal, M.J., Hoeve, H.L.J.,
van der Schroeff, M.P., Wolvius, E.B., 2015. Robin sequence: a European survey
on current practice patterns. J. Cranio-Maxillo-Fac. Surg. 43, 1626e1631.
van Lieshout, M.J., Joosten, K.F., Mathijssen, I.M.J., Koudstaal, M.J., Wolvius, E.B., van
der Schroeff, M.P., 2016. J. Cranio-Maxillo-Fac. Surg. 44, 1871e1879.
Logjes, R.J.H., Breugem, C.C., Van Haaften, G., Paes, E.C., Sperber, G.H., van den
Boogaard, M.J.H., Farlie, P.G., 2018. The ontogeny of Robin sequence. Am. J. Med.
Genet. 176, 1349e1368.
Logjes, R.J.H., Upton, S., Mendelsohn, B.A., Breugem, C.C., Hoffman, W.Y.,
Pomerantz, J.H., 2021a. Long-term speech outcomes of cleft palate repair in
Robin sequence versus isolated cleft palate. Plast Reconstr Surg Glob Open 21,
e3351.
Logjes, R.J.H., MacLean, J.E., de Cort, N.W., Poets, C.F., Abadie, V., Joosten, K.F.M.,
Resnick, C.M., 2021b. Objective measurements for upper airway obstruction in
infants with Robin sequence: what are we measuring? A systematic review. J.
Clin. Sleep Med. 17, 1717e1729. https://doi.org/10.5664/jcsm.9394. PMID:
33960296.
Mahoney, M.H., Swan, M.C., Fisher, D.M., 2013. Prospective analysis of presurgical
risk factors for outcomes in primary palatoplasty. Plast. Reconstr. Surg. 132,
165e171.
Meijer, M.F., 2003. Testing Speech of Children Born with a Cleft: A Report from the
Speech Therapy Workgroup from the Dutch Association for Cleft Palate and
Craniofacial Anomalies Amsterdam. Vrije Universiteit Medisch Centrum, The
Netherlands.
Mermans, J.F., Lissenberg-Witte, B.I., Van Gogh, C.D.L., Broers, C.J.M., Van
Hagen, J.M., Strijers, R.L.M., Griot Jpw, Don, 2018. Tongue lip adhesion in the
treatment of Robin sequence: respiratory, feeding, and surgical outcomes.
J. Craniofac. Surg. 29, 2327e2333.
Morice, A., Renault, F., Soupre, V., Chapuis, V., Zbinden, C.T., Kadlub, N., Giudice, A.,
Vazquez, M.P., Picard, A., 2018. Predictors of speech outcomes in children with
pierre Robin sequence. J. Cranio-Maxillo-Fac. Surg. 46, 479e484.
Patel, K.B., Sullivan, S.R., Murthy, A.S., Marrinan, E., Mulliken, J.B., 2012. Speech
outcome after palatal repair in nonsyndromic versus syndromic Robin
sequence. Plast. Reconstr. Surg. 130, 577e584.
Poets, C.F., Koos, B., Reinert, S., Wiechers, C., 2019. The tübingen palatal plate
approach to Robin sequence: summary of current evidence. J. Cranio-Maxillo-
Fac. Surg. 47, 1699e1705.
Resnick, C.M., LeVine, J., Calabrese, C.E., Padwa, B.L., Hansen, A., Katwa, U., 2018.
Early management of infants with Robin sequence: an international survey and
algorithm. J. Oral Maxillofac. Surg. 77 (136 156).
Robin, P., 1923. La chute de La base de La langue consid
er
ee comme une nouvelle
cause de G^
ene dans La respiration naso-pharyngienne. Bull Acad Med Paris 89
(37 41).
Schwaiger, M., Cook, H., Jordan, Z., Edmondson, S.J., Mischak, I., Wallner, J.,
Atherton, D., Haers, P., Timoney, N., Ferguson, L., 2021. Robin sequence: 5-year
speech OutcomeseA case-control study. Plast. Reconstr. Surg. 147, 676e686.
Scott, A.R., Mader, N.S., 2014. Regional variations in the presentation and surgical
management of pierre Robin sequence. Laryngoscope 124, 2818e2825.
Spruijt, N.E., Beenakker, M., Verbeek, M., Heinze, Z.C.M., Breugem, C.C., Mink van der
Molen, A.B., 2018. Reliability of the Dutch cleft speech evaluation test and
conversion to the proposed universal scale. J. Craniofac. Surg. 29, 390e395.
Stransky, C., Basta, M., Solot, C., Cohen, M., Low, D.W., Larossa, Don, Jackson, O.,
2013. Do patients with pierre Robin sequence have worse outcomes after cleft
palate surgery? Ann. Plast. Surg. 71, 292e296.
Tan, T.Y., Kilpatrick, N., Farlie, P.G., 2013. Developmental and genetic perspectives on
pierre Robin sequence. Am J Med Genet C Semin Med Genet 163, 295e305.
Viezel-Mathieu, A., Safran, T., Gilardino, M.S., 2016. A systematic review of the
effectiveness of tongue lip adhesion in improving airway obstruction in chil-
dren with pierre Robin sequence. J. Craniofac. Surg. 27 (6), 1453e1456.
Witt, P.D., Myckatyn, T., Marsh, J.L., Grames, L.M., Dowton, S.B., 1997. Need for
velopharyngeal management following palatoplasty: an outcome analysis of
syndromic and nonsyndromic patients with Robin sequence. Plast. Reconstr.
Surg. 99, 1522e1524.
Wu, R., Cheraghlou, S., Parsaei, Y., Travieso, R., Steinbacher, D.M., 2017. Does cleft
palate width correlate with Veau classification and outcome? J. Craniofac. Surg.
28, 1369e1374.
Xu, J.X., Kilpatrick, N., Baker, N.L., Penington, A., Farlie, P.G., Tan, T.Y., 2016. Clinical
and molecular characterisation of children with pierre Robin sequence and
additional anomalies. Mol Syndromol 7, 322e328.
Yuan, N., Dorafshar, A.H., Follmar, K.E., Pendleton, C., Ferguson, K., Redett, R.J., 2016.
Effects of cleft width and Veau type on incidence of palatal fistula and velo-
pharyngeal insufficiency after cleft palate repair. Ann. Plast. Surg. 76, 406e410.
R.J.H. Logjes, J.F. Mermans, M.J. Coerts et al. Journal of Cranio-Maxillo-Facial Surgery 51 (2023) 209e216
216
