Intensive & Critical Care Nursing 63 (2021) 102965

Contents lists available at ScienceDirect

Intensive & Critical Care Nursing

journal homepage: www.elsevier.com/iccn

Research Article

The risk of microaspiration during oral care in mechanically ventilated

patients: A randomised cross-over study comparing two different
suction protocols
Marion Griton a, Natacha Naud a, Didier Gruson a,d, Aurélie Bedel b,c, Alexandre Boyer a,d,⇑
a
Medical Intensive Care Unit, CHU Bordeaux, F33000 Bordeaux, France
b
Biochemistry Laboratory, CHU Bordeaux, F-33000 Bordeaux, France
c
Univ Bordeaux, INSERM U1035, F-33000 Bordeaux, France
d
Univ Bordeaux, INSERM U1045, F-33000 Bordeaux, France

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: To assess whether optimised oral care including subglottic suction could reduce microaspira-
Received 26 May 2020 tion in comparison with a routine oral care.
Revised 12 October 2020 Research methodology/design: An open prospective study comparing optimized versus a routine oral
Accepted 13 October 2020
care procedure in two randomised crossover consecutive periods of one day each. Optimised oral care
consisted of suction via the subglottic suction port before and after a 10 seconds chlorhexidine oral care,
compared with no use of the port during routine care.
Keywords:
Setting: Single-centre inclusion of critically ill patients ventilated for 48 hours with a subglottic suction
Amylase
Endotracheal tube
endotracheal tube, no curare, Ramsay score not <3, and semi-quantitative assessments of tracheal
Microaspiration secretions  ++.
Oral care Main outcome measures: Amylase being a relevant surrogate for oropharyngeal content, microaspirations
Subglottic suction were defined by tracheal/oral amylase ratio.
Ventilator-associated pneumonia Results: 21 patients (11 and 10 with routine and optimised care in the first day respectively) with no base-
line difference in risk of microaspiration. Neither difference in tracheal amylase amount or in tracheal/oral
amylase ratio (1.5% (0.7%–16%) and 2.3% (0.6%–6%), p = 0.37) was observed indicating that microaspirations
were not significantly decreased after optimized versus routine oral care.
Conclusion: Suctioning by the subglottic port of endotracheal tubes may not decrease the risk of microaspi-
ration during oral care of ventilated patients.
Ó 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Implications for clinical practice

 Oral care comes with an inherent risk of microaspiration even when endotracheal tube cuffs are adequately inflated
 Manual suction with a syringe connected to the subglottic port of the endotracheal tube during oral care does not decrease
microaspiration.

Introduction
Microaspiration of oropharyngeal secretions contaminated by
endogenous flora is a prerequisite of ventilator-associated
pneumonia (VAP). Oral care contributes to the clearance of con-
⇑ Corresponding author at: CHU Bordeaux, Medical Intensive Care Unit, F-33000
Bordeaux, France.
E-mail address: alexandre.boyer@chu-bordeaux.fr (A. Boyer).
taminated secretions from the mouth (Blot et al., 2014). Despite
the paucity of evidence showing its benefit in most patients
(Klompas et al., 2014), oral chlorhexidine treatment has been
included in most bundles and recommendations (web site). How-
ever, oral care is not clearly standardised. It usually includes oral
rinses with antiseptic solutions, tooth brushing, and repeated suc-
tion. Oropharyngeal and tracheal suction can induce the cough
reflex in non-paralysed patients, leading to mobilisation of the

https://doi.org/10.1016/j.iccn.2020.102965
0964-3397/Ó 2020 The Authors. Published by Elsevier Ltd.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
M. Griton, N. Naud, D. Gruson et al.
endotracheal tube. Consecutive bolus aspiration of contaminated
subglottic secretions should thus occur. Alpha-amylase is a
recently developed biomarker for microaspiration and has been
proposed by many research teams, including ours (Filloux et al.,
2013), to assess their amount (Dewavrin et al., 2014; Filloux
et al., 2013; Weiss et al., 2013). In a recent randomised study using
this biomarker, no evidence of microaspiration decrease has been
observed in a group of patients receiving a deep oropharyngeal
suction intervention compared with patients receiving usual care
(Sole et al. 2019). As subglottic suctioning endotracheal tubes can
be used as part of VAP prevention strategies (Branch-Elliman et al.,
2015), we hypothesised that the drainage of subglottic secretions
in specified phases of oral care, before the start of oral care and
before oro-tracheal suction, could reduce microaspiration.
Methods
Research question
The aim of this study was to assess whether an optimised oral
care including subglottic suction could reduce microaspiration.
Setting
This pilot open prospective study was conducted in a 13-beds
medical intensive care unit (ICU) of a teaching hospital. The study
was performed during an 18 months period and compared patients
receiving two different oral care procedures (optimized versus
routine) in two randomised crossover consecutive periods of
one day each.
Fig. 1. Description of the cross-over design of the study.
2
Intensive & Critical Care Nursing 63 (2021) 102965
Ethical aproval
Surrogates of the patient provided informed consent. The study
was approved by the ethics committee of our hospital. In the data
section VAP means ventilator-associated pneumonia The ethics
approval number is 2013-A00835-40. It has been delivered by the
Comité de Protection des Personnes Sud-Ouest et Outre Mer III. I
join it.
Participants
All adult ICU patients ventilated for at least 48 hours with a sub-
glottic suction endotracheal tube (ISIS, Teleflex) were eligible.
Patients with sufficient amount of tracheal secretions to allow
the amylase dosage (semi-quantitative assessments of tracheal
secretions  ++ on a scale consisting of 0, +, ++, and +++) and no
exclusion criterion were included. Exclusion criteria were cystic
fibrosis, bronchiectasis, pregnancy and protective measure status.
In addition, patients receiving, neuromuscular blocking agents,
who were awake (Ramsay score 1–2) and/or under pressure sup-
port ventilation with the decision to withhold/withdraw life-
sustaining treatment, those with contraindications to tracheal
aspiration (hemorrhagic risk, bronchospasm, PaO2/FIO2 ratio < 100,
or tracheal malformation or fistula), and those with closed endo-
tracheal aspiration systems were excluded.
Data collection
For each included patient, the study lasted two days. Trained,
critical care nurses had a role of research assistants for the study.
M. Griton, N. Naud, D. Gruson et al.
Two different oral care procedures were compared in two ran-
domised crossover consecutive periods of one day each (Fig. 1).
According to randomisation, routine or optimised oral care was
selected for the first one day period, and was followed by another
one day period with the alternate oral care protocol. Routine oral
care consisting of, in sequence, oral suction, 10 seconds chlorhex-
idine rinse, tooth brushing and tracheal suction, was performed
(Fig. 2). During the other period, patients received optimized oral
care. The optimisation was based on the hypothesis that subglottic
suction would subsequently reduce microaspiration prompted by
oral suction or oral care. It therefore consisted of, in sequence, sub-
glottic suction (suction 1) before oral suction, 10 seconds chlorhex-
idine rinse, tooth brushing, a second subglottic suction (suction 2),
and finally tracheal suction (Fig. 2). Every suction was standard-
ized: oral suction was performed through a Yankauer cannula
and lasted 20 seconds, tracheal suction consisted of suction with
a 10 french guage flexible cannula lasting 10 seconds and subglot-
tic suction consisted of manual suction using a 10-cc syringe con-
nected to the subglottic port. Oral care was performed three times
each day at 10 am, 2 pm, and 6 pm. Other VAP prevention strate-
gies or routine practices included enteral nutrition, semi-
recumbent positioning. To specifically avoid microaspirations due
to the endotracheal tube suction, a minimal level of positive end-
expiratory pressure of 5cm and cuff pressure adjustment
(25 mmHg) was regularly checked (Chair et al. 2019).
Outcome measures
Amylase enzymatic activity was measured, as described previ-
ously, for the oral, tracheal, subglottic 1 and 2 suctions. Amylase is
considered to be a relevant surrogate for oropharyngeal content
(Dewavrin et al., 2014; Filloux et al., 2013; Nseir et al., 2011;
Weiss et al., 2013). If present in tracheal suctions, it quantitatively
defines microaspiration (Dewavrin et al., 2014; Filloux et al., 2013;
Nseir et al., 2011). Chlorhexidine has been shown to have a neutral
effect on the amylase quantity (Filloux et al., 2013). As the amount
of amylase in tracheal suctions is potentially influenced by the
amount of amylase in oral suctions, we used the amylase tracheal/
oral ratio as the primary assessment. The 10 am amylase tracheal/
oral ratio was considered to be the baseline measure of cuff leakage
risk (due to individual factors such as awakeness, cough reflex). The
median value of the 2 pm and 6 pm amylase tracheal/oral ratios was
defined as the primary outcome and compared between the routine
and optimized groups. It was adjusted to the baseline 10 am tra-
cheal/oral ratio to better assess the specific effect of the oral care
protocol. Exposure variables potentially affecting the quality of
secretions, such as natremia, cholinergic, anticholinergic, or neu-
roleptic treatment; and the amount of tracheal suction since inclu-
sion and between study measurements were also assessed.
Data analysis
Continuous variables were compared using the paired t-test or
Wilcoxon signed-rank test when appropriate for the matched
paired series. Categorical variables were compared using Fisher’s
exact test. P values < 0.05 were considered to indicate statistical
significance. All data were analysed and processed using SAS 9.2
software (SAS Institute, Cary, NC).
Results
Twenty-four patients were enrolled and 21 were included in the
final analysis (three patients progressed to Ramsay score 1–2 dur-
ing the 2 study days) (Fig. 3). Most patients (SAPSII 51 ± 16) were
ventilated due to respiratory failure (48%) for a median duration of
3
Intensive & Critical Care Nursing 63 (2021) 102965
2 (2–5) days. Ten and 11 patients received optimised-routine and
routine-optimized oral care, respectively. The percentage of
patients with natremia > 145 mmol/L, the amount of secretions
suctioned at 2 pm and 6 pm, the number of tracheal suctions per-
formed between 10 am and 6 pm and baseline (10 am) tracheal/
oral amylase ratios did not differ significantly between day 1 and
day 2. The entire routine and optimised oral care procedures lasted
7.3 ± 1.3 and 9.4 ± 1.4 min, respectively (p < 0.001).
The respective amounts of amylase in oral suctions were similar
in the routine and optimized groups [200.400 (62.700–586.354)
and 182.200 (54.000–423.100) IU/L; p = 0.86]. The subglottic suc-
tion amylase level in the optimized group was 75.420 (27.735–
218.120) IU/L. No difference in the amount of amylase in tracheal
suctions was observed between the routine and optimised groups
[2.429 (1.226–5.842) and 3.246 (1.385–12.881) IU/L, respectively].
The median tracheal/oral amylase ratio was not significantly
decreased after optimised or routine oral care [1.5% (0.7%–16%)
and 2.3% (0.6%–6%), respectively; p = 0.37; Fig. 4]. These results
did not differ when adjusted to baseline (10 am) tracheal/oral amy-
lase ratios.
Discussion
In this pilot study, despite protection of the trachea by the
endotracheal tube cuff, amylase was found in tracheal suction
samples from the last step of a standardized oral care procedure.
Indeed, oropharyngeal content may continuously reach the trachea
past the cuff. This mechanism may be independent of oral care per
se. However, oral care is a risk factor for microaspiration because it
can induce movement of the endotracheal tube within the trachea,
spontaneous patient movement and changes in trans-cuff pressure
as a result of suctioning (Chair et al., 2020). However, no decrease
in microaspiration was demonstrated when subglottic suction was
interleaved between oral and tracheal suctions. This study may
then suggest that optimized oral care is ineffective in comparison
to routine care which may be due to the inability of subglottic suc-
tion to prevent the microaspiration of oro-pharyngeal content dur-
ing oral care. The use of a cross-over design allows patients specific
factors to be controlled. Tracheal and oral amylase levels and the
tracheal/oral ratio were similar to those previously reported by
our previous study [4] [tracheal 6.661 (2.774–19.358) IU/L, sub-
glottic 130.750 (55.257–157.717) IU/L, oral 307.606 (200.725–
461.300) IU/L, tracheal/oral ratio 5.5% (1.1%–36%)] and to those
of Nandapalan et al. (1995) (tracheal/oral ratio 10%), which
strengthens the external validity of this marker.
Limitations
Two limitations, leading to a biased underestimation of the op-
timized care protective effect, deserve to be discussed. First, amy-
lase may have remained in trachea between the 2 pm and 6 pm
measurements since the rate of amylase tracheal clearance is not
known. However, the variations in individual patients’ amylase
levels within the same day (i.e., 2 pm vs. 6 pm) support active amy-
lase clearance. No automatic cuff pressure adjustment was used in
the study and we cannot eliminate that microaspirations occurred
during the manometer connection (which was systematically per-
formed before oral care) (Nseir et al., 2011). This study has other
limitations. It was a single-centre pilot study with no sample size
calculation; therefore, increased power may have yielded more sig-
nificant results. However, in this study, the estimated decrease in
microaspiration in patients receiving optimised vs. routine oral
care seems to have been very limited and not clinically relevant.
Also, patients included in this study were not deeply sedated, with
Ramsay scores of 3 and 4. No Ramsay score difference was
M. Griton, N. Naud, D. Gruson et al. Intensive & Critical Care Nursing 63 (2021) 102965

Fig. 2. Description of the routine vs. optimized oral care protocols.

4
M. Griton, N. Naud, D. Gruson et al. Intensive & Critical Care Nursing 63 (2021) 102965

Fig. 3. Flow chart of the study.

Fig. 4. Comparison of amylase tracheal/oral median ratio afetr optimized versus routine oral care.

observed between groups. However, this status could have
favoured microaspiration and led to the absence of difference
between groups. Finally, in this study, no continuous subglottic
suction was used between oral care procedures since it has been
associated with tracheal injuries (Berra et al., 2004). Had the sub-
glottic zone been continuously suctioned, the effect of optimised
oral care might have been modified. The amount of subglottic
secretions would have probably been decreased, then limiting
the risk of microaspiration associated with the oral care procedure.
According to these limitations, should another study been fur-
ther designed, several issues should be pointed. A multi-centre
study with an increased sample size should be designed. Patients
needing more sedation for deeper and longer hypoxaemia would
5
be more prone to detect oral care specific effect and limit
microaspirations due to agitation. Accordingly, automatic cuff
pressure management should be used. Finally, if clinical endpoints
such as the incidence of ventilated associated tracheobronchitis or
pneumonia were to be chosen, routine or optimised oral cares
should be randomised in separate patients.
Conclusion
Suctioning the subglottic port of endotracheal tubes may not
decrease the risk of microaspiration during oral care of ICU venti-
lated patients. The single-centre design of the study however
precludes the generalisation of this conclusion. This study was
M. Griton, N. Naud, D. Gruson et al.
not designed to assess whether the use of subglottic suctioning of
endotracheal tubes is an efficient VAP prevention measure.
Ethical aproval
Surrogates of the patient provided informed consent. The study
was approved by the ethics committee of our hospital.
Declaration of Competing Interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared
to influence the work reported in this paper.
Acknowledgements
We thank the subjects and the clinical and clerical teams
involved in this study.
Role of the funding source
This study has been funded by TELEFLEX MEDICAL SAS, La
Pousaraque, 31 460 Le Faget – France. Teleflex had no role on the
design, the data analysis, the writing of the manuscript
Clinical registration number
ClinicalTrials.gov (n°NCT01807884).
Intensive & Critical Care Nursing 63 (2021) 102965
References
Berra, L., De Marchi, L., Panigada, M., Yu, Z.-X., Baccarelli, A., Kolobow, T., 2004.
Evaluation of continuous aspiration of subglottic secretion in an in vivo study.
Crit. Care Med. 32 (10), 2071–2078.
Blot, S., Poelaert, J., Kollef, M., 2014. How to avoid micro-aspiration? A key element
for the prevention of ventilator-associated pneumonia. BMC Infect. Dis. 14, 119.
Branch-Elliman, W., Wright, S.B., Howell, M.D., 2015. Determining the Ideal Strategy
for Ventilator-associated Pneumonia Prevention. Cost–Benefit Analysis. Am. J.
Respir. Crit. Care Med. 192 (1), 57–63.
Chair, S.Y., Chan, D.W.K., Cao, X.i., 2020. The interaction of subglottic drainage, cuff
pressure, and oral care on endotracheal tube fluid leakage: A benchtop study.
Australian Critical Care 33 (4), 358–363.
Dewavrin, F., Zerimech, F., Boyer, A., et al. 2014. Accuracy of alpha amylase in
diagnosing microaspiration in intubated critically-ill patients. PLoS One 9:
e90851.
Filloux, B., Bedel, A., Nseir, S., et al., 2013. Tracheal amylase dosage as a marker for
microaspiration: a pilot study. Minerva Anestesiol. 79, 1003–1010.
Klompas, M., Speck, K., Howell, M.D., Greene, L.R., Berenholtz, S.M., 2014.
Reappraisal of Routine Oral Care With Chlorhexidine Gluconate for Patients
Receiving Mechanical Ventilation: Systematic Review and Meta-Analysis. JAMA
Intern Med 174 (5), 751.
Nandapalan, V., McIlwain, J.C., Hamilton, J., 1995. A study of alpha-amylase activity
in tracheobronchial secretions of seriously ill patients with tracheostomies. J.
Laryngol. Otol. 109 (7), 640–643.
Nseir, S., Zerimech, F., Fournier, C., et al., 2011. Continuous control of tracheal cuff
pressure and microaspiration of gastric contents. Am. J. Respir. Crit. Care Med.
184, 1041–1047.
Sole, M.L., Talbert, S., Yan, X., Penoyer, D., Mehta, D., Bennett, M., Emery, K.P.,
Middleton, A., Deaton, L., Abomoelak, B., Deb, C., 2019. Impact of deep
oropharyngeal suctioning on microaspiration, ventilator events, and clinical
outcomes: A randomized clinical trial. J. Adv. Nurs. 75 (11), 3045–3057.
Weiss, C.H., Moazed, F., DiBardino, D., Swaroop, M., Wunderink, R.G., 2013.
Bronchoalveolar lavage amylase is associated with risk factors for aspiration
and predicts bacterial pneumonia. Crit. Care Med. 41 (3), 765–773.