P ulmonary Critical Care

M ECHANICAL VENTILATION
ANDCYTOPATHOLOGICAL
CHANGES IN THE ORAL
MUCOSA
By Ana Carolina Machado Landgraf, MSc, Angélica Reinheimer, MSc, Júlio
Cezar Merlin, PhD, Soraya de Azambuja Berti Couto, PhD, and Paulo Henrique
Couto Souza, PhD

Background The oral mucosa is an important defense

barrier to penetration of microorganisms. Thus, changes
in the oral epithelium might indicate risk for infection in
intensive care patients receiving mechanical ventilation.
Objective To evaluate the oral mucosa of intensive care
patients who did or did not receive mechanical ventilation
by using liquid-base exfoliative cytology.
Methods The sample consisted of 3 groups: 27 patients
admitted to intensive care during a 7- to 14-day period
who received mechanical ventilation, 29 patients
admitted during the same period who did not receive
mechanical ventilation, and 27 healthy patients who
had no lesions in the mouth. For all 3 groups, samples
were collected from the buccal mucosa by using cytol-
ogy brushes. Smears were applied to glass slides before
Papanicolaou staining and were codified for blind anal-
yses by a cytopathologist. Kruskal-Wallis and Dunn tests
were used to analyze the results.
Results Patients receiving mechanical ventilation had
higher prevalence and intensity of karyomegaly, perinu-
clear halos, cell keratinization, deep cells, and leukocyte

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infiltrates than did patients in the other 2 groups (P < .05).
No significant differences were observed between the
control group and the group who did not receive mechan-
ical ventilation.
Conclusions Liquid-base exfoliative cytology can be used
to detect preclinical alterations in the oral mucosa. Patients
treated with mechanical ventilation are vulnerable to infec-
tions, and oral care may be valuable in their prognosis.
(American Journal of Critical Care. 2017;26:297-302)

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 O
ral care of patients admitted to the intensive care unit (ICU) is an emerging topic
of great interest because the oral environment includes several microbiological
pathogens, which potentially influence secondary infections.1-5 In this context,
endotracheal intubation for mechanical ventilation plays an important part
because of the risk for ventilator-associated pneumonia.3,4

Despite some differences, research indicates a
correlation between the decreased incidence of
respiratory infections and routine oral care in ICU
patients.4,6-10 Specifically, dental studies indicate
relevant alterations in the oral cavity of ICU patients,
such as lesions in the oral mucosa, periodontal dis-
ease,11 lip and mucosal dryness, fungal infections,12
and increased biofilm on dental surfaces.13,14 These
alterations may be associated with several variables
in routine ICU care, such as the use of specific drugs
that reduce salivary flow and consequently worsen
oral health.2,9,12 Additionally,
Oral mucosa were patients receiving mechanical
ventilation are necessarily
compared between positioned with their mouth
patients who were open12 and are incapable of
mastication, contributing to
and patients who the reduction of salivary flow
and mucosal dryness. Other
were not receiving variables that increase the risk
mechanical ventilation. for secondary infections include
difficult access to the oral cav-
ity and the level of sedation in most of these patients,
which makes them unresponsive and uncoopera-
tive15,16 and more vulnerable over time.17,18
Currently, research is needed to develop
approaches for diagnosing oral conditions in ICU
patients and for determining the patients’ needs for
oral care.2,3,11,12,14 Specifically, most recent studies
have been based on subjective clinical criteria and
thus have been highly dependent on the observer.2,8,11
In order to be clinically relevant, studies on ICU
patients must be designed to guide professionals’
About the Authors
Ana Carolina Machado Landgraf and Angélica Reinheimer
are stomatologists, Soraya de Azambuja Berti Couto is an
assistant professor, and Paulo Henrique Couto Souza is a
full professor, Department of Stomatology, School of Life
Sciences, Pontifícia Universidade Católica do Paraná,
Curitiba, PR, Brasil. Júlio Cezar Merlin is an assistant
professor, Department of Pharmacy, School of Life
Sciences, Pontifícia Universidade Católica do Paraná.
Corresponding author: Ana Carolina Machado Landgraf,
MSc, Rua Imaculada Conceição 1155–Prado Velho, 80215-901,
Curitiba, Paraná, Brazil (e-mail: ana.landgraf1@gmail.com).
responses to the patients’ needs for oral care.9,14 Hence,
oral risk factors of ICU patients must be identified
before the development of treatment strategies.9,18
On the basis of the following, we designed
our research to investigate the oral mucosa of ICU
patients who were or were not receiving mechanical
ventilation: First, liquid-base exfoliative cytology
(LBEC) is a noninvasive, painless, low-cost, and
quick procedure19,20; second, cell alterations may
be detected early by using cytopathological analy-
sis21; and third, the oral mucosa plays an important
part in the immune response.22
Methods
Our study was carried out in accordance with
the ethical standards set forth in the Helsinki Decla-
ration of 1975 and was performed after approval by
the committee of ethics in research at Pontifícia Uni-
versidade Católica do Paraná, Curitiba, PR, Brasil.
Study Sample
From March to November 2014, a total of 83
patients, paired by age and sex, were selected and
divided into 3 groups. The first group consisted of
27 patients admitted to the ICU who were receiving
mechanical ventilation. The second group consisted
of 29 patients admitted to the ICU who were not
receiving mechanical ventilation. The third group,
the control group, consisted of 27 healthy outpa-
tients who did not have clinically visible oral lesions,
did not smoke, did not drink alcohol, and had not
been treated with mechanical ventilation in the pre-
ceding 3 months.
Patients were included in the sample if they
were more than 18 years old and were admitted to
the ICU for 7 to 14 days. Patients were not eligible
for the study if they were positive for HIV or were
undergoing chemotherapy or radiotherapy of the
head or neck.
Cell Samples
After study participants had lip hydration and
careful oral hygiene with gauze and distilled water,
samples of oral mucosal cells were obtained by a
trained examiner by pressing a cytology brush 10

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times in clockwise movements, on both the right
and left sides of the oral cavity for each patient.23
For the 2 groups who did or did not receive
mechanical ventilation, cell samples were obtained
only once per patient. The mean time of collection
was about the 12th day of ICU hospitalization. The
ICU patients were matched on the basis of an ICU
length of stay of 7 days minimum and 14 days
maximum, and all patients from the group receiving
mechanical ventilation had a tracheotomy. The cell
sample of the control group was obtained from
outpatients treated at the dental clinics of Pontifí-
cia Universidade Católica do Paraná according to
the same protocol used for the ICU patients. After
the surface of the oral mucosa was brushed, the part
of the cytology brush with the collected cells was
removed and submerged in a specimen collection
vial (10 mL), which is part of the Liqui-PREP Cytol-
ogy Processing (LGM International Inc) LBEC kit.
Laboratory Preparation
The biological material was processed on glass
slides in the cytology laboratory of the School of
Pharmacy, Pontifícia Universidade Católica do
Paraná, according to the standards described by the
manufacturer of the LBEC kit. The cell were fixed by
using 95% alcohol for 10 minutes, hydrated with
tap water for 3 minutes, and treated with Papanico-
laou stain (Newprov Products for Laboratory Ldt).
Cover slips were sealed by applying 2 drops of
Entellan (Merck) varnish.
Cytological Analysis
The glass slides were coded, masking the identi-
fication data. A specialist in cytopathology analyzed
the cell smears by using a planochromatic binocular
microscope (Nikon). The specialist examined the
slide by using a zigzag up and down motion.
Statistical Analysis
The total score for each group was calculated
on the basis of the keratinization, perinuclear halos,
leukocyte infiltration, karyomegaly and deep cells
indexes. The scores of the 3 groups were compared
by using 1-way analysis of variance. Power analysis
(observed power) indicated a power rating greater
than 99%, considering the significance level of .05,
when the null hypothesis is rejected.
The significance of differences between sample
pairs was tested by using the Kolmogorov-Smirnov
test and analysis of variance for the variable age and
r2 analysis and the likelihood ratio for the variable
sex. Cytopathological findings were analyzed by
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using tables and graphs of cross-frequency, compar-
ing the 3 groups. The Kruskal-Wallis test was used for
analysis of nonparametric data. When the Kruskal-
Wallis test indicated differences between groups, the
Dunn test for multiple comparisons was performed.
For all analyses, results were considered significant
if P was less than .05.
Results
Among the entire sample, mean ages were 64.7
years (SD, 12.2) for the group receiving mechanical
ventilation, 64.1 years (SD, 10.9) for the group not
receiving mechanical ventilation, and 66.4 years
(SD, 12.1) for the control group. Statistical tests for
sample pairing indicated that the patients were prop-
erly matched by age (P = .77) and sex (P = .84).
A total of 83 glass slides were analyzed.
Intermediate-type epithelial cells were predominant
among the 3 groups. Cytopathological alterations
were registered and classified as follows, in ascend-
ing order of severity:
0 Absent
1 Rare: the alteration was detected in less
than 25% of the cells on a slide
2 Discrete: the alteration was detected in 25%
to 50% of the cells on a glass slide.
3 Moderate: the alteration was detected in
50% to 75% of the cells on a glass slide
4 Severe: the alteration was detected in 75%
to 100% of the cells on a glass slide
The Table gives significant differences (P < .05) among
the groups.
In general, karyomegaly was the most prevalent
alteration in the group who received mechanical
ventilation (P < .001). The group who did not have
mechanical ventilation and the control group did
not differ significantly (P ≥ .05).
Perinuclear halos were detected To be clinically rele-
in 67% of the specimens from
the group who had mechanical vant, studies must be
ventilation, revealing a major
prevalence with evident statisti-
designed to guide
cal significance (P < .001). The caregivers’ responses
same alteration was also detected
in the group who did not have
to ICU patients’ needs
mechanical ventilation (17%) for oral care.
and the control group (4%).
However, the differences between these 2 groups
were not significant (P ≥ .05). Keratinization was
observed in 48% of the specimens from the group
who had mechanical ventilation. This percentage
differed significantly (P < .001) from the values for
the group who did not have mechanical ventilation
299
 Table
Comparison of results from the 3 groups of patients
No. (%) of patientsa
Alteration Classification Mechanical ventilation (n = 27) No mechanical ventilation (n = 29) Healthy outpatients (n = 27)
b
Karyomegaly Absent 8 (30) 20c (69) 24c (89)
Rare 12b (44) 8b,c (28) 3c (11)
Discrete 7b (26) 1c (38) 0c (0)
Meand 0.96 0.34 0.11
Perinuclear halo Absent 9b (33) 24c (83) 26c (96)
Rare 8b (30) 3b,c (10) 1c (4)
Discrete 6b (22) 2b,c (7) 0c (0)
Moderate 4b (15) 0c (0) 0c (0)
Meand
1.19 0.24 0.04
Keratinization Absent 14b (52) 23c (79) 26c (96)
Rare 11b (41) 6b,c (21) 1c (4)
Discrete 2b (7) 0b (0) 0b (0)
Meand
0.56 0.21 0.04
Leukocyte infiltrate Absent 1b (4) 10c (34) 11c (41)
Rare 18b (67) 15b (52) 13b (48)
Discrete 5b (19) 2b (7) 2b (7)
Moderate 0b (0) 0b (0) 1b (4)
Severe 3b (11) 2b (7) 0b (0)
Meand 1.48 0.93 0.74
Deep cells Absent 17b (63) 28c (97) 26c (96)
Rare 7b (26) 1c (3) 1c (4)
Discrete 2b (7) 0b (0) 0b (0)
Severe 1b (4) 0b (0) 0b (0)
Meand 0.56 0.03 0.04

a
Because of rounding, not all percentages total 100.
b,c
Dunn test: equal letters indicate no statistically significant difference between the groups (P * .05).
d
Kruskal-Wallis test.

(21%) and the control group (4%). The differences ventilation. This alteration is common in inflammatory
between the latter 2 groups were not significant processes, mostly involving young cells with intense
(P ≥ .05). Leukocyte infiltration was detected in 97% proliferative activity.24 This condition may be asso-
of the specimens from the group who received ciated with mucosal dryness and potential alter-
mechanical ventilation (P = .003). Again, differences ations in salivary flow, which consequently alter
between the group who did the immune response in patients treated with
LBEC can reveal not have mechanical ventila- mechanical ventilation.
tion (66%) and the control The situation becomes worse when karyomegaly
preclinical alterations group (59%) were not signifi- is combined with the high level of cell keratinization
that are predictive cant (P ≥ .05). Specifically, the
leukocytes were mainly poly-
in these patients. The epithelium of the buccal mucosa
is not keratinized, so most likely keratinization is
of risks for complica- morphonuclear neutrophils in an important alteration. This alteration may occur
all 3 groups. Deep cells occurred as an adaptive response of the cell to environmental
tions such as second- in 37% of the specimens from pathogens,22 indicating an acceleration of cell matu-
ary infections. the group who had mechanical ration. Additionally, a higher association between
ventilation (P < .001), in 3% of keratinization and enlarged cell nuclei has been
specimens from the group who did not have reported,25 an association that we confirmed as a
mechanical ventilation, and in 4% of specimens secondary finding in our study. Moreover, keratini-
from the control group. The differences between the zation may be associated with the ageing process.26
last 2 groups were not significant (P ≥ .05). However, independent of pairing the sample by age,
distribution of keratinization was asymmetric in
Discussion our sample, with a higher prevalence in specimens
We detected a high prevalence of karyomegaly in from the group who had mechanical ventilation.
specimens from the group who received mechanical This result may be due to the typical conditions of

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mechanical ventilation, which increase patients’
exposure to local and systemic pathogens and sus-
ceptibility to associated disorders.
Although we found no data on the cytopatho-
logical condition of the oral mucosa in patients who
have endotracheal ventilation, the close association
we observed between karyomegaly, perinuclear halos,
and cell keratinization is relevant, as these changes
are all typical of inflammatory processes.22,26 The
presence of leukocyte infiltration with predominant
polymorphonuclear neutrophils in the group who
had mechanical ventilation highlights the constant
presence of local pathogens. In addition, lesions on
the oral mucosa explain the detection of deep cells
in patients treated with mechanical ventilation, who
are constantly injured by the endotracheal tube. Only
2 patients who received mechanical ventilation had
oral ulcers detected during clinical examinations.
Additionally, deep cells are rarely detected in healthy
tissues, corroborating the notion that LBEC is an
accurate and useful method for the evaluation and
early detection of alterations that precede clinical
manifestations in the oral mucosa.27
Cell changes are an adaptive response to irrita-
tion of the oral mucosa. The cell nucleus may have
a marked increase in volume, with uniform distribu-
tion of nuclear chromatin granules (karyomegaly).
In another situation, a clear outline around the
nucleus, visualized as a halo a lighter color than
the cytoplasm (perinuclear halo), may be present.
A slight nuclear blurring in a reddish or orange
cytoplasm and a wrinkled appearance of the cell
may occur (keratinization). In all of these condi-
tions, the cell nuclei keep the normal shape of the
cell from which they arose, showing no derangements
compatible with cell atypia or malignant neoplasia.
Then, the cell sample will show infiltration of poly-
morphonuclear neutrophils (leukocyte infiltration)
in the first 48 hours of an inflammatory process.22
We used a simple, low-cost and noninvasive method,
LBEC, to detect these changes objectively, avoiding
subjective clinical criteria.
Our study has some limitations. Performing a
longitudinal study would have been difficult because
of the patients’ critical condition, which might lead
to loss of patients in the sample due to medical com-
plications or high mortality rates within the ICU.
Also, critical illness and the polypharmacy common
among ICU patients affect oral mucosal health and
could influence the results. However, we were unable
to correlate those factors with our results of exfolia-
tive cytology. The main determinant of oral health
we investigated was mechanical ventilation in
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tracheostomy patients after 7 days of hospitalization
without oral care. Last, we did not compare different
approaches to evaluate the efficacy of oral hygiene
between ICU patients who did and did not receive
mechanical ventilation. A potential clinical applica-
tion of our results for nurses and dentists who work
in ICUs is the necessity of using moisturizers and
humectant substances on the lips and oral mucosa
of ICU patients, mainly patients treated with mechan-
ical ventilation, during the entire hospitalization
period to ensure cell adhesion and consequent
maintenance of the cellular integrity of the oral
mucosa, which is constantly exposed to physical
and microbiological injuries.
Conclusions
Our results confirm the deterioration of oral
health in patients treated with mechanical ventila-
tion as indicated by a major prevalence and severity
of cell alterations in the oral mucosa. Our findings
highlight the important role of nurses and dentists
in supporting medical care in the ICU. In addition,
care providers must be aware that LBEC can be used
to detect preclinical alterations predictive of risks for
complications such as secondary infections and even
systemic disorders.
ACKNOWLEDGMENT
This research was performed at Pontifícia Universidade
Católica do Paraná, Brasil.
FINANCIAL DISCLOSURES
None reported.
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SEE ALSO
For more about mechanical ventilation and oral care,
visit the Critical Care Nurse website, www.ccnonline.
org, and read the article by Parisi et al, “Use of Ventila-
tor Bundle and Staff Education to Decrease Ventilator-
Associated Pneumonia in Intensive Care Patients”
(October 2016).
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Mechanical Ventilation and Cytopathological Changes in the Oral Mucosa
Ana Carolina Machado Landgraf, Angélica Reinheimer, Júlio Cezar Merlin, Soraya de Azambuja Berti
Couto and Paulo Henrique Couto Souza
Am J Crit Care 2017;26 297-302 10.4037/ajcc2017218
©2017 American Association of Critical-Care Nurses
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