Am J Otolaryngol xxx (xxxx) xxxx

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Am J Otolaryngol
journal homepage: www.elsevier.com/locate/amjoto

Risk factors associated with microbial colonisation and infection of

tracheostomy tubes
⁎
Dulitha Kumarasinghea, Eugene Wonga,b, , Marin Duvnjaka, Niranjan Sritharana,
Mark C. Smitha,b,c, Carsten Palmec, Faruque Riffata,b,c
a
Department of Otolaryngology, Head and Neck Surgery, Westmead Hospital, University of Sydney, Camperdown, NSW 2006, Australia
b
Department of Otolaryngology, Head and Neck Surgery, Macquarie University Hospital, Australia
c
Chris O'Brien Lifehouse, Sydney, Australia

A R T I C LE I N FO A B S T R A C T

Keywords: Background: A long-term tracheostomy tube has the potential to cause significant morbidity and mortality in
Tracheostomy both hospitalised patients and those in the community. This study aims to assess the rates of microbial colo-
Infection nisation and infection of tracheostomy tubes.
Colonisation Materials and methods: Consecutive patients were enrolled from both inpatient and outpatient settings during
Diabetes
their routine tracheostomy changes. During changes, culture swabs were taken from the cuff/outer-cannula and
Smoking
inner-cannula. Analysis were performed to compare culture results with risk factors.
Results: 65 patients were enrolled in the study. Inpatients (65.9% vs 38.1%, χ2 4.48, p = 0.03), increasing acuity
of care (from outpatient; ward; HDU; and ICU in increasing acuity) (τb = 0.289, p = 0.012), cuffed tracheostomy
tubes, (66.7% vs 39.1%; χ2 4.59, p = 0.032); diabetics (64.6% vs 35.3%; χ2 4.39, p = 0.036); and males were
associated with increased colonisation (72.4% vs 44.4%; χ2 5.12, p = 0.024).
Conclusion: Factors associated with an increase in colonisation and infection of tracheostomy tubes were loca-
tion, and in males, diabetics and in cuffed tubes.

1. Introduction awake patients to talk and commence oral intake.

A surgical tracheostomy is a procedure used to create an alternate
airway by making an incision into the anterior portion of the trachea.
Dating back to 3600 BCE; where ancient Egyptian engravings have been
found depicting the process, it remains to be one of the oldest surgical
procedures to date [1]. Currently it is one of the most commonly per-
formed procedures in critically unwell patients, with over 100,000
tracheostomies performed every year in the United States alone [2].
Tracheostomies are occasionally used to provide a protected airway
for people who develop potential upper airway obstruction, with
pathologies including large obstructing tumours and deep space infec-
tions. Other indications for tracheostomy include respiratory failure
with prolonged mechanical ventilation requirements, traumatic or
catastrophic neurological insult limiting self-protection of the airway or
management of copious secretions. Compared to conventional en-
dotracheal intubation, tracheostomies have been shown to reduce rates
of ventilator associated pneumonia, laryngeal injury and overall ven-
tilation and sedation requirements [3,4]. Overall, they are much better
tolerated by patients and provide more functional capacity by allowing
Tracheostomy tubes come in various sizes, materials and designs
including cuffs and fenestrations [5,6]. Cuffed tubes have an inflatable
balloon on their distal end that can be externally filled with air to
prevent dislodgement, aspirations and secretion plugging. Un-cuffed
tubes are hence reserved for specific cases where patients have an
adequate cough reflex and can manage their own secretions. It provides
benefits over cuffed tubes by reducing tracheal trauma and aiding in
speech and swallowing. Fenestrated tubes have one or more small holes
in their distal convexity and are often used in the weaning of ventilation
and the de-cannulation process. However, in theory these fenestrations
may cause an increase in granulation tissue formation as tissue healing
occurs over the fenestrations which are continually disrupted with tube
changes. Currently, very little evidence is present identifying links be-
tween tracheostomy tube design factors and their relationship to colo-
nisation and infection.
Tracheostomy tubes are changed routinely based on manufacturer
guidelines and expiry dates. Clinicians believe that these tube changes
should be performed for a variety of perceived benefits, with the
common justifications to prevent potential infections; and reduce

⁎
Corresponding author at: Department of Otolaryngology, Head and Neck Surgery, Westmead Hospital, University of Sydney, Camperdown, NSW 2006, Australia.
E-mail address: eugene.hl.wong@gmail.com (E. Wong).

https://doi.org/10.1016/j.amjoto.2020.102495
Received 18 November 2019
0196-0709/ © 2020 Elsevier Inc. All rights reserved.

Please cite this article as: Dulitha Kumarasinghe, et al., Am J Otolaryngol, https://doi.org/10.1016/j.amjoto.2020.102495
D. Kumarasinghe, et al.
granulation formation around stomas [7]. However, while tra-
cheostomy tube changes are commonplace, they can carry a significant
a real risk of potential airway compromise and should be done by an
experienced health care professional.
This study aims to identify and characterise colonisation and in-
fection rates of tracheostomy tubes in adult patients currently partici-
pating within a large multidisciplinary tracheostomy service based at a
tertiary Australian hospital. The current literature regarding the rate
and predictive factors of tracheostomy tube colonisation and infections
remain limited, and therefore the purpose of this study was to bridge
this gap in knowledge.
2. Materials and methods
2.1. Patient population
A prospective cohort study was performed on consecutive adult
patients (age > 16 years) with a tracheostomy enlisted into a multi-
disciplinary tracheostomy service based at a tertiary hospital in
Westmead, Sydney, Australia. All patients with tracheostomies (both
surgical and percutaneous) performed onsite at the hospital were ac-
tively enrolled into the service for ongoing follow up. Furthermore,
through referral and consultation, patients with pre-existing tracheos-
tomies from outside the hospital were able to be enlisted. Inpatients
were seen at the bedside by the dedicated tracheostomy team, while
outpatients were seen at a walk-in tracheostomy clinic or as part of the
community outreach program. This program allows for patients to be
seen at their home residence or aged care facility by the service.
However, due to the risk associated with tracheostomy tube changes,
these procedures were done within the hospital setting (either as an
inpatient or through the outpatient clinic) in the presence of a fellow-
ship trained otolaryngologist.
The data collection period took place over 18-months from
September 2017 to March 2019. Patients were excluded if they un-
derwent an emergency tracheostomy tube change (i.e from dislodge-
ment or obstruction), continued to require ongoing active machine
ventilation, had an active lower respiratory tract infection or was im-
munosuppressed (through the use of medications such as steroids,
biologic immunomodulators or chemotherapy agents).
3. Study population and data collection
A database of patients enrolled into the tracheostomy service are
kept ensuring ongoing follow-up and coordination of care. The current
practice of our service is for an initial routine tracheostomy tube change
to be performed approximately 2–4 weeks post tracheostomy formation
and subsequently every 4–6 weeks thereafter. For patients with long
term tracheostomies in an outpatient setting, these changes may be
extended up to 3-monthly depending on the specific patient require-
ments and only after approval following assessment by an otolar-
yngologist. During these routine changes, patients undergo a detailed
review including a thorough history, examination of the external stoma
site, as well as flexible nasendoscopy assessment above the glottis, the
subglottis and through the new tracheostomy tube where possible.
Both pre-existing and new patients were enrolled into the study
during these routine tracheostomy changes by members of the tra-
cheostomy team. All patients provided informed consent and were
given a participant information sheet prior to recruitment.
During routine tracheostomy changes, microbiology swabs were
taken from the Cuff/Outer Cannula and Tip/Inner Cannula and sent to a
pathology laboratory for Microscopy, Culture and Sensitivity (MCS). An
aseptic technique in line with our local health district protocols were
used for the changes. These microbiology swabs were considered to be a
suitable method of identifying bacteria colonising the surface of tra-
cheostomy tubes and hence potentially cause clinically relevant re-
spiratory and stoma site infections. Alongside tube changes, the stoma
2
Am J Otolaryngol xxx (xxxx) xxxx
site was also assessed for signs of infection.
Concurrently, electronic medical records were accessed to collect
demographic, medical and tracheostomy data. Demographic data col-
lected included age, gender, active smoking, alcohol use and location of
the patient (inpatient vs outpatient). Each patient's past medical history
was assessed for hypertension (defined as taking current, regular anti-
hypertensive medication), Chronic Obstructive Pulmonary Disease
(COPD) (defined as spirometry demonstrating FEV1/FVC < 0.7 after
bronchodilator challenge or diagnosis made by a respiratory physician)
and Obstructive Sleep Apnoea (OSA) (Apnoea-hypopnea Index > 5).
Details of the tracheostomy tube and its changes were also collected,
including the indication for tracheostomy; time since last change,
number of times the inner cannula changed daily; ventilator use; tube
model/type; the inner diameter of the inner tube, whether the tube was
cuffed; whether the tube was fenestrated; and whether the tube was
fixed or had an adjustable flange.
A true colonised sample was only considered if both swabs (cuff/
outer cannula and tip/inner cannula) demonstrated a positive culture of
similar microorganisms. Isolated positive swab cultures from only one
swab were considered contaminants from the collection process and
excluded from analyses. Specimens that cultured ‘normal skin flora’,
were also not considered to be significant.
4. Data analysis
All categorical variables were presented using percentages and raw
numbers. Continuous parametric data was presented using means with
standard deviations while non-parametric continuous data was pre-
sented as medians with ranges. Comparison of microbiology culture
results between tube change time frames as well as other tracheostomy
tube endpoints were performed using the chi-square test to examine
binary categorical data. Correlation between ordinal variables was
performed using a Kendall's tau-b.
A p value less than 0.05 (p < 0.05) was deemed to be statistically
significant. All data analysis was performed by Statistical Package for
the Social Sciences (SPSS) version 23.0 (IBM Corporation, Armonk, NY,
USA).
5. Results
A total of 65 patients met the inclusion criteria for participation in
this study. After informed consent was obtained, all 65 patients (mean
age 52.3 years ± SD 15.2, 55.4% female) were then formally recruited
in the study. A greater proportion of enrolled patients were inpatients
(n = 44, 67.7%) compared to outpatients. Of the inpatients, most were
either from the ward (n = 20, 30.8%) followed by the high dependency
unit (HDU) (n = 14, 21.5%) and intensive care unit (ICU) (n = 10,
15.4%). The demographics and distribution of the patients are de-
monstrated in Table 1.
The age of the tracheostomy stoma varied from 1 week old to over
6 years old, with a median age of 8 weeks. The indication for tra-
cheostomy varied considerably with the most common surgical in-
dication being extensive head and neck surgeries (n = 12, 18.5%)
followed by laryngeal oedema/obstruction (n = 10, 15.4%), vocal cord
palsy (n = 4, 6.2%) and tracheal stenosis (n = 4, 6.2%). While the most
common medical indication was for a stroke (n = 14, 21.5%) followed
by prolonged intubation (n = 10, 15.4%), traumatic brain injury
(n = 7, 10.8%) and status epilepticus (n = 4, 6.2%).
On average inner cannulas were changed 5.2hrly (SD 2.7). The
average inner diameter of the tracheostomy tube placed was found to
be 7.07 mm (SD 0.75). All tubes were Portex® branded.
A chi squared analysis showed a statistically significant increase in
culture positive patients was found in inpatients compared to out-
patients (65.9% vs 38.1%; χ2 4.48, p = 0.03) (OR 0.32; 95% I: 0.11 to
0.94). A Kendall's tau-b correlation was run to determine the relation-
ship between culture positive patients and location of patients ranked
D. Kumarasinghe, et al. Am J Otolaryngol xxx (xxxx) xxxx

Table 1 (M = 7.05, SD 0.69) (t (63) = 0.21, p = 0.82).

Patient demographics and risk factors and their association with culture posi- The most common microorganism cultured was Pseudomonas aeru-
tive tracheostomy tubes. ginosa which was present in 37%, followed by Methicillin-Sensitive
Culture Culture Statistical test Significance Staphylococcus aureus (MSSA) (15%). Of note 14% had a combination of
positive negative 2 colonisers.

Number of patients 37 28 – –
Mean age (SD) 50.2 (15.8) 55.0 (14.1) – –
Female gender 44.4% 72.4% Chi-square 0.02
6. Discussion
(%)
Smoking 32.4% 25.0% Chi-square 0.51 This study demonstrated that there are certain tracheostomy tube
Hypertension 35.1% 57.1% Chi-square 0.08 factors associated with increased rates of tracheostomy tube colonisa-
COPD 8.1% 10.7% Chi-square 0.94
tion and infection. Adult inpatients with tracheostomy tubes were as-
OSA 0.0% 7.1% Chi-square 0.73
GERD 24.3% 42.9% Chi-square 0.11 sociated with an increased risk of colonisation and infection compared
Asthma 5.4% 14.2% Chi-square 0.22 with those in the outpatient setting. When further expanded this
Diabetes 64.6% 35.3% Chi-square 0.04 showed a significant positive relationship to rates of colonisation and
CVA 16.2% 28.6% Chi-square 0.23
infection dependent on the acuity of setting, with patients in the ICU
Cuffed tube 66.7% 39.1% Chi-square 0.03
Fenestrated tube 53.8% 59.0% Chi-square 0.68
colonising significantly more than those on standard wards.
Inpatient 65.9 38.1% Chi-square 0.03 Furthermore, there was an increased risk shown in diabetics, in males
Diabetes 64.6% 35.3% Chi-square 0.04 and in cuffed tubes.
Surgical indication 50.0% 62.9% Chi-square 0.30 It is the author's opinion that each of these findings were largely
Tube size (SD) 7.09 (0.79) 7.05 (0.69) t-Test 0.82
expected: there is significant literature demonstrating that the risk of
The significance of bold is p < 0.05 increased nosocomial infections is associated with hospital stay, and
furthermore hospitalised patients are likely to be more unwell and
by level of care (from outpatient; ward; HDU; and ICU in increasing hence vulnerable to colonisation. This increased risk could also be di-
acuity). There was a strong, positive correlation between culture posi- rectly related to an increased rate of physical contact with the tubes in
tive patients and the higher acuity of setting, which was statistically an inpatient setting as well as the exposure to ward nursing staff who
significant (τb = 0.289, p = 0.012). This is demonstrated in Table 1 and may not necessarily be experienced with their maintenance. Hence
Fig. 1. when safe to do so, the authors suggest that patients should be stepped
A statistically significant increase in culture positive patients was down to a ward and then outpatient setting as soon as it is safe to do so.
found in cuffed tracheostomy tubes compared with patients with un- A tracheostomy tube should not be a deciding factor in preventing the
cuffed tracheostomy tubes (28/42, 66.7% vs 9/23, 39.1%; χ2 4.59, stepdown or discharge of patients, and this is where a multidisciplinary
p = 0.032) (OR 0.32; 95% CI: 0.11 to 0.92); and in inpatients compared tracheostomy service can be of great help.
to outpatients (65.9% vs 38.1%; χ2 4.48, p = 0.03) (OR 0.32; 95% I: The significant difference in positive culture rates among patients
0.11 to 0.94); in diabetics compared to non-diabetics (31/48, 64.6% vs with cuffed tubes may indicate that the cuff itself may hinder certain
6/17, 35.3%; χ2 4.39, p = 0.036) (OR 0.29; 95% CI: 0.09 to 0.95); and innate immune responses such as mucociliary clearance in the pre-
in males compared to females (72.4% vs 44.4%; χ2 5.12, p = 0.024) vention of infection. A study by Hernandez et al. found that having a
(OR 0.30; 95% CI 0.10 to 0.87). cuff deflated during trials of spontaneous breathing shortened weaning
There was no significant difference in rates of positive culture based times, reduced infection rate and improved swallowing [8]. While
on Medical vs Surgical indication of tracheostomy (22/35, 62.9% vs cuffed tracheostomy tubes certainly are required in some patients –
15/30, 50%; χ2 1.09, p = 0.30) (OR 0.59: 95% CI 0.22 to 1.59) or most commonly to facilitate a closed circuit during mechanical venti-
Fenestrated vs Non-Fenestrated tubes (14/26, 53.8% vs 23/39; 59%; χ2 lation or to provide airway protection against aspiration – it is therefore
0.16, p = 0.68) (OR 1.23: 95% CI 0.45 to 3.35). Using an independent t- critical that when these indications are no longer applicable, early
test there was also no significant difference in tube size between tubes transition to uncuffed tubes is recommended.
who had a positive culture (M = 7.09, SD 0.79) and negative culture The role of diabetes in promoting colonisation and infection has
been well studied in the past [9]. Clinicians should be wary in not only

Fig. 1. Graph 1: Culture rates by location in increasing acuity.

HDU: High Dependency Unit; ICU: Intensive Care Unit.

3
D. Kumarasinghe, et al.
patients with tracheostomies but those with any hardware as this may
increase the risk of infection and colonisation in diabetic patients.
There is literature indicating that these patients can have their relative
risk reduced by improving glycaemic control through the use of mul-
timodal therapies including diet, exercise and pharmacological inter-
ventions to reduce blood sugar levels and HbA1c [10]. This remains a
growing area of research and is a possibility for further expansion of
this study.
The association between infection and male sex is more speculative
[11]. Past studies have demonstrated similar increases in infections
associated with bacteraemia, surgical site colonisation and infections in
males over females. A variety of reasons have been postulated as to the
cause of this including the presence of facial hair. Beard growth and
shaving may interfere with wound dressing and adherence leading to
higher infection rates. Other possible explanations including poorer
hygiene habits and increased smoking rates. Therefore, all of these
factors should be taken into account when managing a male tra-
cheostomy patient.
This study does carry several limitations. The cohort size is small,
which may limit the power of our study. However, to our knowledge,
this is the largest study examining microbial colonisation in tra-
cheostomy tubes, with recruitment of larger cohort sizes challenging
without multicentre or global coordination. Secondly, we concede that
a positive swab culture does not necessarily indicate active infection.
However, this does suggest colonisation, which the authors believe is
the best surrogate marker for infection available. Finally, this study is
prospective observational study, and therefore did not involve rando-
misation or any controls, which may introduce unforeseen bias or
confounding factors. Future studies of a higher level of evidence may be
considered in order to strengthen the conviction of the positive findings
of this study.
7. Conclusion
Inpatients, and particularly those in higher acuity settings such as
the ICU, have a significantly increased risk of colonisation and infection
when compared to those managed in an outpatient setting. Other fac-
tors that are also that may also put patients at an increased risk include
cuffed tubes, being a male and being a diabetic. Therefore, it is the
authors opinion that when clinically safe to do so patients should be
stepped down and discharged into the community sooner rather than
later. Similarly, close attention should be focussed on diabetic patients
(particularly with poor glycaemic control) and that patients with cuffed
tubes considered for transition to uncuffed tubes when able to. A
dedicated multidisciplinary tracheostomy service with outpatient reach
has the ability to help facilitate this process through the early
Am J Otolaryngol xxx (xxxx) xxxx
coordination, management and education of staff, patients and their
carers.
Copyright transfer
In consideration of the American Journal of Otolaryngology's re-
viewing and editing my submission, “Risk factors associated with mi-
crobial colonisation and infection of tracheostomy tubes”, the author(s)
undersigned transfers, assigns and otherwise conveys all copyright
ownership to Elsevier Inc. in the event that such work is published in
the American Journal of Otolaryngology.
Declaration of competing interest
This manuscript has not been published and is not under con-
sideration elsewhere.
Acknowledgements
None.
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