healthcare

Article
A Systematic Review of Healthcare-Associated
Infectious Organisms in Medical Radiation
Science Departments
D’arcy Picton-Barnes 1 , Manikam Pillay 1,2 and David Lyall 1, *
1 School of Health Sciences, The University of Newcastle, Callaghan 2308, Australia;
d.picton-barnes@uon.edu.au (D.P.-B.); manikam.pillay@newcastle.edu.au (M.P.)
2 Centre for Resources Health and Safety, School of Health Sciences, The University of Newcastle,
Callaghan 2308, Australia
* Correspondence: david.lyall@newcastle.edu.au; Tel.: +61-2492-15083




Received: 7 February 2020; Accepted: 24 March 2020; Published: 30 March 2020


Abstract: Healthcare-associated infections (HAIs) pose a significant occupational risk to medical

radiation science (MRS) professionals, who have a high degree of patient contact. Current research
largely focusses on HAIs in patients, with limited attention given to infectious organisms that MRS
professionals are exposed to. This is a significant gap that this systematic review seeks to address
by summarizing current literature to determine the infectious organisms within MRS departments,
their reservoirs, and transmission modes. Reporting of this systematic review follows the preferred
reporting items for systematic reviews and meta-analyses guidelines. Five databases were searched
(Scopus, Medical Literature Analysis and Retrieval System Online (MEDLINE), the Cochrane Library,
EMBASE, and Cumulative Index to Nursing and Allied Health Literature (CINAHL)) for relevant
studies published between 1983 and 2018. Quality assessment was performed using checklists
from the Johanna Briggs Institute. Nineteen studies were included in the review; twelve of which
were set in diagnostic radiography departments, two in radiotherapy departments, and five in
non-MRS departments. No studies were set in nuclear medicine departments, indicating a gap in
the available literature. A total of 19 genera of infectious organisms were identified in the literature,
with Staphylococcus, Escherichia, Bacillus, and Corynebacterium reported in all MRS departments.
Infectious organisms were identified in all observational studies, indicating a need for better infection
control methods and/or compliance training within MRS to minimize the risk of infections.

Keywords: Healthcare-associated infection; occupational-associated infection; infectious organisms;

medical radiation science; diagnostic radiography; radiation therapy; nuclear medicine

1. Introduction
Healthcare-associated infections (HAIs) arise from the colonization of microorganisms on a new
host within a healthcare setting [1]. These include infectious organisms that patients are exposed to
when receiving care, and carry occupational risks of infection among healthcare workers [1]. HAIs are
problematic as they result in greater rates of mortality and morbidity, increase antimicrobial resistance
in microorganisms, and also increase costs for healthcare systems and those receiving care [1]. Over the
last century, developed countries have relied upon immunizations and antimicrobial medications as
the primary methods of disease prevention and management [2]. However, with the rise of multi-drug
resistant bacteria, the efficacy of these infection control methods has diminished [2]. More recently,
focus has shifted to hygiene and sanitation practices as the primary solution for preventing the
spread of these infections; aiming to reduce the occurrence of infections rather than treating infections

Healthcare 2020, 8, 80; doi:10.3390/healthcare8020080 www.mdpi.com/journal/healthcare

Healthcare 2020, 8, 80 2 of 14

post-colonization [1,3]. Despite improvements in these practices, HAIs are still prevalent in healthcare
facilities, affecting hundreds of millions of patients worldwide each year [1]. Appropriate infection
control guidelines, as well as healthcare worker compliance in applying these measures, are imperative
in reducing the number of HAIs, thereby reducing their burden and improving both patient and staff
outcomes [1]. Though many microbes (including viruses and fungi) are responsible for HAIs, where
an estimated 90% are caused by bacteria, including species of Staphylococcus, Escherichia, Enterococci,
and Klebsiella [4].
Different classes of bacteria behave differently in the presence of antimicrobial agents [5], therefore
distinguishing between them is necessary to ensure appropriate infection control methods are being
implemented, thus minimizing the occurrence of infections [5]. Using the Gram stain test, bacteria
can be separated phenotypically into Gram-positive and Gram-negative [5]. The primary difference
between Gram-positive and Gram-negative bacteria is the size and structure of the cell wall [5].
Gram-positive bacteria have a relatively thick, continuous peptidoglycan wall (20–80 nm) containing
teichoic and lipoteichoic acids [5]. Gram-negative bacteria have a thin layer of peptidoglycan; an outer
membrane that contains phospholipids; lipopolysaccharide; proteins; and while not directly involved
in staining, Gram-negative bacteria have a third layer (inner membrane) [5]. These two layers are
separated by a periplasmic space containing transport, degradative and cell-wall synthetic proteins [5].
The Gram-stain test involves staining bacteria with a crystal violet, attempting to remove the stain,
and then staining any decolourized cells with a red stain (safranin) [5]. Because of the differing
characteristics of the cell wall, Gram-positive bacteria trap the stain within the cross-linked structure of
the peptidoglycan layer, turning them purple [5]. Conversely, the crystal violet is not retained by the
thin peptidoglycan layer of Gram-negative bacteria, which washes off [5]. Accordingly, the presence of
the outer membrane gives Gram-negative bacteria a barrier that prevents substances accessing the
peptidoglycan layer, including antibacterial drugs and antimicrobial cleaning solutions [5]. Without
this extra layer of protection, mild detergents have a greater effect on Gram-positive bacteria than
Gram negative bacteria [5].
Medical radiation science (MRS) professionals have a high degree of direct contact with members
of the community who are susceptible to infections including children, the elderly, and those with
compromised immune systems [6]. This level of interaction means that if an MRS worker develops
an infection, there is a high chance of it spreading to these susceptible patients (and similarly from
patients to healthcare workers) [6]. In addition, a lot of the equipment utilized within MRS is shared
between patients with a broad range of pathologies [6]. As such, appropriate hygiene practices are
imperative to ensure this equipment does not harbor harmful microorganisms [6]. Reducing the
risk of exposure to infectious organisms is the responsibility of both the healthcare institution and
individual practitioners [1,7]. Most healthcare departments follow general infection control guidelines.
For instance, the New South Wales Health Infection Prevention and Control Policy [8] specifies that
shared patient equipment must be cleaned “according to manufacturer’s instructions” [8]. However,
due to the high-risk nature of patients within MRS, more specific methods of infection control may be
necessary in order to reduce the risk of HAIs. Furthermore, as different organisms require different
methods of infection prevention and control [5], such as sterilization or disinfection, infection control
methods should be specific to the nature of practice performed within the healthcare setting [1,5].
Research into the specific infectious organisms found within MRS departments may serve to guide
infection control strategies.
Current research predominantly focuses on HAIs among patients only, and not on the
occupational-associated infections (OAIs) that staff are exposed to. When addressing this gap,
Nienhaus et al. reported that the annual rate of recognized OAIs in non-government hospitals in
Germany were 15.3 per 100,000 healthcare workers [9]. This study did note that the data may have been
incomplete as it relied upon healthcare workers reporting infections, and considerable underreporting
of OAIs was likely to have occurred [9]. Nienhaus et al. concluded that the risk of OAIs remains high,
and as such “awareness for the infection risk and knowledge about infection prevention should be
Healthcare 2020, 8, 80 3 of 14

improved” [9]. Along with limited research regarding OAIs in healthcare workers, the prevalence of
infectious organisms across MRS professions has also been underexplored in the literature. As such,
this study aims to address these research gaps and contribute to the available literature by determining
the OAIs that MRS staff are most likely at risk of contracting within their departments. Having an
understanding of infectious organisms in MRS departments is an important first step in establishing
programs and approaches for reducing infection risks among healthcare workers, and consequently
among patients [10]. This systematic review therefore aims to collect and analyze data from recent
literature to determine the infectious organisms that MRS staff are exposed to within their departments;
and examine the reservoirs and modes of transmission of these organisms. This review extends the
scope of existent literature by including MRS, which has not been covered in previous research [10].

2. Materials and Methods

A systematic review (SR) of the literature was performed to identify studies and establish which
infectious organisms found in MRS have been identified in the literature, as the first part of an on-going
research project on improving healthcare risk management in MRS departments. The methodology
of this review was adapted from a previous SR analyzing the relationship between hospital staffing
and HAIs [10]. Reporting of this SR follows the preferred reporting items for systematic reviews and
meta-analyses (PRISMA) guidelines [11].

2.1. Protocol and Registration

The protocol for this SR was developed and registered to the international prospective register of
systematic reviews (PROSPERO; registration number: CRD42019127575).

2.2. Search Strategy

Electronic databases Scopus, EMBASE, the Cochrane Library, Medical Literature Analysis and
Retrieval System Online (MEDLINE), and the Cumulative Index to Nursing and Allied Health
Literature (CINAHL) were searched for relevant studies published between 1983 and 2018. The earliest
date restriction for studies included in this SR was chosen as a number of international infection control
documents were published in 1983, including the Association for Professionals in Infection Control
and Epidemiology Curriculum [12]. The search was performed on 27 January 2019 and restricted
to studies published in the English language. The search strategy (Table 1) was developed using a
combination of medical subject headings (MeSH) and keywords associated with the topic, including
“healthcare associated infection”, “hospital pathogens”, and “allied health.” Additional studies were
identified through a manual search of citations in included studies.

Table 1. The search strategy performed in one of the five databases (Medical Literature Analysis and
Retrieval System Online; MEDLINE).

# Searches
1 healthcare associated infection/
(“hospital acquired infection *” or “healthcare associated infection*” or hospital pathogens or “nosocomial”).mp. [mp = title, abstract, original
2 title, name of substance word, subject heading word, floating sub-heading word, keyword heading word, organism supplementary concept
word, protocol supplementary concept word, rare disease supplementary concept word, unique identifier, synonyms]
3 1 or 2
4 exp Allied Health Occupations/ or exp Allied Health Personnel/
(“radiation therap *” or “radiotherap*” or “allied health” or “nuclear medicine” or “molecular imag*”).mp. or radiography/ or “medical
imaging”.mp. [mp = title, abstract, original title, name of substance word, subject heading word, floating sub-heading word, keyword heading
5
word, organism supplementary concept word, protocol supplementary concept word, rare disease supplementary concept word, unique
identifier, synonyms]
6 4 or 5
7 3 and 6
8 limit 7 to English language
9 Limit 8 to year = ”1983–2018”
Healthcare 2020, 8, 80 4 of 14

2.3. Selection Criteria

All studies examining infectious organisms found directly in MRS departments, or outlining a risk
of infection to MRS staff, were included. Studies on clothing or equipment commonly found in these
departments were also included. Studies set in intensive care, critical care, surgical wards, or maternity
wards were excluded. Case studies, non-peer reviewed literature, reviews, editorials, commentaries,
articles on community-acquired infections, articles published prior to 1983, and articles not published
in English language were also excluded.

2.4. Definitions
For the purpose of this review, the following definitions were used:

• Medical radiation scientists were defined as healthcare professionals that perform diagnostic
imaging studies or plan and deliver radiation treatments to patients. Australian titles
for these professionals include diagnostic radiographers, nuclear medicine scientists, and
radiation therapists.
• Healthcare-associated infections (HAIs) comprise of infections acquired by persons in a healthcare
setting [4]. These include bloodstream infections and organism-specific infections (such as
methicillin-resistant Staphylococcus aureus and Clostridium difficile) that were defined as being
associated with healthcare in the literature [4].
• Occupational-associated infections (OAIs) refer to infections that healthcare professionals
acquire or are at risk of contracting from occupational exposure to infectious organisms within
their departments.

2.5. Study Selection

The titles and abstracts of all studies were assessed for relevance according to the SR aim, and
articles that were not relevant were excluded. The full texts of remaining articles were acquired to
further assess relevance based on the SR inclusion and exclusion and criteria. Articles with relevant
study design and data were included. The study selection process was performed by researches
using Covidence, an online SR management program. Two researches reviewed the title and abstracts
of studies, checking the level of agreement at several intervals. The average level of inter-reviewer
agreement was 93%. A third reviewer cross-checked included studies against the criteria at each stage
of the study selection process. Any disagreements or discrepancies in the application of the selection
criteria were resolved by discussion between all reviewers.

2.6. Data Extraction

Data was extracted into a Microsoft Excel spreadsheet. Data extracted from eligible studies
included: title, author(s), year of publication, country, study population, healthcare department
(setting), sample, type(s) of organisms, organism incidence and/or prevalence data, outcomes, and
limitations. Extracted data were reviewed by a second researcher.

2.7. Risk of Bias

Due to the varying study designs of included articles, checklists from The Joanna Briggs Institute
(JBI) were utilized to assess content validity [13]. The results of each eligible study were recorded;
however, these results were not used as a basis for exclusion. This assessment was performed
independently by two reviewers, and the level of correlation was determined.

2.8. Data Analysis

Data from included studies were synthesized and displayed in evidence tables. Summary tables
included studies that examined the prevalence of infectious organisms, specific department and
Healthcare 2020, 8, x 5 of 14
Healthcare 2020, 8, 80 5 of 14
Data from included studies were synthesized and displayed in evidence tables. Summary tables
included studies that examined the prevalence of infectious organisms, specific department and
infectious organisms,
infectious organisms, and
and equipment
equipment and
and infectious
infectious organisms.
organisms. Reporting
Reporting of
of organism
organism classifications
classifications
varied across the literature, and as such the data had to be analyzed further when formulating
varied across the literature, and as such the data had to be analyzed further when formulating these
these tables.
tables.
3. Results
3. Results
3.1. Overview
3.1. Overview
The volume of literature related to infectious organisms within MRS departments was initially
The volume of literature related to infectious organisms within MRS departments was initially
unknown, therefore the research question originally included all allied health professions as well
unknown, therefore the research question originally included all allied health professions as well as
as MRS. The search across five electronic databases returned 2063 studies, with an additional 8
MRS. The search across five electronic databases returned 2063 studies, with an additional 8 studies
studies identified through manual searching of reference lists. This number was reduced to 1676 once
identified through manual searching of reference lists. This number was reduced to 1676 once
duplicates were excluded. A total of 1634 abstracts that did not focus on medical radiation science
duplicates were excluded. A total of 1634 abstracts that did not focus on medical radiation science
departments (or associated equipment) or focused on community-acquired infections were excluded
departments (or associated equipment) or focused on community-acquired infections were excluded
at this stage.
at this stage.
The full texts of the remaining 42 articles were acquired and screened against the inclusion and
The full texts of the remaining 42 articles were acquired and screened against the inclusion and
exclusion criteria, resulting in 19 articles eligible for review and evaluation [6,14–31]. This iterative
exclusion criteria, resulting in 19 articles eligible for review and evaluation [6,14–31]. This iterative
process was carried out in accordance with the PRISMA statement [11] and is presented in Figure 1.
process was carried out in accordance with the PRISMA statement [11] and is presented in Figure 1.

Figure 1.
Figure Preferredreporting
1. Preferred reportingitems
itemsfor
forsystematic
systematicreviews
reviewsandandmeta-analyses
meta-analyses(PRISMA)
(PRISMA) flow flow
diagram [11] depicting the stages of article identification, screening, assessment for eligibility, and final
diagram [11] depicting the stages of article identification, screening, assessment for
inclusion of 19 articles.
eligibility, and final inclusion of 19 articles.
3.2. Characteristics of Included Studies
3.2. Characteristics of Included Studies
The final set of 19 included articles were published from Africa, Asia, North America, and Europe,
and were final
The set ofbetween
published 19 included articles
1998 and were
2018. published
A total from were
of 12 studies Africa,
setAsia, North America,
in diagnostic and
radiography
Europe, and were published between 1998 and 2018. A total of 12 studies were set
departments, and two were set in radiotherapy departments. Five studies were of a non-specific in diagnostic
radiography departments, and two were set in radiotherapy departments. Five studies were of a non-
Healthcare 2020, 8, 80 6 of 14

or non-MRS setting but included information on equipment found in MRS (such as mobile phones,
scissors, or identification badges). There were no studies set in nuclear medicine departments.
Of the included studies, 15 were of observational design and aimed to identify
the healthcare-associated organisms within MRS departments, or on equipment utilized in
MRS [6,14–18,20–24,26,28,30,31]. An additional observational study was included as it identified
the risk of occupational blood exposure, and therefore risk of infection to particular groups of
healthcare workers [19]. The other three included studies were quasi-experimental, and were designed
to test the ability of organisms to attach to and survive on equipment within MRS [25,27,29]. Table 2
describes the setting and healthcare equipment analyzed within the included studies, as well as the
number of infectious organisms identified.

Table 2. Characteristics of included studies.

Infectious Organisms
Reference Design Sample Setting Equipment Examined
Identified (n)
P=3
Ultrasound probes, couches,
Akpochafor et al. (2015) [14] CO 36 DR (US) N=3
coupling gel
F=2
P=6
Arora et al. (2009) [15] CS 160 NS Mobile phones
N=4
P=5
Bhat et al. (2011) [16] CS 204 NS Mobile phones
N=7
Boyle and Strudwick (2010) [17] CS 15 DR Lead rubber aprons P=4
Brewer et al. (2014) [18] CS 24 RT Heating appliances P=3
Denis et al. (2003) [19] CO 814 DR n/a n/a
Fox and Harvey (2008) [20] CS 40 DR Radiographic cassettes P=4
X-ray tubes, control panels,
Giacometti et al. (2004) [6] CS 144 DR n/a
radiographic cassettes, imaging plates
P=6
Hodges (2001) [21] CO 10 DR Radiographic markers N=4
NS = 1
P=5
Kelly and Trundle (2014) [22] CS 100 Nursing Pocket scissors
N=1
Kiran et al. (2018) [23] CO 98 DR (US) Ultrasound probes, coupling gel P=3
LaBan et al. (2004) [24] CS 14 RU Patient charts P=1
P=2
Lawson et al. (2002) [25] QE 3 DR Imaging cassettes
N=1
X-ray couches, chest stands,
radiographic cassettes, handles of x-ray P=2
Ochie and Ohagwu et al. (2009) [26] CO 301 DR
tube heads, control panels, exposure N=2
buttons, patient x-ray gowns
P=2
Ohara et al. (1998) [27] QE 9 DR (US) Ultrasound probes
N=2
P=6
Ota et al. (2007) [28] CS 118 NS Identification badges N=5
F=1
P=2
Ravine et al. (2017) [29] QE 4 RT Thermoplastic immobilization masks
N=2
P=4
Ultrasound probes, gel bottle tips,
Ridge (2005) [30] CS 28 DR (US) N=1
pressure cuffs
F=1
Tugwell and Maddison (2011) [31] CS 50 DR Radiographic markers P=4

CO, Cohort; CS, Cross-Sectional; DR, Diagnostic Radiography; F, Fungi; N, Gram-Negative Bacteria; NS, Non-Specific;
P, Gram-Positive Bacteria; QE, Quasi-Experimental; RT, Radiation Therapy; RU, Rehabilitation Unit; US, Ultrasound.

3.3. Infectious Organisms

Of the included studies, 15 examined the prevalence of specific organisms within MRS or on
equipment found in MRS departments. There were 88 counts of infectious organisms reported across
the included literature, which were then classified by their genus. A total of 19 different genera were
identified (Table 3), as well as three counts of coliforms (a group of Gram-negative bacteria that includes
the genera Escherichia, Klebsiella, Enterobacter, Serratia, and Citrobacter) and one count of unspecified
diplococci (Gram-positive or Gram-negative bacteria that occur as pairs of cocci). Seven different
genera of Gram-positive bacteria were identified, including Staphylococcus, Micrococcus and Bacillus; 10
Healthcare 2020, 8, 80 7 of 14

different genera of Gram-negative bacteria were identified including Acinetobacter and Escherichia; as
well as two genera of fungi (Candida and Cladosporium).

Table 3. Genera of healthcare-associated infectious organisms identified in the literature and their
common route/s of transmission.

Gram-Positive (n = 7) T Gram-Negative (n = 10) T Fungi (n = 2) T

Staphylococcus C Acinetobacter C Candida B/C
Micrococcus C Pseudomonas C Cladosporium C
Kocuria B Escherichia C
Bacillus A/C Klebsiella C
Streptococcus A/C Enterobacter C
Enterococcus C Citrobacter C
Corynebacterium A/C Proteus C
Neisseria A/C
Moraxella C
Vibrio C
A, Airborne; B, Bloodborne; C, Contact; T, Mode of Transmission.

At least one species of Staphylococcus was identified in every included study assessing
contamination of healthcare departments, with the exception of one study [6] that expressed their
results in terms of colony-forming units (CFUs) rather than specific organism(s). Staphylococcus,
Escherichia, Bacillus, and Corynebacterium species, as well as coliforms other than Escherichia, were
reported in all MRS departments studied, including diagnostic radiography, ultrasonography, and
radiation therapy. The three most frequently identified infectious organisms were Staphylococcus
(18.2%), Corynebacterium (11.7%), and Bacillus (10.4%), all of which are Gram-positive. In total, 13
different genera of infectious organisms were reported in diagnostic radiography departments (plus
one count of diplococci), 13 were reported in ultrasonography departments, and six were reported in
radiation therapy departments. There were 16 different genera reported from other departments with
Vibrio being the only organism not also identified in MRS departments (found on identification badges).
With the exception of Kocuria (blood transmissible), all of the infectious organisms identified in the
literature are transmissible via contact. Four of those organisms can also be transmitted through air.

3.4. Contamination of Equipment

A total of 31 different healthcare items were analyzed for infectious organisms within the included
studies, with observational studies assessing 30 different items of equipment, and quasi-experimental
studies assessing an additional item. Within this review, the majority of observational studies examining
contamination of equipment were set in diagnostic radiography departments (n = 8). Consequently,
most of the equipment analyzed (79.3%) was also located in diagnostic radiography departments, with
radiographic cassettes (n = 3) and ultrasound probes (n = 3) being the most commonly evaluated
sources of contamination.
The studies included in this SR reported that a relatively large percentage of healthcare equipment
used within MRS departments was contaminated with infectious microorganisms. Eight out of 15
studies (60%) noted that over 70% of sampled equipment was contaminated, with a pooled mean
of 62.5% and a range of 13.6%–100%. Five studies reported the contamination to be less than 50%,
with only one of those studies reporting contamination of less than 30%. Of all sampled equipment,
identification badges were reported to have the lowest level of contamination (13.6%). The number
of different infectious organisms identified on sampled equipment ranged from one to ten, with an
average of five genera identified per study.
Two of the included studies expressed the levels of contamination in terms of colony-forming
units (CFUs). The number of CFUs present on sampled equipment ranged from none to more than
1000, with a pooled mean of 82.6 CFUs per sample. One article examining the levels of contamination
Healthcare 2020, 8, 80 8 of 14

on radiographic cassettes reported bacterial contamination on 95% of samples [20]. However, this
study reported relatively low levels of contamination, with a range of 0–194 CFUs and a pooled mean of
approximately 30 CFUs per cassette [20]. Another study examined the CFUs on a range of equipment
utilized in diagnostic radiography departments, including x-ray tubes, control panels, imaging plates,
and radiographic cassettes [6]. This study reported control panels to be the most heavily contaminated
item, with a range of six to more than 1000 CFUs, and a pooled mean of 280.5 CFUs per control panel [6].
The pooled mean and ranges for each outcome measure evaluated are presented in Table 4, which was
adapted from a study by Schabrun and Chipchase [32].

Table 4. Pooled range and mean for each outcome measure investigated [32].

Outcome Measure Pooled Range Pooled Mean

Percentage of contamination of equipment 13.6–100 62.5
Number of colony-forming units present on sampled equipment 0–1000 82.6
Number of different genera on sampled equipment 1–10 5

3.5. Methodological Quality

Quality assessment of studies was performed using JBI critical appraisal tools [13]. According to
the hierarchy of evidence, all 19 studies included in this SR demonstrate the use of low (cross-sectional
and quasi-experimental) to intermediate (cohort) quality research designs [33]. Of the 19 studies,
18 were of sound methodological quality, with the remaining article reported to have indeterminate
quality. The appraisal results of each included study are reported in Table 5.

Table 5. Methodological quality of included studies.

Critical Appraisal Checklist Item Number
Study Outcome
1 2 3 4 5 6 7 8 9 10 11
Akpochafor et al. (2015) [14] Y Y Y Y Y Y Y Y Y Y Y Y
Arora et al. (2009) [15] Y Y Y Y U U Y Y - - - Y
Bhat et al. (2011) [16] Y Y Y Y Y Y Y Y - - - Y
Boyle and Strudwick (2010) [17] Y Y N Y Y Y U U - - - Y
Brewer et al. (2014) [18] Y Y Y Y Y Y U Y - - - Y
Denis et al. (2003) [19] Y Y Y Y Y Y Y Y Y Y Y Y
Fox and Harvey (2008) [20] Y Y Y Y Y Y U Y - - - Y
Giacometti et al. (2004) [6] Y Y Y Y Y Y Y Y - - - Y
Hodges (2001) [21] Y Y Y Y Y Y Y Y U Y Y Y
Kelly and Trundle (2014) [22] Y Y Y Y Y Y Y Y - - - Y
Kiran et al. (2018) [23] Y Y Y Y Y Y Y Y Y Y Y Y
LaBan et al. (2004) [24] Y Y U Y U U U Y - - - U
Lawson et al. (2002) [25] Y Y Y Y Y Y Y U Y - - Y
Ochie and Ohagwu et al. (2009) [26] Y Y Y Y U Y Y Y Y Y Y Y
Ohara et al. (1998) [27] Y Y Y Y Y Y Y U Y - - Y
Ota et al. (2007) [28] Y Y Y Y Y Y Y Y - - - Y
Ravine et al. (2017) [29] Y Y Y Y Y Y Y U Y - - Y
Ridge (2005) [30] Y Y Y Y Y Y Y Y - - - Y
Tugwell and Maddison (2011) [31] Y Y Y Y Y Y U Y - - - Y

* All studies appraised with the JBI checklist appropriate to the study design [13]. N, No; U, Unclear; Y, Yes.

4. Discussion
This SR was aimed at investigating the different infectious organisms that MRS staff may be
exposed to, their reservoirs, and their modes of transmission. The authors believe this is one of the
first such reviews to focus on this specific context. The literature search resulted in the inclusion of 19
relevant studies. Of the 19 studies, 15 aimed to identify the healthcare-associated organisms found
within MRS or on equipment utilized in MRS; one study investigated the risk of occupational blood
exposure among diagnostic radiographers; and the other three assessed the potential for equipment
used in MRS to act as a reservoir for infectious organisms.
Healthcare 2020, 8, 80 9 of 14

4.1. Infectious Organisms

A total of 19 different genera were identified, as well as three counts of coliforms and one count of
unspecified diplococci. These organisms included seven genera of Gram-positive bacteria, 10 genera
of Gram-negative bacteria, and two genera of fungi. Out of the 88 organisms recorded in the literature,
64% (n = 56) were Gram-positive bacteria, 31% (n = 27) were Gram-negative bacteria, 5% (n = 4)
were fungi, and 1% (n = 1) was unspecified bacteria. The majority of normal skin flora is comprised
of Gram-positive bacteria (such as Staphylococcus epidermidis species), increasing the likelihood of
it being transferred onto healthcare equipment during patient contact [28]. The inclusion of these
environmental flora in some studies may explain the higher levels of Gram-positive bacteria observed
on healthcare equipment.
With respect to exposure of MRS staff to HAI organisms, many of those identified (such as
normal flora) are considered “opportunistic”, whereby they generally will not cause infections
in healthy humans. However, as Maczulak [34] pointed out, under certain conditions (including
immunodeficiency, trauma, injury, or chronic disease), these opportunistic pathogens can cause infection.
MRS professionals often utilize needles within their practice; for example, when administering contrast
or radiopharmaceuticals, or when giving a patient positioning tattoos for radiotherapy. One of the
included articles outlining the prevalence of needle-stick injures noted that 34 out of 814 (4.18%)
of radiologists in the study group had experienced an occupational blood exposure at some point
in their career [19]. Due to this inherent risk of blood exposure through needlestick injuries, many
of these opportunistic infectious organisms (including Staphylococcus, Kocuria, and Candida) were
considered to be OAIs and as such were included in results. Furthermore, with the steady increase of
antibiotic-resistant bacteria, it can be expected that the prevalence of these serious infections among
immunocompetent humans will continue to increase, further justifying their inclusion [34].
A range of both Gram-positive and Gram-negative bacteria were identified in all MRS departments,
including Staphylococcus, Bacillus, Escherichia, and Corynebacterium. These results suggest that current
infection control methods may not be effective in preventing the occurrence of significant pathogens.
Of the 15 studies that identified the presence of Staphylococcus, 12 studies (80%) also reported the presence
of Staphylococcus aureus (S. aureus). S. aureus is considered a significant pathogen in healthcare settings,
affecting both immunocompromised and immunocompetent individuals [4]. Methicillin-resistant S.
aureus (MRSA) is a highly pathogenic strain of S. aureus that is resistant to antibiotics, significantly
increasing the difficulties associated with controlling the spread of disease [4]. Fortunately, only
one study [16] classified the identified species as MRSA. Of the three studies that did not report S.
aureus, two studies reported counts of coagulase-negative Staphylococcus, and the other study reported
Staphylococcus as a genus (failing to specify what species or strain was identified). As several of
the studies failed to do further testing to determine antibiotic resistance, it is possible that the true
prevalence of MRSA within MRS departments may have been underestimated.

4.2. Healthcare Equipment as a Reservoir for Microorganisms

Previous research has identified healthcare equipment as a common source of infectious organism
contamination [3,4]. A large proportion of sampled healthcare equipment was reported to be colonized
with infectious organisms. The pooled mean of 62.5% contamination is concerning, indicating that
over half of all healthcare equipment utilized in MRS harbors the infectious organisms responsible for
OAIs. As previously mentioned in microbiology, CFUs approaching 100 may be considered heavy
levels of contamination [20]. Giacometti et al. [6] reported a range of 6–1000 CFUs on equipment used
in diagnostic radiography, with a pooled mean of 280.5 CFUs found on control panels. This result is
concerning as it indicates that frequent points of contact for radiographers may be heavily contaminated,
increasing the risk of OAIs. These findings were consistent across the majority of studies, indicating a
need for more appropriate infection control approaches and/or compliance training.
Conflicting results were observed from the included studies examining microbial contamination
on mobile phones. [15,16] Bhat et al. [16] reported that 99% of all mobile phones assessed (201/204) were
Healthcare 2020, 8, 80 10 of 14

contaminated with bacteria, whereas Arora et al. [15] reported contamination in only 41% (65/160) of
samples from mobile phones. The samples were acquired using similar swabbing techniques, culturing
mediums and incubation periods, with the only obvious difference being the substances on the swabs
used during data collection. Considering the variation in organism counts, the conclusion that mobile
phones are a potential reservoir for infectious organisms is consistent.
There were no counts of viral organisms recorded in the included literature, which could potentially
be due to them not being tested for during data collection and analysis. Another explanation could be
that viruses require a host to reproduce, whereas bacteria do not [35]. This greatly reduces the lifespan
of viruses when compared to bacteria [35]. On equipment and surfaces, viruses have an average life
expectancy of a few days, whereas bacteria can survive for months [35]. There are several practical
reasons that may explain why viruses were not similarly examined for on MRS equipment. The largest
being the relatively high cost of testing for viral contamination when compared to bacteria. In addition,
there is a requirement for specialized medium, in vitro cell cultures/embryonated eggs, and low usage
of high cost test kits (e.g., Enzyme Linked Immunosorbent Assay (ELISA)) with a short outdate, which
means many hospital laboratories must send their viral cultures to a reference lab for analysis.

4.3. Transmission of Occupational-Associated Infections

The infectious organisms identified in the literature are transmissible through a number of
routes, including air, contact, and blood. Out of the 19 genera of organisms identified, 18 are contact
transmissible. This indicates that there is a high risk for these organisms to be transferred between
patients, healthcare equipment, and MRS professionals. Four of the included studies evaluated the
potential for organisms to attach and survive on equipment used in MRS. Hodges [21] concluded
that radiographic markers could be a reservoir for a range of bacteria, particularly if not cleaned
regularly or adequately. Similarly, Lawson et al. [25] reported a high potential for infectious organisms
to thrive on diagnostic imaging cassettes, with no noticeable reduction in growth throughout entire
test period (2 weeks). Ohara et al. [27] also demonstrated the capability of Staphylococcus species
to attach to ultrasound instruments, and Ravine et al. [29] evaluated the attachment potential of
bacteria on thermoplastic masks used in radiation therapy. These studies concluded that both
ultrasound instruments and thermoplastic masks could harbor infectious organisms, however the
tested bacteria did not appear to survive for long [27,29]. All four studies highlight the ability for
infectious microorganisms to attach and survive on MRS equipment, indicating a need for appropriate
infection control methods to prevent the occurrence of OAIs.

4.4. Limitations
While recognizing that SRs allow for a more objective appraisal of available evidence in comparison
to integrative, narrative, or scoping reviews, they can have a number of limitations. First, they cannot
pick up all the articles that may be published in any area [36,37]. In addition, they can also be
subject to a number of biases [38]. According to the hierarchy of evidence, observational studies are
ranked relatively low (in comparison to the “gold standard” randomized controlled trials) [33]. All
19 studies included in this review demonstrate the utilization of research designs that typically lack
adequate methodological rigor to minimize the effects of bias [33]. However, the use of such a rigid
hierarchy is being questioned by some authors such as Concato [39], who argue that evidence-based
hierarchies overstate the limitations of observational studies [39]. The majority of studies evaluating
the effectiveness of such a hierarchy have concluded that the importance of a study design depends on
the research question being studied [33,39]. A rigid hierarchy of evidence may not be well suited for
microbiological research, where the aim is observing the levels of organisms that are living within
an environment [40]. Randomized controlled trials are often not an appropriate study design for
this type of research as an intervention is not applied [39,40]. As such, applying a rigid design
hierarchy to research of this nature is potentially less important than evaluating the rigor of the study’s
methodology [40].
Healthcare 2020, 8, 80 11 of 14

Of the 19 studies included in this SR, 10 used samples involving less than 50 subjects. Additionally,
only five of those studies provided justification for their sample size. Smaller sample sizes increase
the probability of a sample returning a non-significant result [39], which makes it more difficult to
determine the true levels of infectious organisms within MRS departments and limits the application
of results to the wider population.
Several included studies failed to randomly select subjects, further limiting the ability for findings
to be extrapolated to a wider population. Six of the 19 studies used random selection, three used
convenience sampling, and the remaining 10 did not state their sampling procedure. Without
sufficient sampling information, it is difficult to determine whether sampled equipment is unbiased
and representative of the equipment most commonly used in MRS departments. Several studies
also incorporated a questionnaire into their research or recruited samples over several months, and
some studies failed to report whether participating professionals were blinded to the nature of
the study [15,22]. Without being blinded, subjects may have been inclined to clean their personal
equipment (radiographic markers, scissors, etc.) more regularly, thus directly affecting the reported
level of contamination.
The ability to extrapolate results even to other MRS departments (let alone broader healthcare)
is difficult as only two studies were set in radiation therapy departments, and there are no studies
set in nuclear medicine departments. Whilst the results were relatively consistent across the settings
of included studies, further research is necessary to determine whether the findings reported in this
review can be applied to other MRS departments.
Variable methods of data collection were used across the included studies, including different
swabbing techniques and culturing mediums. Levels of contamination were also reported differently,
with one study reporting the results solely in terms of CFUs rather than actual infectious organisms [6].
There were also discrepancies between which organism(s) each study was testing for, as well as
variations in classifications of reported organisms. Due to these factors, it is possible that the true
prevalence of infectious organisms in MRS may be underestimated.
Most studies classify coagulase-negative Staphylococcus as a significant pathogen, despite it being
part of the environmental skin flora [28]. However, certain studies, such as Ota et al. [28], excluded
environmental flora from their results to prevent overestimation of contamination. Accordingly, this
study also reported equipment with the lowest levels of contamination (13.6%). With the inclusion
of environmental flora, bacterial contamination was reported on 96.6% of samples [28]. This result
increases the pooled mean level of contamination from 62.5% to 68%. This discrepancy in reporting
across studies could result in either an underestimation or an overestimation of potentially infectious
organisms. Given the nature of opportunistic pathogens and the high-risk environment of MRS,
healthcare professionals should be mindful when applying infection control strategies to minimize the
occurrence of OAIs.

4.5. Research Gaps and Avenues for Further Research

Based on this SR, a number of research gaps have been identified.

1. No studies have been published on infectious organisms within nuclear medicine departments,
thus the risks of exposure for nuclear medicine staff and the potential of nuclear medicine
equipment to be vectors for OAIs remains unknown. Further research needs to be conducted to
address this gap and assess the correlation to other MRS professions.
2. No studies were undertaken and published from Australia or any South American countries.
Further research needs to be undertaken to determine whether the infectious organisms identified
within this study or different organisms are present in Australia and South America.
3. The reservoirs of infectious microorganisms identified in the SR are the basis for experimental
studies to assess the risk and burden of OAI exposure specifically in nuclear medicine departments
and among MRS staff and in MRS equipment.
Healthcare 2020, 8, 80 12 of 14

4. The literature has not identified if there is common OAI exposure risks when comparing MRS staff
and other allied health professionals OAI risk. Further empirical research needs to be undertaken
within diagnostic radiography, nuclear medicine, and radiation therapy departments and to be
compared to differing allied health professions.

5. Conclusions
This SR aimed to identify the infectious organisms that may be found in MRS, their reservoirs,
and modes of transmission. A range of different infectious organisms were identified in the literature,
including Gram-positive bacteria, Gram-negative bacteria, and fungi. Equipment utilized in MRS
departments, such as radiographic cassettes and ultrasound probes, was demonstrated to be a potential
reservoir for bacteria and a source of OAIs. As a vast majority of the infectious organisms identified
are transmissible by contact, appropriate infection control strategies are imperative to minimize the
number of infectious organisms on MRS equipment and surrounding surfaces. Reducing the number
of infectious organisms within MRS departments minimizes the risk of OAIs, and also decreases the
risk of these infectious organisms being transferred to patients and the wider community.
Only two of the included studies were set in radiation therapy departments and no studies were
set in nuclear medicine departments, limiting the generalizability of the results. Further research
would be recommended in order to provide clinically meaningful results that can be extrapolated to all
MRS professions.

Author Contributions: Conceptualization, D.L., M.P., and D.P.-B.; methodology, D.L., M.P., and D.P.-B.;
validation, D.L., M.P., and D.P.-B.; formal analysis, D.L., M.P., and D.P.-B.; data curation, D.L., M.P., and D.P.-B.;
writing—original draft preparation, D.P.-B.; writing—review and editing, D.L., M.P., and D.P.-B.; visualization,
D.L., M.P., and D.P.-B.; supervision, D.L. and M.P.; project administration, D.L., M.P., and D.P.-B. All authors have
read and agree to the published version of the manuscript.
Funding: This research received no external funding.
Acknowledgments: This research was undertaken as part of an honors project by the first-named author at the
University of Newcastle, Australia. The authors acknowledge the contributions of Debbie Booth, a senior research
librarian at the University of Newcastle for providing research training and assistance with the search. In addition,
the authors thank the anonymous experts who examined the honors thesis whose comments and feedback has
strengthened the final paper. The authors thank the peer reviewers whose invaluable comments, feedback and
insights helped us improve the quality of this article
Conflicts of Interest: The authors declare no conflict of interest.

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