Analysis of the Microbiota of the Physiotherapist's Environment.

OBJECTIVES: To analyze the microbiota of the physiotherapist's work environment to understand the existing potential risks and to adopt appropriate preventive measures.
DESIGN: Cross-sectional descriptive observational study.
SETTING: Physiotherapist's working environment. PARTICIPANTS: Physiotherapy and rehabilitation centers (N=19).
INTERVENTIONS: A microbiological sampling was carried out in the physiotherapy centers. The samples were studied using the usual culture and analysis methodology for characterization and isolation of a range of bacteria. MAIN OUTCOME MEASURES: Absolute and relative frequency of microorganism isolation.
RESULTS: In the analysis, pathogens normally responsible for nosocomial infections were detected, especially on instruments and equipment used by the physiotherapist such as sponge electrodes, and were significantly more contaminated than the rest of the places studied (P<.01).
CONCLUSION: This situation confirms the absence of measures and protocols for the prevention and control of such infections in the physiotherapist's environment, which is why they must be considered to protect both physiotherapy professionals and patients.

According to the data reported for the Study of Prevalence of Nosocomial Infections in Spain for the year 2016, the prevalence of nosocomial infections stood at 5.5% in hospital rehabilitation services, placing it fourth in the ranking, just behind surgical specialties. These particular types of infection often affect geriatric patients, children, and people with chronic diseases, all of whom are susceptible to acquiring infections within the hospital environment. Several factors that may be related to the high prevalence of nosocomial infections have been identified, including the current trend of starting the rehabilitation process at an early stage (even after a stay in an intensive care unit); difficulties in the isolation of patients susceptible to infection; heterogeneity in training among professionals in infection control interacting in these units; and the use of instruments and equipment whose handling, maintenance, and cleaning is frequently not included in the prevention protocols of nosocomial disease transmission.2, 3, 4, 5, 6, 7, 8, 9, 10

Previous investigations have been conducted to determine the microbiological contamination of the equipment and materials routinely used in physiotherapy, such as ultrasonic devices and therapy machines.11, 12, 13, 14 However, studies related to microbiological hazards that may occur in the physiotherapeutic environment are scarce both in our country and much of the Western world. ,

At present, there are no specific recommendations for the management and infection control in the physiotherapist’s environment based on objective data, despite calls to do so in the past by various authors. Therefore, the objective of this study was to discover the bacterial microbiota present in the physiotherapeutic environment in order to detect potential risks of nosocomial infections.

Methods

Design

A cross-sectional descriptive observational study was proposed to analyze the nosocomial bacterial microbiota present in the work environment of the physiotherapist.

Participants

Nineteen physiotherapy centers were selected for this investigation. Permission for the sampling was requested from the management or owners of the centers, and they were instructed not to inform the personnel of the time of the visit for the collection of samples to prevent influencing the behavior of the workers in the center. In each center, samples were collected from the treatment couches, the instruments and equipment being used, from the hands of the physiotherapists, and the ambient air. All samples were classified and numbered as shown in table 1 .

Table 1

Criterion for collection and numbering of the samples

Sample Groups	Samples
Treatment table, A
1	Head section
2	Intermediate section
3	Caudal section
Instruments and equipment, B
1	Reusable sponge electrodes
2	Adhesive reusable electrode
3	Single use adhesive electrode
4	Ultrasound probe
5	Ultrasound gel
6	Short-wave electrodes
7	Laser probe
8	Cold packs
Physiotherapist, C	Hands
Ambient air, D	250 liters of ambient air

Intervention

The collection of samples was carried out using 3 methods depending on the characteristics of the study site. With the exception of the samples taken from the ultrasound gel and the ambient air, a sterile swab with Copan Venturi Transystema transport medium was used. Each swab was handled individually using non-sterile vinyl gloves, the container was opened immediately before the collection of the sample, and the swab applicator was placed immediately and directly into the tube containing the transport medium without touching any external surfaces. For samples of ultrasound gel, a 5 cm3 sterile syringe was used for the extraction of 1 cm3 of gel from the container next to the therapeutic ultrasound equipment. Once the sample was taken, the extraction cannula of the syringe was sealed with the needle cap to avoid contamination during transport until the time of culturing. Finally, the collection of environmental air was done by collecting 250 liters of air directly onto a Petri dish with cysteine lactose electrolyte deficient agar, using an impactor device for taking aerial samples on standard 90 mm plates (MAS-100; Merck Milliporeb). All samples were labeled for correct follow-up and were transferred to the laboratory under cold conditions in a portable refrigerator for a period not exceeding 24 hours.

Once in the laboratory, the samples were aseptically plated on Difcoc prepared plates with the following solid culture media: blood agar, Baird-Parker agar, MacConkey agar, Mossel agar, and King B agar. The semisolid culture medium GI was used for the detection of bacterial motility. The plates were incubated at 37°C±1°C for a period of 24 hours. Thereafter, the plates were checked for the presence of colony-forming units. Identification of colonies was made through observational methods (ie, Gram stain negative and direct microscopic observation), biochemical tests (ie, catalase test and oxidase test), tests using miniaturized selected BBL Enterotube IId galleries for the identification of Enterobacteriaceae and other Gram-negative bacilli with negative oxidase results, and BBL Oxi/Ferm Tube IId for the detection of Gram-negative fermenting bacteria positive for oxidase and non-fermenting Gram-negative bacteria. After characterization of samples using the house commercial systems bioMérieux Viteke with gallery ATB STAPH 5 was used for the detection of staphylococci, and Vitek 2 Compact (applying the cards ID-GNB, ID-GPC, ID-NH) was used to identify Gram-negative bacilli, Gram-positive coccus, and Neisseria-Haemophilus, respectively.

Data analysis

All data obtained from the samples, respecting the confidentiality of their origin, were used and processed using the statistical analysis software SPSS (version 15.0)f and Statgraphics (version 5.1),g in addition to Microsoft Excel 2007h for the preparation of graphs and calculation tables.

The relative and absolute frequencies were calculated, and the value of the Spearman correlation coefficient between the grouping categories of the centers was calculated according to (1) their average daily care load, (2) the ownership of the center, and (3) their type of care (ambulatory or integrated into an organization with hospitalization of patients) versus the frequency of contamination of the samples and number of contaminating colonies. Analysis of variance was also performed on the total number of colonies in the 4 groups of samples analyzed. Finally, the differences between the total number of contaminated colonies with group B samples were analyzed using the Student t test to compare the incidence of contamination between certain instruments and equipment.

Results

Not all of the originally proposed samples to be obtained from each center could be collected because of the different characteristics and work modes normally used in the physiotherapy centers. Of the 247 potential samples, a total of 201 were collected. Of these, 83 were positive in growth after cultivation. The presence and distribution in the appearance of the species found was variable. Their absolute and relative frequencies are shown in tables 2 and 3 .

Table 2

Absolute frequency of microorganism isolated from the samples studied

Sample Type		Species
Sample Group A	Valid Samples	S.ep	C.fr	P.ag	A.b	St.m	S.au	S.s	Mc	M.ca	Aer	C.l	P.ae	P.nae	D.n	P.neu	K.r	P.m	S.ho
Head section of treatment table	19	4	1	−	−	−	−	−	−	−	1	−	−	1	2	1	1	−	1
Intermediate section of treatment table	19	2	−	1	1	−	−	1	−	−	−	−	−	−	−	−	−	1	−
Caudal section of treatment table	19	3	−	−	1	1	1	−	1	1	1	1	1	1	−	−	1	−	−
Total	57	9	1	1	2	1	1	1	1	1	2	1	1	2	2	1	2	1	1

Abbreviations. A.l, Acinetobacter lwoffii; A.b, Acinetobacter baumannii; Aer, Aeromonas spp.; Bac, Bacillus spp.; C.l, Cedecea lapagei; C.br, Citrobacter braakii; C.fr, Citrobacter freundii; Cor, Corynebacterium spp; D.n, Dermacoccus nishinomiyaensis; E.col, Escherichia coli; Flv, Flavobacterium spp.; K.r, Kocuria rosea; Mc, Micrococcus spp.; M.ca, Moraxella catarrhalis; P.ae, Pseudomonas aeruginosa; P.ag, Pantoea agglomerans; P.m, Pasteurella multocida; P.nae, Pseudomonas no aeruginosa spp.; P.neu, Pasteurella pneumotropica; Pr.s, Providencia stuartii; S.au, Staphylococcus aureus; S.ep, Staphylococcus epidermidis; Ser.m, Serratia marcescens; Ser.r, Serratia rubidaea; S.ho, Staphylococcus hominis; S.hy, Staphylococcus hyicus; S.int, Staphylococcus intermedius; S.s, Staphylococcus sciuri; St.m, Stenotrophomonas maltophilia.

Table 3

Relative frequency of microorganism isolated from the samples studied, expressed as percentages

Sample Type		Species
Sample Group A	Valid Samples	S.ep	C.fr	P.ag	A.b	St.m	S.au	S.s	Mc	M.ca	Aer	C.l	P.ae	P.nae	D.n	P.neu	K.r	P.m	S.ho
Head section of treatment table	19	21.0	5.3	−	−	−	−	−	−	−	5.3	−	−	5.3	10.5	5.3	5.3	−	5.3
Intermediate section of treatment table	19	10.5	−	5.3	5.3	−	−	5.3	−	−	−	−	−	−	−	−	−	5.3	−
Caudal section of treatment table	19	15.8	−	−	5.3	5.3	5.3	−	5.3	5.3	5.3	5.3	5.3	5.3	−	−	5.3	−	−
Total	57	15.8	1.7	1.7	3.5	1.7	1.7	1.7	1.7	1.7	3.5	1.7	1.7	3.5	3.5	1.7	3.5	1.7	1.7

Abbreviations. A.l, Acinetobacter lwoffii; A.b, Acinetobacter baumannii; Aer, Aeromonas spp.; Bac, Bacillus spp.; C.l, Cedecea lapagei; C.br, Citrobacter braakii; C.fr, Citrobacter freundii; Cor, Corynebacterium spp; D.n, Dermacoccus nishinomiyaensis; E.col, Escherichia coli; Flv, Flavobacterium spp.; K.r, Kocuria rosea; Mc, Micrococcus spp.; M.ca, Moraxella catarrhalis; P.ae, Pseudomonas aeruginosa; P.ag, Pantoea agglomerans; P.m, Pasteurella multocida; P.nae, Pseudomonas no aeruginosa spp.; P.neu, Pasteurella pneumotropica; Pr.s, Providencia stuartii; S.au, Staphylococcus aureus; S.ep, Staphylococcus epidermidis; Ser.m, Serratia marcescens; Ser.r, Serratia rubidaea; S.ho, Staphylococcus hominis; S.hy, Staphylococcus hyicus; S.int, Staphylococcus intermedius; S.s, Staphylococcus sciuri; St.m, Stenotrophomonas maltophilia.

The Spearman rank correlation coefficient was established by clustering the centers according to their average daily care load (0-50 patients/d, 50-100 patients/d, and 100-200 patients/d) , and the frequency of contamination of the samples. The ownership (privately or publicly owned), character of the center (centers with outpatient admission or centers with inpatients), and the frequency of contamination of the samples was also established. There was no correlation for a P value less than .05 in any of the cases.

The use of analysis of variance (table 4 ), showed there were significant differences between the different types of samples (differences between groups) with a P value less than .01. The least significant difference test indicated that the differences were proven (P<.05) between the B samples (instruments), which would be the most contaminated, and the rest of the samples. The result of the Student t test (see table 4) on the samples obtained from B1 (sponge electrodes) showed greater contamination than the rest of the group B samples, with a 99% probability (P<.01) compared with B4, B5, B7, and B8 samples (ultrasound probe, ultrasound gel, laser probe, and cryotherapy bags, respectively), and an 84% probability (P<.16, not significant) compared with B2 samples (reusable adhesive electrodes).

Table 4

Results of the analysis of the variance and the Student t test on the Group B samples (instruments)

ANOVA	P Value
Differences between groups	P<.01
Intra-group differences	NS

NOTE. B3 and B6 samples are not included because no microbiological contamination was found in these fomites.

Abbreviations: ANOVA, analysis of variance; LSD, least significant difference; NS, not significant.

Discussion

Considering the relative and absolute frequencies of isolation of microorganisms (see tables 2 and 3), it can be affirmed that there was a greater presence of coagulase-negative staphylococci, and Gram-negative non-Enterobacteriaceae bacteria on treatment couches or tables where patients are treated (A samples), which is in agreement with the studies by Kim et al and Kim et al, who also found significant contamination by these types of microorganisms. Other authors have studied the treatment tables exclusively in their work and have also found a higher presence of Gram-positive bacteria, especially species of coagulase-negative Staphylococcus. It should be noted that in all of the studies cited, except for that conducted by Burnham et al, the presence of S. aureus was low, which agrees with the findings of this study (see tables 2 and 3). Regarding the type of contamination between the 3 sections evaluated (head, intermediate, and caudal sections), there were no large differences observed with coagulase-negative S. spp. being predominant in all of them, a fact that is novel as there are no such data in the existing literature.

In the samples from group B, which were taken from various instruments commonly used in the physiotherapy room, a greater presence of Enterobacteriaceae bacteria was found, including species such as Pantoea agglomerans, Citrobacter freundii, Serratia marcescens, Serratia rubidaea, and Providencia stuartii. A significant presence of S. epidermidis was also detected. The samples obtained from group B were significantly more contaminated (P<.05) than the rest of the group of samples. The samples obtained from the sponge electrode (B1) presented higher and more varied contamination compared with the other samples (P<.01 for samples B4, B5, B7, and B8) (see table 4). These data indicate that the sponge electrode is a major source of microorganisms among the instruments evaluated, with more than 20 different bacterial species identified (see table 2, fig 1 ), including important pathogens such as S. aureus, Acinetobacter spp., and Escherichia coli. The identification of this type of electrode as the main source of microorganisms is concordant with the study by Kim et al, although most of the microorganisms identified in their study were non-Enterobacteriaceae Gram-negative bacteria (Acinetobacter baumannii, Acinetobacter lwoffii, and Acinetobacter junii). On the other hand, in their investigations of sponge electrodes, Lambert et al found a predominance of negative coagulase Staphylococcus and other Gram-negative species (Acinetobacter spp., Pasteurella spp., and Pseudomonas spp.). In this latter case, there was greater agreement with the results of the present study in relation to the high presence of negative coagulase Staphylococcus.

Fig 1

Total number of different species isolated in each type of sample.

Among the group B samples evaluated in this investigation, other instruments and equipment previously investigated were also studied, such as the probe (sample B4) and the ultrasound gel (sample B5). The study by Schabrun et al found that these devices were contaminated to a greater percentage with negative coagulase Staphylococcus, followed by Micrococcus spp., and certain environmental species of fungi. We found that the ultrasound heads had a lower presence of Gram-positive bacteria (Bacillus spp. and Micrococcus spp.) but S. epidermidis and S. aureus were also detected in isolation. As for the transduction ultrasound gel, small amounts (<5 colony-forming units/cm2) isolated from P. agglomerans, Stenotrophomonas maltophilia were found. In contrast, the study by Schabrun et al detected high concentrations of S. maltophilia and A. baumannii in the samples analyzed.

The microorganisms detected on the hands of the physiotherapists (C samples), were mostly Gram-positive bacteria, in keeping with the usual microbiota of the human body. Specifically, S. maltophilia and Corynebacterium spp. were detected. This fact reinforces the necessity of hand washing before touching the patient, and even combining hand washing with the use of gloves. Furthermore, it is necessary to wash properly after touching the patient to avoid cross contamination.

Finally, only S. epidermidis, Micrococcus spp., and Bacillus spp. were detected in the air samples from the centers, as well as fungi that were not isolated or identified as they were not the aim of this work. The presence of fungal spores as the main contaminant is also consistent with normal atmospheric conditions.

The absence of Enterobacteriaceae bacteria in the hand and air samples, along with the predominant presence of these microorganisms in B samples (especially the sponge electrodes [B1]), suggest that the transmission routes of these microorganisms are not attributable to the atmosphere or to the clinical staff. These microorganisms appear mainly in wastewater because they are part of the intestinal microbiota of mammals. Thus, fecal-oral transmission is the probable predominant route. Although the contaminant load of these bacteria is low, conditions of humidity, temperature, and the presence of organic remains, combined with poor hygiene practices with the sponge electrode, may favor their growth, which would explain the abundance of microorganisms found. In most of the literature consulted on the use, application, and conservation of sponge electrodes, there are no specific protocols for their disinfection and cleaning. The lack of sanitation behavior for this type of electrode is striking, especially when some texts recommend the direct application of the electrode on ulcers and scars, with only the interposition of a saline-moistened pad.

The absence of adequate cleaning and maintenance entails the accumulation and proliferation of nosocomial pathogens detected during this study in several of the fomites analyzed, among which are coagulase-positive staphylococci, Enterobacteriaceae bacteria, and Pseudomonas spp.22, 23, 24 The pathogenic action of many of these microorganisms has been exacerbated in recent years by the increasing frequency of antibiotic resistance, which affects a greater number of species.25, 26, 27, 28, 29, 30

The importance of maintaining good hygiene and disinfection measures in physiotherapy areas has recently been highlighted with the coronavirus disease 2019 pandemic that is currently extended worldwide. One of the main routes of contagion of severe acute respiratory syndrome coronavirus 2 occurs through the contact of the hands with contaminated surfaces and fomites, followed by the contact with the mucosa of the nose, mouth, and eyes. Furthermore, it is known that the survival of severe acute respiratory syndrome coronavirus 2 on materials such as copper, cardboard, stainless steel, and plastic has been reported to be 4, 24, 48, and 72 hours, respectively, when it is maintained at 21 to 23°C and with 40% of relative humidity. Disinfection is absolutely essential, not only of the physiotherapist's hands, but also of all instruments, equipment, and other fomites that will be in contact with the patient. Although these habits are widely described in community health hygiene practices, they are not always carried out in daily work and might have been a focus of transmission in the current pandemic.

Study limitations

It will be necessary to develop new studies aimed at determining the antibiotic susceptibility of the microorganisms found, as well as to develop preventive and regular monitoring strategies that control microbiological contamination with the aim of reducing the rate of nosocomial infections in the physiotherapist’s work environment. Moreover, in the present study, only the contamination of aerobic bacterial microorganisms has been analyzed. It is necessary to extend the analysis to include anaerobic bacteria, fungi, and viruses as well, especially as the current coronavirus disease 2019 pandemic leads us to consider viruses as a potential threat in the health care work environment.

Conclusions

The microbiota of the physiotherapist's work environment is formed by a heterogeneous group of microorganisms, essentially commensals, coming from the environment, which are common on the surface of the skin and other processes of cross-contamination. What is significant is the presence of microbial contamination found on the everyday working instruments and equipment of the physiotherapist, especially the electrode sponges used in electrotherapy treatments, which seem to concentrate a wide variety of microorganisms, many of them responsible for the most common nosocomial infections. The microorganisms isolated most frequently in the physiotherapist's environment are opportunistic pathogens in immunosuppressed patients, those weakened by chronic diseases, elderly patients, or patients vulnerable owing to their immaturity. Therefore, it is necessary to establish corrective measures to evaluate and control these risks, as well as expanding this research with new studies focused on anaerobic bacteria, fungi, and viruses.

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