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Alteration of Bacterial Antibiotic Sensitivity After Short-Term Exposure to Diagnostic Ultrasound


1 Department of Medical Physics and Medical Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran
2 Department of Radiology, Faculty of ParaMedicine, Hormozgan University of Medical Sciences, Bandar Abbas, IR Iran
3 Department of Radiology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran
4 Department of Microbiology, School of Medicine, Bushehr University of Medical Sciences, Bushehr, IR Iran
5 Department of Microbiology, School of Medicine, Kerman University of Medical Sciences, Kerman, IR Iran
6 Department of Biostatistics, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran
*Corresponding Authors: Seyed Mohammad Javad Mortazavi, Department of Medical Physics and Medical Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran. Tel: +98-7112349332, Fax: +98-7112349332; +98-7112289113, E-mail: mmortazavi@sums.ac.ir; Leili Darvish, Department of Medical Physics and Medical Engineering, School of Medicine, Shiraz University of Medical Sciences, Shiraz, IR Iran., E-mail: leili.darvish@gmail.com.
Iranian Red Crescent Medical Journal. 17(11): e26622 , DOI: 10.5812/ircmj.26622 | PMID: 26732124 | PMCID: PMC4698328
Article Type: Research Article; Received: Jan 5, 2015; Revised: Mar 27, 2015; Accepted: Apr 14, 2015; epub: Nov 28, 2015; collection: Nov 2015

Abstract


Background: Many pathogenic bacteria show different levels of antibiotic resistance. Furthermore, a lot of hospital-acquired infections are caused by highly resistant or multidrug-resistant Gram-negative bacteria. According to WHO, patients with drug-resistant infections have higher morbidity and mortality. Moreover, patients infected with bacteria that are resistant to antibiotics considerably consume more healthcare resources.

Objectives: In this study, we explored a physical method of converting drug-resistant bacteria to drug-sensitive ones.

Materials and Methods: This is an in vitro case-control study, performed at the Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences (SUMS), Shiraz, Iran in 2014. All experiments were carried out using Gram-negative bacteria Klebsiella pneumonia and E. coli and Gram-positive Staphylococcus aureus and Streptococcus group A, isolated from hospitalized patients. The bacterial strains were obtained from the Persian Type Culture Collection, IROST, Iran (Klebsiella pneumonia PTCC 1290) and Bacteriology Department of Shahid Faghihi Teaching Hospital, Shiraz, Iran (E. coli, Staphylococcus aureus, and Streptococcus group A). The bacteria in culture plates were exposed to diagnostic ultrasound using a MyLab70XVG sonography system for 5 minutes. Then, the bacteria were cultured on Mueller-Hinton agar and incubated at 35°C for 18 hours. Finally, antibiotic susceptibility test was performed and the inhibition zone in both control and exposed groups were measured. Three replicate agar plates were used for each test and the inhibition zones of the plates were recorded.

Results: Compared with the results obtained from unexposed bacteria, statistically significant variations of sensitivity to antibiotics were found in some strains after short-term exposure. In particular, we found major differences (making antibiotic-resistant bacteria susceptible or vice versa) in the diameters of inhibition zones in exposed and non-exposed samples of Klebsiella pneumonia and Streptococcus.

Conclusions: This study clearly shows that short-term exposure of microorganisms to diagnostic ultrasonic waves can significantly alter their sensitivity to antibiotics. We believe that this physical method of making the antibiotic-resistant population susceptible can open new horizons in antibiotic therapy of a broad range of diseases, including tuberculosis.

Keywords: Drug Resistance; Ultrasound; Infection; Antibiotics

1. Background


The World Health Organization (WHO) believes that antimicrobial resistance (AMR) is a progressive and serious threat to global public health that endangers the effective prevention and treatment of an ever-increasing range of infections caused by bacteria, parasites, viruses, and fungi. According to WHO, as AMR can be found in all parts of the world, international actions are needed to overcome this problem as new resistance mechanisms emerge and spread globally.


Diagnostic sonography as a very safe, reliable, and economic way to observe various organs of the body (1, 2) uses ultrasound waves in the frequency range of 1 - 20 MHz (however, frequencies up to 50 - 100 MHz have been used experimentally in ultrasound biomicroscopy, a technique used for obtaining high-resolution in vivo imaging of special regions of the body such as the anterior chamber of the eye). The annual number of ultrasound examinations has increased dramatically over the past decade.


The induction of “adaptive response” in bacteria has been already reported (3). Adaptive response can be defined as the induction of repair by pre-exposure to a low level chemical or physical stress. We have previously shown that pre-exposure of living organisms to low levels of ionizing (4-7) or a large dose of non-ionizing radiation (8-12), decrease the detrimental biological effects on these organisms compared to exposure to the large dose alone. Therefore, adaptive response in bacteria can also be observed as the decrease in lethal effects of antibiotics after exposure to a low level physical stress such as short exposure to electromagnetic radiation or ultrasound.

2. Objectives


On the other hand, we have previously shown that pre-exposure of laboratory animals to non-ionizing electromagnetic radiation in radiofrequency (RF) range can induce a survival adaptive response which can be observed as increased resistance to a subsequent Escherichia coli infection (13, 14). Furthermore, over the past years, we have investigated the bio effects of physical stresses such as exposure to ultrasound for enhancing the sensitivity of bacteria to different antibiotics. This study aimed at developing an ultrasound-assisted method for increasing bacterial sensitivity to antibiotics.

3. Materials and Methods


3.1. Isolation and Identification of Isolates

This is an in vitro case-control study, performed at the Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences (SUMS), Shiraz, Iran in 2014. The bacterial strains were obtained from the Persian Type Culture Collection, IROST, Iran (Klebsiella pneumonia PTCC 1290) and Bacteriology Department of Shahid Faghihi Teaching Hospital, Shiraz, Iran (E. coli, Staphylococcus aureus and Streptococcus group A).


The samples were cultured on blood agar and MacConkey agar for the isolation of microorganism. The culture plates were incubated at 37°C for 24 hours and observed for the presence or absence of visible bacterial growth.


3.2. Antibiotic Susceptibility Tests

We performed the antibiotic susceptibility tests by using the Kirby-Bauer disk diffusion method on Muller-Hinton agar (Figure 1). Drug susceptibility test was performed for nitrofurantoin, nalidixic acid (30 μg), gentamicin (10 μg), sulfamethoxazole, cephalexin, ciprofloxacin (5 μg), and cephalothin for Gram-negative bacteria and vancomycin (30 μg), erythromycin (15 μg), amoxicillin (20 μg), penicillin (10 Units), clindamycin (2 μg), and cefixime (5 μg) for Gram-positive bacteria. All culture media and antibiotic disks were purchased from Merck (Germany) and HiMedia Laboratories (Mumbai, India), respectively. Results for antibiotic susceptibility pattern before and after exposure to ultrasound were recorded and analyzed. The inhibition zone of each plate was recorded as the average of 2 diameters (mm) measured at right angles to one another. Three replicate agar plates were used for each regime. According to the CLSI guidelines (2013), the result were categorized as sensitive, intermediate, and resistance.


Figure 1.
Antibiotic Susceptibility Test Performed by Using the Kirby-Bauer Disk Diffusion Method on Muller-Hinton Agar

3.3. Ultrasound Apparatus

The bacteria in culture plates were exposed to diagnostic ultrasound using a recently calibrated MyLab70XVG sonography system (EsaoteBiomedicaMyLab70XVG–Genova, Italia). All ultrasound exposures were performed by a 7.5 - 13 MHz linear array probe (type LA523) by an expert radiologist at Shahid Faghihi teaching Hospital, Shiraz, Iran.


3.4. Statistical Methods

The mean diameters of inhibition zones of the 3 replicates in exposed and non-exposed groups were compared using the nonparametric Mann-Whitney test. The significance level was considered at P < 0.05.

4. Results


Findings of this study are summarized in Tables 1 and 2. Compared to the results obtained from unexposed bacteria, statistically significant variations of sensitivity to antibiotics were found in some strains after short-term exposures. Tables 1 and 2 show the mean diameters of the inhibition zones of non-exposed Klebsiella and those exposed to diagnostic ultrasound in PenM, Res H and Doppler modes, respectively. This part of the study showed major differences in the diameters of zones of inhibition in exposed and non-exposed samples of Klebsiella pneumonia and Staphylococcus aureus. In two modes of ultrasound exposure (PenM and Doppler), ultrasonic waves made sensitive Klebsiella pneumonia resistant to cephalexin (P = 0.001). In ResH mode, ultrasound made sensitive Klebsiella pneumonia intermediate resistant to cephalexin (P = 0.011).


Table 1.
The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa

Table 2.
The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteria a

Tables 3 and 4 show the mean diameters of the inhibition zones of non-exposed Staphylococcus epidermidis and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. Again, statistically significant variations of sensitivity to antibiotics were found in Staphylococcus epidermidis after short-term exposure to ultrasound. However, ultrasound was unable to make antibiotic-resistant bacteria susceptible or to make sensitive bacteria, resistant.


Table 3.
The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus epidermidis in bacteria Exposed to Diagnostic Ultrasound (PenM and Res H modes) and Non-Exposed Bacteria

Table 4.
The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus epidermidis in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

Tables 5 and 6 show the mean diameters of the inhibition zones of non-exposed Staphylococcus aureus and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. As observed in previous tests, statistically significant variations of sensitivity to antibiotics were found in Staphylococcus aureus after short-term exposure to ultrasound. In this experiment, ultrasound was able to make antibiotic-resistant bacteria susceptible. In one mode of ultrasound exposure (PenM) ultrasound made resistant Staphylococcus aureus sensitive to amoxicillin (P = 0.003). However, ultrasound was unable to make antibiotic-resistant bacteria susceptible in other modes (ResH and Doppler). Tables 7 and 8 show the mean diameters of the inhibition zones of non-exposed Salmonella sp. and those exposed to diagnostic ultrasound in PenM, ResH and Doppler modes, respectively. Although statistically significant variations of sensitivity to antibiotics were found in Salmonella sp. after short-term exposure to ultrasound, conversion of antibiotic-resistant bacteria to susceptible or vice versa was not found.


Table 5.
The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (PenM and ResH Modes) and Non-Exposed Bacteriaa

Table 6.
The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

Table 7.
The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa

Table 8.
The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

5. Discussion


To the best of our knowledge this is the first study that explores the effect of ultrasound exposure as a mechanical stress on the antibiotic susceptibility of some microorganisms. In this study, we found some major alterations in the diameters of the inhibition zones in Klebsiella pneumonia and Staphylococcus aureus after exposure to ultrasound waves. Interestingly, ultrasound was capable of making some antibiotic-resistant bacteria susceptible as well as making some sensitive bacteria, resistant. Antibiotic resistance can be defined as the ability of microorganisms to resist the lethal effects of specific antibiotics. This phenomenon occurs when the effectiveness of drugs to cure or prevent infections reduces or vanishes (15). Lattimer et al. (16) in a paper published in JAMA in 1961 reported that in spite of great advances in medicine, scientists are losing the battle against drug resistance. At that time, they believed that the speed of discovery and development of new drugs was not fast enough to take over the significant ability of some microorganisms to develop resistant mutants. Therefore, they predicted that humans might encounter lethal epidemics in the future if they could not control drug-resistant microorganisms (16). Now, we should confess that the situation has not changed significantly since the publication of this paper more than 50 years ago.


The decrease observed in the diameters of the inhibition zones in Klebsiella pneumonia and Staphylococcus aureus after exposure to ultrasound waves, can be interpreted as an adaptive response. Adaptive response can be defined as the acquisition of radiation resistance against exposure to high dose in cultured cells or organisms which had been previously pretreated with an adapting low dose radiation (this low dose radiation is also called “priming dose” or “conditioning dose”) (17). This observation is generally in line with our previous reports on the induction of adaptive response after exposure to low levels of ionizing (4-7) and non-ionizing radiation (8-12). More specifically, our findings are in line with the reports indicating that when bacteria are exposed to mild forms of different stresses (chemical and physical stresses), this stress improves their abilities to adapt and become resistant to any subsequent more extreme exposures (18-20). Also, that pre-exposure can increase the resistance to other exposures (e.g. exposure to antibiotics) and induce “cross-protection” phenomenon (3).


The main limitation of our experiment was the low number of bacterial strains studied. However, the unique inter-department collaboration in our study was a significant strength point. Based on these results, we believe that short-term exposure of microorganisms to diagnostic ultrasonic waves can significantly alter their sensitivity to antibiotics. It can be concluded that the physical methods of making the antibiotic-resistant population susceptible can open new horizons in antibiotic therapy fora broad range of diseases, including tuberculosis. On the other hand, when exposure to ultrasound makes the antibiotic-susceptible population resistant, this may endanger patients’ lives.

Footnotes

Authors’ Contribution: Study concept and design: Seyed Mohammad Javad Mortazavi. Acquisition of data: Seyed Mohammad Javad Mortazavi, Leili Darvish, Mohammad Abounajmi, Sina Zarei, Tahereh Zare, Mohammad Taheri, and Samaneh Nematollahi. Analysis and interpretation of data: Seyed Mohammad Javad Mortazavi and Samaneh Nematollahi. Drafting of the manuscript: Seyed Mohammad Javad Mortazavi. Critical revision of the manuscript for important intellectual content: Seyed Mohammad Javad Mortazavi. Statistical analysis: Samaneh Nematollahi. Study supervision: Seyed Mohammad Javad Mortazavi.
Funding/Support: This study was financially supported by the Ionizing and Non-ionizing Radiation Protection Research Center (INIRPRC), Shiraz University of Medical Sciences (SUMS), Shiraz, Iran.

References


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Table 1.

The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
PenM Mode
Nitrofurantoin 17.67 ± 0.58 Sensitive 16.34 ± 0.58 Intermediate 0.047
Nalidixic acid 20.34 ± 0.58 Sensitive 19.67 ± 0.58 Sensitive 0.230
Gentamicin 14.34 ± 0.58 Intermediate 14.67 ± 0.58 Intermediate 0.519
Sulfamethoxazol 20.67 ± 0.58 Sensitive 21.34 ± 0.58 Sensitive 0.230
Cephalexin 10.67 ± 1.15 Resistant 16.67 ± 0.58 Sensitive 0.001
Ciprofloxacin 19.67 ± 0.58 Intermediate 20.34 ± 0.58 Intermediate 0.230
Cephalothin 16.67 ± 0.58 Intermediate 18.34 ± 0.58 Sensitive 0.024
Res H Mode
Nitrofurantoin 17.34 ± 0.58 Sensitive 16.34 ± 0.58 Intermediate 0.101
Nalidixic acid 19.34 ± 0.58 Sensitive 19.67 ± 0.58 Sensitive 0.519
Gentamicin 13.67 ± 0.58 Intermediate 14.67 ± 0.58 Intermediate 0.101
Sulfamethoxazol 20.34 ± 0.58 Sensitive 21.34 ± 0.58 Sensitive 0.101
Cephalexin 13.34 ± 1.15 Intermediate 16.67 ± 0.58 Sensitive 0.011
Ciprofloxacin 17.67 ± 0.58 Intermediate 20.34 ± 0.58 Intermediate 0.005
Cephalothin 16.34 ± 0.58 Intermediate 18.34 ± 0.58 Sensitive 0.013
a (N = 3).
b Data are presented as mean ± SD.

Table 2.

The Mean Diameters of the Inhibition Zones (mm) of Klebsiella (PTCC: 1290) in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteria a

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
Nitrofurantoin 16.34 ± 0.58 Intermediate 16.34 ± 0.58 Intermediate > 0.999
Nalidixic acid 18.34 ± 0.58 Intermediate 19.67 ± 0.58 Sensitive 0.047
Gentamicin 12.34 ± 0.58 Resistant 14.67 ± 0.58 Intermediate 0.008
Sulfamethoxazole 17.67 ± 0.58 Sensitive 21.34 ± 0.58 Sensitive 0.001
Cephalexin 12.34 ± 0.58 Resistant 16.67 ± 0.58 Sensitive 0.001
Ciprofloxacin 17.34 ± 0.58 Intermediate 20.34 ± 0.58 Intermediate 0.003
Cephalothin 16.34 ± 0.58 Intermediate 18.34 ± 0.58 Sensitive 0.013
a (N = 3).
b Data are presented as mean ± SD.

Table 3.

The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus epidermidis in bacteria Exposed to Diagnostic Ultrasound (PenM and Res H modes) and Non-Exposed Bacteria

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesa Sensitivity Inhibition Zonesa Sensitivity
Pen M Mode
Vancomycin 16.34 ± 0.58 Sensitive 18.67 ± 0.58 Sensitive 0.008
Erythromycin 9.34 ± 0.58 Resistant 10.67 ± 0.58 Resistant 0.047
Amoxicillin 14.5 ± 0.5 Resistant 19.67 ± 0.58 Resistant 0.0001
Penicillin 17.34 ± 0.58 Resistant 19.67 ± 0.58 Resistant 0.008
Cefixime 9.84 ± 0.77 Resistant 9.34 ± 0.58 Resistant 0.417
ResH Mode
Vancomycin 16.67 ± 0.58 Sensitive 18.67 ± 0.58 Sensitive 0.013
Erythromycin 10 Resistant 10.67 ± 0.58 Resistant 0.184
Amoxicillin 15.5 ± 0.87 Resistant 19.67 ± 0.58 Resistant 0.002
Penicillin 19.67 ± 0.58 Resistant 19.67 ± 0.58 Resistant > 0.999
Cefixime 9.34 ± 0.58 Resistant 9.34 ± 0.58 Resistant > 0.999
a Data are presented as mean ± SD.

Table 4.

The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus epidermidis in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
Vancomycin 16.34 ± 0.58 Sensitive 18.67 ± 0.58 Sensitive 0.008
Erythromycin 8.84 ± 0.29 Resistant 10.67 ± 0.58 Resistant 0.008
Amoxicillin 16.67 ± 0.58 Resistant 19.67 ± 0.58 Resistant 0.003
Penicillin 19.34 ± 0.58 Resistant 19.67 ± 0.58 Resistant 0.519
Cefixime 9.34 ± 0.58 Resistant 9.34 ± 0.58 Resistant > 0.999
a (N = 3).
b Data are presented as mean ± SD.

Table 5.

The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (PenM and ResH Modes) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
Pen M Mode
Vancomycin 17.67 ± 0.58 Sensitive 14.67 ± 0.58 Sensitive 0.003
Erythromycin 0 Resistant 8.34 ± 0.58 Resistant 0.002
Amoxicillin 20.34 ± 0.58 Sensitive 17.34 ± 0.58 Resistant 0.003
Penicillin 17.67 ± 0.58 Resistant 13.17 ± 0.77 Resistant 0.001
Clindamycin 29.34 ± 0.58 Sensitive 26.34 ± 0.58 Sensitive 0.003
Cefixime 15.17 ± 0.29(I) ntermediate 16.84 ± 0.29 Intermediate 0.002
ResH Mode
Vancomycin 16.67 ± 0.58 Sensitive 14.67 ± 0.58 Sensitive 0.013
Erythromycin 0 Resistant 8.34 ± 0.58 Resistant 0.002
Amoxicillin 17.5 ± 0.87 Resistant 17.34 ± 0.58 Resistant 0.795
Penicillin 16.67 ± 0.58 Resistant 13.17 ± 0.77 Resistant 0.003
Clindamycin 29.67 ± 0.58 Sensitive 26.34 ± 0.58 Sensitive 0.002
Cefixime 15.34 ± 0.58 Intermediate 16.84 ± 0.29 Intermediate 0.016
a (N = 3).
b Data are presented as mean ± SD.

Table 6.

The Mean Diameters of the Inhibition Zones (mm) of Staphylococcus aureus in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
Vancomycin 18.67 ± 0.58 Sensitive 14.67 ± 0.58 Sensitive 0.001
Erythromycin 0 Resistant 8.34 ± 0.58 Resistant 0.002
Amoxicillin 18.84 ± 0.29 Resistant 17.34 ± 0.58 Resistant 0.016
Penicillin 16.34 ± 0.58 Resistant 13.17 ± 0.77 Resistant 0.005
Clindamycin 29.5 ± 0.87 Sensitive 26.34 ± 0.58 Sensitive 0.006
Cefixime 15.5 ± 0.5 Intermediate 16.84 ± 0.29 Intermediate 0.016
a (N = 3).
b Data are presented as mean ± SD.

Table 7.

The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (PEN M and RES H Modes) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
PenM Mode
Ciprofloxacin 28.34 ± 0.58 Sensitive 34.34 ± 0.58 Sensitive 0.0001
Cefixime 23.67 ± 0.58 Sensitive 25.67 ± 0.58 Sensitive 0.013
Amikacin 21.67 ± 0.58 Sensitive 21.67 ± 0.53 Sensitive > 0.999
Sulfamethoxazole/trimethoprim 26.67 ± 0.58 Sensitive 29.67 ± 0.58 Sensitive 0.003
Cephalexin 26.34 ± 0.58 Sensitive 24.34 ± 0.58 Sensitive 0.013
Gentamycin 20.67 ± 0.58 Sensitive 20.67 ± 0.58 Sensitive > 0.999
ResH Mode
Ciprofloxacin 27.34 ± 0.58 Sensitive 34.34 ± 0.58 Sensitive 0.0001
Cefixime 22.34 ± 0.58 Sensitive 25.67 ± 0.58 Sensitive 0.002
Amikacin 20.67 ± 0.58 Sensitive 21.67 ± 0.53 Sensitive 0.101
Sulfamethoxazole/trimethoprim 26.34 ± 0.58 Sensitive 29.67 ± 0.58 Sensitive 0.002
Cephalexin 23.17 ± 0.29 Sensitive 24.34 ± 0.58 Sensitive 0.035
Gentamycin 17.67 ± 0.58 Sensitive 20.67 ± 0.58 Sensitive 0.003
a (N = 3).
b Data are presented as mean ± SD.

Table 8.

The Mean Diameters of the Inhibition Zones (mm) of Salmonella in Bacteria Exposed to Diagnostic Ultrasound (Doppler) and Non-Exposed Bacteriaa

Antibiotic Bacteria Exposed to Diagnostic Ultrasound Non-Exposed Bacteria P Value
Inhibition Zonesb Sensitivity Inhibition Zonesb Sensitivity
Ciprofloxacin 27.67 ± 0.58 Sensitive 34.34 ± 0.58 Sensitive 0.0001
Cefixime 23.34 ± 0.58 Sensitive 25.67 ± 0.58 Sensitive 0.008
Amikacin 21.34 ± 0.58 Sensitive 21.67 ± 0.53 Sensitive 0.519
Sulfamethoxazole/trimethoprim 28.84 ± 0.77 Sensitive 29.67 ± 0.58 Sensitive 0.206
Cephalexin 23.67 ± 0.58 Sensitive 24.34 ± 0.58 Sensitive 0.203
Gentamycin 18.5 ± 0.5 Sensitive 20.67 ± 0.58 Sensitive 0.008
a (N = 3).
b Data are presented as mean ± SD.

Figure 1.

Antibiotic Susceptibility Test Performed by Using the Kirby-Bauer Disk Diffusion Method on Muller-Hinton Agar