Kuwait, a country in the Gulf area of the Middle East (southwest Asia), is mostly a dry desert with regular sandstorms. Occasionally, sandstorms could result in closures of operating theatres due to high levels of dust in the atmospheric air. Air samples from clinical and outdoor settings often share properties and similar distribution of bacteria [7], therefore, it is important to study the impact of the air during sandstorms and rising dust on the indoor hospital air. Increasingly high temperatures and hot climates, coupled with high population and over prescription of antibiotic medication, may play a significant role in the presence of
The sand and dust effectively impact human health, the environment, and the economy of countries. Its damage to the infrastructures and interruption to transportation is evident. But the long-term effect of these particles on human health explored here should be studied more [12]. The airborne dust and its particle size determine the amount of impact on people’s health. World scientists have linked environmental conditions like dust storms to the increasing pattern of bacterial infections amongst the populations. When the dust particles are inhaled in hot dry weather, the nose and throat mucosa are damaged, giving rise to bacterial infections. This extreme event is prevalent in many parts of the world because of its ability to travel through the earth’s atmosphere. However, the main sources of dust are the arid regions of North Africa, the Arabian Peninsula, China, and Central Asia [12]. The Middle East, especially the places like Kuwait and Dubai, experience dusty weather more commonly when compared to others. Kuwait has a subtropical desert climate that results in extremely hot and dry summers with a very short winter. The oil industries present here contribute to toluene and sulphur dioxide pollution. The increase in dust storms every year certainly plays an important role in the antibiotic resistance amongst the people of Kuwait, and it should lead to more studies.
In this study, we were able to isolate the following bacteria from hospital air samples: Staphylococcus aureus, coagulase-negative Staphylococcus, Bacillus spp., Acinetobacter spp., Micrococcus spp., Corynebacterium simulans, Luteimonas terrae, Agrobacterium salinitolerans, Corynebacterium amycolatum, Corynebacterium casei, and Escherichia fergusonii. Our findings are similar to the study conducted by Toar et al. [13] who studied hospital operating room air samples and found the following isolates: Klebsiella pneumoniae, coagulase-negative Staphylococcus,*[1] and Bacillus subtilis. In another study Solomon et al. [14] collected hospital indoor air samples via passive air sampling method. They found coagulase-negative Staphylococci (29.6%), Staphylococcus aureus (26.3%), Pseudomonas aeruginosa (5.3%), Acinetobacter spp., (9.5%), Enterococci species, Enterococcus faecalis and Enterococcus faecium (16.5%), Acinetobacter species (9.5%), and Escherichia coli (5.8%). Similar types of bacteria were found in our study, however, only they did not isolate Bacillus spp., and we did not isolate Enterococcus spp. In another study by Kunwar et al.[15] across eight hospitals in Kathmandu, Nepal, isolated bacteria from hospital air samples included Staphylococcus aureus (47.18%), Pseudomonas spp. (1.82%), and others such as coagulase negative Staphylococcus, Streptococcus spp., Micrococcus spp., Bacillus spp., E. coli, and Proteus spp. Like our study, Kunwar et al. were able to isolate Staphylococcus spp. and Bacillus spp., but not Acinetobacter.
In terms of Staphylococcus, the isolates in our study exhibited resistance to trimethoprim, erythromycin, ciprofloxacin, cefoxitin, tetracycline, and clindamycin; only 12% were resistant to oxacillin. In the study performed by Solomon et al. 14, methicillin resistance was observed in 38.9% of the isolates, higher than this study. In other studies performed by Toar et al. [13] and Kunwar et al. [15], the results of antibiotic sensitivity testing for their isolates were not reported.
Solomon et al. [14] found that Acinetobacter were resistant to gentamicin, trimethoprim-sulfamethoxazole, and ciprofloxacin; whereas, in our study, we found that Acinetobacter were resistant to imipenem, meropenem, and tetracycline. Our finding of multidrug resistance pattern for Acinetobacter was different from Solomon et al. In another study conducted by Shamsizadeh et al. [16], Acinetobacter resistant to ceftazidime, imipenem, and gentamicin were isolated from the intensive care units.
Outdoor Air Isolates
We isolated Pseudomonas, Staphylococcus aureus, and coagulase-negative Staphylococcus, from outdoor air samples which were similar to the findings from studies as discussed below. In one study [17], the dominant species isolated from a school in Nigeria were Escherichia coli, Micrococcus spp., Klebsiella spp., Pseudomonas spp., and Staphylococcus spp. In another study [18] indoor and outdoor air samples in a school in India were tested and Micrococcus, Staphylococcus, Streptococcus, Bacillus, Legionella, Pseudomonas, Klebsiella, and Mycobacteria were isolated from both samples. They observed differences between locational indoor concentrations of the microorganisms depending on which areas were more frequently visited and showed environmental outdoor microorganisms can spread indoors.
Li et al. [19] performed a global survey of antibiotic-resistance genes from urban air and found that there were 30 antibiotic-resistance gene subtypes resistant to the following classes of antibiotics: beta-lactam, quinolones, tetracyclines, macrolides, aminoglycosides, sulphonamides, and vancomycin. Cities that were included in the study were Haikou, Hong Kong, Guangzhou, Shanghai, Beijing in China, Bandung in Indonesia, San Francisco in the USA, Melbourne and Brisbane in Australia, Singapore, Paris and Tours in France, amongst others. This study highlighted the notion that urban air across the globe can contain antibiotic-resistant microorganisms.
In this study, various species of Staphylococcus and Bacillus with different antimicrobial resistance profiles were found from both outdoor and hospital air samples during sandstorms. Comparing the resistance patterns of the isolates obtained from outdoor air samples with hospital indoor air samples, shows remarkably more Staphylococcus isolates obtained from atmospheric outdoor air samples were resistant to oxacillin (95% outdoor vs 12% hospital). Resistance to trimethoprim and erythromycin amongst outdoor and hospital Staphylococcus isolates were: 65% outdoor vs 73% hospital and 60% outdoor and 50% hospital, respectively. In terms of multiple drug resistance patterns, 75% of the outdoor isolates versus 42% of hospital isolates were resistant to at least three different classes of antibiotics. However, outdoor isolates did not exhibit resistance to linezolid and vancomycin, whilst one isolate collected from hospital air, was resistant to vancomycin and two isolates were resistant to linezolid. This could translate to a higher occurrence of methicillin-resistant Staphylococcus spp. and multidrug-resistant strains in atmospheric outdoor air, nevertheless, the findings support the ubiquity of Staphylococcus spp. both in outdoor air and in hospital premises.
In contrast to the results of our study, Tamberkar et al., 2007 [20], showed that Staphylococcus were isolated more from the outdoor air samples than from indoor samples. The authors attributed this to shedders as being the sources of the high burden of Staphylococcus, which disperse large numbers of Gram-positive cocci into the environment. In the same study, they were also able to isolate Pseudomonas aeruginosa, which had a higher concentration in the indoor air than outdoor air. In our present study, we were only able to isolate Pseudomonas spp. from hospital air samples.
Oxacillin resistance was detected in Bacillus isolates from both outdoor (83%) and hospital (63%) air isolates. There were also higher rates of resistance amongst outdoor air isolates against mupirocin (58% outdoor vs 25% hospital), trimethoprim (58% outdoor vs 38% hospital), and erythromycin (50% outdoor vs 38% hospital). Of the outdoor isolates, 75% showed resistance to more than three antibiotic classes, whilst amongst the hospital isolates, only 38% showed multiple drug resistance. Moreover, three of the outdoor isolates exhibiting multiple drug resistance patterns also were resistant to one or two of the following antibiotics: imipenem, linezolid, and vancomycin. Such findings support the notion of environmental Bacillus spp. (usually in soil) as a source of hospital-acquired infection [21] that would be harder to treat with available antibiotics.
From indoor air samples we identified Staphylococcus Species, Bacillus, Acinetobacter, and micrococcus. Outdoor air samples contained Bacillus, Pseudomonas, and Staphylococcus. In comparison, Bacillus and Staphylococcus were found from both outdoor and hospital air samples. Acinetobacter, Micrococcus, and Bacillus were not found in outdoor samples and indicated the possibility of contamination from outdoor environmental sources.
There was no isolated Acinetobacter from outdoor air samples. Acinetobacter survives best in water and soil, whereas our research was focused on collection of air samples. Acinetobacter can be found on human skin and can survive for long under unconducive settings, thus attributing possible contamination of indoor environment [16].
There are some limitations to our study, the sample collection method included both targeted and non-targeted bacteria. Different growth conditions and rates could affect the distribution of the bacteria in the samples. Overgrowing bacteria could inhibit the growth of the slow-growing bacteria through competition for resources and thus affect the results. The study only used data from two hospitals and two outdoor target sites, making statistical relationships for all hospitals in Kuwait difficult, moreover this is the first study in Kuwait to sample air during sand storms and therefore lack of prior research data limited the scope of the study analysis.
In conclusion, antibiotic-resistance is a public health concern that greatly affects the progression and management of infective diseases. In this study, we have determined the types and the distribution of antibiotics-resistant bacteria present in the Kuwaiti air samples and compared the results with the bacteria present in the clinical settings. Dust rising from sandstorms contribute to the species of bacteria seen in clinical settings in Kuwait. Moreover, some bacteria tend to be able to survive for longer periods and thrive in the clinical settings, such as Acinetobacter that has the capability of remaining for prolonged periods in the environment. The exact nature and the extend of how environment plays its contributory role in propagation of antimicrobial resistance is still not clear. More attention should be paid to the environment as a critical contributing factor to link the ecological influences to the propagation of resistant bacteria in air.
*1 Coagulase-negative Staphylococcus include S. saprophyticus, S. epidermidis, S. hominis