Abstract
Background
Disinfection has a fundamental role in the control of pathogens in the hospital environment. This study was designed to assess the efficacy and functional impact of disinfectants in reducing pathogens related to healthcare associated infections (HAIs) in hospitals.
Methods
This observation study was conducted at three university hospitals in Gorgan, Iran, from May to Oct 2023. The data including used disinfectants and microbiological examination were obtained from the infection control unit of each hospital.
Results
The results showed that a variety of disinfectants from intermediate to high levels were employed in accordance with the World Health Organization (WHO) protocols. The microbial result revealed that 31.6% (286 out of 906) of the sample had at least one microorganism. Among identified organisms, Bacillus spp. were the predominant species followed by Staphylococcus epidermis, fungus genera, Enterobacter spp., Enterococcus spp., Pseudomonas spp., Escherichia coli, Alcaligenes spp., Staphylococcus aureus, Citrobacter spp., Corynebacterium spp., Klebsiella spp., Acinetobacter spp., Micrococcus spp., Staphylococcus saprophyticus, and Serratias spp. The highest prevalence rates of microorganisms were observed in the wards of ICU, emergency, internal medicine, and women’s ward. The chi-square test revealed a significant relationship between the presence of organisms and hospital wards (P < 0.05).
Conclusion
The presence of pathogens indicates a defect in the disinfection process, probably due to both little attention to disinfection protocols and multidrug resistance. It is not yet possible to eliminate pathogens from the hospital environment, but it can be minimized by education intervention, standardizing disinfecting processes, and monitoring by the infection control committee.
Keywords: Disinfection, Drug Resistance, Environmental health, Infectious disease transmission, Hospital infection
Introduction
The hospitals’ environments are known as the main source spread of pathogens related to Hospital-acquired infections or healthcare associated infections (HAIs) [1, 2]. The term HAIs refers to infections that people get while receiving medical care, or soon after receiving health care, or three days of discharge, or 30 days after receiving medical attention [3, 4]. Today, HAIs are one of the most important challenges of the health system regarding significantly increased morbidity and mortality rates, rising healthcare expenses, and patient safety [5, 6]. It is estimated that over 2.5 million cases of HAIs still occur per year in European countries, where comprehensive healthcare services are suitable [7]. The estimated rate of HAIs is about 25% in low and middle-income countries and 5 to 15% in high-income countries [8]. According to a report by the national nosocomial infections surveillance system, the incidence rate of HAIs is 1.3–10% in Iran [9]. Consequently, a public health intervention and urgent action is required to reduce HAIs morbidity and mortality rates due to antimicrobial resistance [10].
In recent years, there has been more attention to HAIs due to the importance of adhering to health protocols in the reduction of morbidity and mortality rates, and financial burden on individuals and healthcare systems [11]. This increased attention is associated with the rising trend of antibiotic resistance microorganisms, e.g. vancomycin-resistant enterococcus (VRE), methicillin-resistant Staphylococcus aureus (MRSA), and Clostridioides in healthcare environments [12]. It is important to indicate that some of these pathogens can survive between several hours to days and sometimes to months depending on the type of microorganism and the quality of health service in healthcare institutions [2, 13]. The nosocomial infection risk is higher when disinfection of a ward is not correctly done after the discharge of a patient, and a new patient is admitted to the same ward with similar illnesses [4].
Nowadays, the management of infectious diseases requires an integrated and multifaceted approach to tackle the resistance of the pathogen to drugs, and cleaning and disinfection are some of the most important to reduce HAIs in hospital environments [14, 15]. The Coronavirus disease pandemic management experience showed that cleaning and disinfecting contaminated environments helps prevent the spread of COVID-19 [16]. In the hospital environment, there are many spaces and equipment used for diagnosing, treating, and caring for patients [17], but the highest risk places for contamination are those located nearest to the patients [13]. Healthcare personnel, patients, and visitors inadvertently transfer pathogens by touching contaminated surfaces. This contributes significantly to the transmission of HAIs [18]. Research indicates that 60–80% of pneumonia, bloodstream, and urinary tract infections associated with HAIs may be linked to the use of medical devices [19]. Therefore, the cleaning and disinfection of hospital environments can reduce the risk associated with nosocomial infection [20, 21]. All activities performed with water and detergents to remove foreign material such as soil, dust, fat, oil microorganisms, etc. from contaminated surfaces are called cleaning. Cleaning is an effective process to achieve acceptable disinfection efficiency. The term disinfection refers to a process that can eliminate pathogenic microorganisms, however, spore-forming more resistant microorganisms will probably not be destroyed [22]. This study was focused on the evaluation of disinfectant efficacy against pathogens related to HAIs in hospital environments.
Methods
An observational study was conducted at three university hospitals in Gorgan, Iran, from May 1 to October 31, 2023. Samples were collected from various locations within these hospitals, including the coronary care unit (CCU), intensive care unit (ICU), emergency department, internal medicine, burn unit, urology, dialysis, women’s ward, men’s ward, neurology and neurosurgery, hematology and oncology, operating room, psychiatry, infectious disease, endoscopy, pediatrics, neonatal intensive care unit (NICU), laboratory, radiology, and kitchen. The sampling procedure from wound included swabs taken from areas of the floor, wall, surface metals, patient bed, trolley, thermometer, blood pressure monitors, and electronic equipment. The samples were placed in an insulated cooler (T ≤ 5 °C) and transferred to the reference laboratory for isolation and identification of microbes.
To distinguish microorganisms, references like the practical handbook of microbiology 4th edition [23] and jawetz melnick & adelbergs medical microbiology 26/E [24] were employed using several biochemical tests, including gram-staining, oxidase production and catalase tests, glucose and lactose fermentation, hydrogen sulfide production, indole production, methyl red, voges-proskauer, citrate utilization, motility, urea hydrolysis, ONPG hydrolysis, ornithine and lysine decarboxylase, arginine dihydrolase, gelatin hydrolysis, schaeffer-fulton staining. All phenotypical tests were conducted using products from leading manufacturers in the field, namely bioMérieux (Marcy-l’Étoile, France) and HiMedia (Mumbai, India), ensuring accurate and reliable results according to Standard Methods. Quality control and quality assessment were cautiously performed according to the standard method at all stages of the study regarding sampling, preservation, and examination.
The used disinfectants were obtained from the control infection unit in each hospital. The data were collected by documents existence and interviews with physicians, nurses, and cleaning workers about all disinfectants used in the different departments of the hospital. Disinfectants were then categorized into three levels: high, intermediate, and low based on the spectrum of efficacy against types of microorganisms including bacteria, viruses, fungi, and protozoa. At the next stage, we determine each disinfectants were used in which wards or departments, and on which surfaces (e.g. high-touch and low-touch) as well as used medical equipment such as critical items, semi-critical items, and non-critical items. Statistical processing of data was done by using the SPSS version 22 (IBM, USA). The Chi-square test was applied to assess the presence of microorganisms in different wards of the hospital. A P-value of < 0.05 was considered significant.
Results
The result showed that all disinfectants used in the investigated hospitals have been approved by Iran’s Health Ministry as recommended by the WHO protocols. All disinfectants were from groups of intermediate and high levels, the characteristics of disinfectants are shown in Table 1. The percent of isolated organisms in different wards of sampling in the university hospital of Gorgan, Iran are present in Table 2. The study results showed that 31.6% of samples were positive for pathogens. Bacillus spp. (10.71%) were the predominant genera, followed by Staphylococcus epidermidis (9.3%), fungal genera (6.6%), Enterobacter spp. (3.5%), Enterococci spp. (2.5%), Pseudomonas spp. (2.4%), Escherichia coli (1.9%), Alcaligenes spp. (1.3%), Staphylococcus aureus (1.1%), Citrobacter spp. (1%), Corynebacterium spp. (0.9%), Klebsiella spp. (0.6%), Acinetobacter spp. (0.4%), Micrococcus spp. (0.3%), Staphylococcus saprophyticus (0.3%), and Serratia spp. (0.2%). Based on our findings, the highest rate of microbial contamination between all departments was found in the wards of ICU, emergency, and internal. The chi-square test demonstrated a remarkable relationship between hospital wards and the presence of pathogenic microorganisms (P < 0.05). Figure 1 shows isolated microorganisms in an investigated hospital. The results also demonstrated that out of 36.4% of positive samples, contamination with microorganisms was observed in 15.2%,6.1%, 4.2%, 3.3%, 1.9%, and 0.9% of samples taken from unsterile medical instruments, sterile medical instruments, office instrument, trolley, bed and floor and wall, respectively. Statistical analysis showed there were significant correlations between different surfaces of sampling and the presence of Bacillus spp. (P< 0.001), Staphylococcus epidermidis (P< 0.001), fungal genera (P=0.018), and Alcaligenes spp. (P=0.006). In contrast, no statistically significant relationships between the occurrence and distribution of Enterobacter spp., Enterococci spp., Pseudomonas spp., Escherichia coli, Staphylococcus aureus, Citrobacter spp., Corynebacterium spp., Klebsiella spp., Acinetobacter spp., Micrococcus spp., Staphylococcus saprophyticus, and Serratia spp. and surface of sampling. Table 3 represent the percent of isolated organisms in different surfaces of sampling in university hospital of Gorgan, Iran.
Table 1.
Cleaner and disinfectants used in the three university hospitals of Gorgan, North of Iran
| Disinfectant name | Ingredients | Disinfected place | Hospital |
|---|---|---|---|
| Deconex 54 sporicide | Glutaraldehyde | Operation room, Anesthesia equipment, Respiratory equipment, Endoscopy and colonoscopy devices | A, C |
| Stril C | Hydrogen peroxide | Endoscopy and colonoscopy devices | A |
| VentiSept F | Didecyldimethylammonium chloride, Benzalkonium chloride, Ethylene diamine tetraacetic acid | Operation room (Floor, Wall, Surface metals, patient bed) | B, C |
| VentiSept M Plus | Didecyldimethylammonium chloride, Benzalkonium chloride, Benzotriazole | Anesthesia Equipment, Respiratory equipment, Operation room (Floor, Wall, Surface metals, patient bed), trolley, Thermometer, Blood pressure monitor, Electronic equipment | B, C |
| VentiSept Liquid AF | Etanol 70 , Didecyl dimethyl ammonium chloride, cocamide diethanolamine | Anesthesia equipment, Respiratory equipment, Operation room (Floor, Wall, Surface metals, patient bed), trolley, Thermometer, Blood pressure monitor, Electronic equipment | C |
| Micro ZCS | Didecyldimethylammonium chloride, | Anesthesia Equipment, Respiratory equipment, Anesthesia equipment, Respiratory equipment, Operation room (Floor, Wall, Surface metals, patien bed), trolley, thermometer, Blood pressure monitors, electronic equipment | C |
| RioSept F-D Universal | Alkyl Dimethyl Ethyl Benzyl Ammonium, Benzalkonium chloride, | Anesthesia equipment, Respiratory equipment, Anesthesia equipment, Respiratory equipment, Operation room (Floor, Wall, Surface metals, patient bed), trolley, thermometer, Blood pressure monitors, Electronic equipment | C |
| Saya Sept HI | Didecyldimethylammonium chloride, Hexamethylene Biguanide Hydrochloride | Anesthesia equipment, Respiratory equipment, Operation room (Floor, Wall, Surface metals, patient bed), Trolley, Thermometer, Blood pressure monitor, Electronic equipment | C |
| Saya Sept HP | Didecyldimethylammonium chloride, Alkyl Dimethyl Ethyl Benzyl Ammonium, Hexamethylene Biguanide Hydrochloride | Operation room (Floor, Wall, Surface metals, patient bed), Trolley, Thermometer, Blood pressure monitor, Electronic equipment | C |
| Septisurface | DimethylEthylBenzylAmmonium chloride, Etanol 70, Chlorhexidine Gluconate | Anesthesia equipment, Respiratory equipment, | C |
| Sodium hypochlorite | NaOCl | Kichen | A, B,C |
| Salt ink | (HCL) | Toilet | A, B,C |
Table 2.
Percent of isolated organisms in different ward of University Hospital of Gorgan, Iran
| Wards | Bacillus spp. | s. epidermis | Fungus | Enterobacter spp | Enterococcus spp. | Pseudomonas spp. | Escherichia coli | Alcaligenes spp. | S.aureus | Citrobacter spp. | Corynebacterium spp. | Klebsiella spp. | Acinetobacter spp. | Micrococcus spp. | S. saprophyticus | Serratias spp. |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| CCU | 0.8 | 1.1 | 0.2 | 0.2 | 0 | 0.2 | 0 | 0.3 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Emergency | 2 | 1.7 | 0.8 | 0.7 | 0.4 | 0.1 | 0.3 | 0.1 | 0.1 | 0.1 | 0.1 | 0 | 0 | 0.1 | 0.1 | 0 |
| Internal | 1.7 | 0.9 | 0.6 | 0.1 | 0.2 | 0.4 | 0 | 0.2 | 0.1 | 0.3 | 0 | 0 | 0 | 0 | 0 | 0 |
| Laboratory | 0.4 | 0.1 | 0.1 | 0 | 0.1 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| ICU | 1.2 | 1.5 | 1.3 | 0.3 | 0.2 | 0.2 | 0.4 | 0 | 0.3 | 0.3 | 0 | 0.1 | 0.3 | 0 | 0.2 | 0 |
| Dialysis | 0.6 | 0 | 0 | 0 | 0 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0.1 | 0 | 0 |
| NICU | 0.7 | 0.4 | 0.1 | 0.7 | 0 | 0.3 | 0.4 | 0.2 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 |
| Womens | 1 | 1.5 | 0.3 | 0.4 | 0.2 | 0.1 | 0.1 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Neurology&Neurosurgery | 0.4 | 0.3 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Hematology & Oncology | 0.6 | 0.2 | 0.1 | 0.2 | 0 | 0.1 | 0.1 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Operating room | 0 | 0.3 | 0.6 | 0.4 | 0.3 | 0.4 | 0 | 0 | 0.1 | 0 | 0 | 0.3 | 0.1 | 0 | 0 | 0 |
| Men | 0.1 | 0.3 | 0.2 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Psychiatry | 0 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 |
| Kitchen | 0.4 | 0.1 | 0 | 0.1 | 0 | 0.1 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0.1 | 0 | 0 |
| Radiology | 0.3 | 0.3 | 0.4 | 0.1 | 0.2 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Infants | 0.2 | 0.1 | 0.2 | 0.1 | 0 | 0 | 0 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Infectious | 0 | 0 | 0.3 | 0 | 0.1 | 0.1 | 0.1 | 0 | 0.1 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 |
| Endoscopic | 0 | 0.2 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0 |
| Burn | 0 | 0 | 0.9 | 0 | 0.6 | 0.1 | 0 | 0 | 0 | 0 | 0.2 | 0.1 | 0 | 0 | 0 | 0 |
| Urology | 0 | 0 | 0.1 | 0 | 0 | 0 | 0 | 0 | 0 | 0 | 0.2 | 0 | 0 | 0 | 0 | 0.2 |
| total | 10.4 | 9.3 | 6.6 | 3.5 | 2.5 | 2.4 | 1.9 | 1.3 | 1.1 | 0.9 | 0.9 | 0.6 | 0.4 | 0.3 | 0.3 | 0.2 |
| p-value | < 0.001 | 0.021 | 0.027 | 0.654 | 0.023 | 0.907 | 0.068 | 0.526 | 0.23 | 0.743 | < 0.001 | 0.234 | 0.702 | 0.008 | 0.957 | < 0.001 |
Fig. 1.
The isolated microorganisms in different wards of Gorgan (Iran) university hospitals
Table 3.
Percent of isolated organisms in different surfaces of University Hospital of Gorgan, Iran
| surface sampling | Bacillus spp. | s. epidermis | Fungus | Enterobacter spp | Enterococcus spp. | Pseudomonas spp. | Escherichia coli | Alcaligenes spp. | S.aureus | Citrobacter spp. | Corynebacterium spp. | Klebsiella spp. | Acinetobacter spp. | Micrococcus spp. | S. saprophyticus | Serratias spp. |
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Bed | 0.5 | 0.5 | 0.9 | 0.2 | 0.5 | 0.1 | 0.1 | 0.1 | 0.0 | 0.0 | 0.2 | 0.0 | 0.0 | 0.0 | 0.1 | 0.1 |
| Trolley | 0.9 | 1.5 | 0.9 | 0.2 | 0.2 | 0.1 | 0.2 | 0.0 | 0.0 | 0.1 | 0.1 | 0.1 | 0.0 | 0.0 | 0.1 | 0.0 |
| Steril Medical insterument1 | 1.4 | 1.4 | 1.5 | 0.9 | 0.9 | 0.8 | 0.1 | 0.1 | 0.5 | 0.3 | 0.2 | 0.3 | 0.2 | 0.0 | 0.0 | 0.0 |
| Unsteril Medical insterument2 | 5.6 | 4.0 | 2.6 | 1.7 | 0.7 | 1.1 | 0.9 | 0.8 | 0.6 | 0.3 | 0.3 | 0.1 | 0.2 | 0.3 | 0.1 | 0.1 |
| Office instrument3 | 1.5 | 1.9 | 0.8 | 0.6 | 0.3 | 0.2 | 0.2 | 0.1 | 0.1 | 0.2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 |
| Floor and Wall | 0.3 | 0.0 | 0.1 | 0.0 | 0.0 | 0.1 | 0.1 | 0.2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 |
| p.value | < 0.001 | < 0.001 | 0.018 | 0.383 | 0.082 | 0.819 | 0.285 | 0.006 | 0.758 | 0.815 | 0.148 | 0.799 | 0.893 | 0.379 | 0.179 | 0.077 |
1Steril Medical insterument; laryngoscope blade, operating room pack, anaesthesia equipment, cutting instruments, and incubator
2Unsteril Medical insterument; baby scale, stethoscope, dialysis machine, oxygen manometer, electrocardiogram pedal, and medication refrigerator
3Office instrument; computer monitor, computer mouse, staff desk, medical record, pen and marker, whiteboard, and workstations
Discussion
It is well known that environmental hospitals have a direct and indirect role in the spread of pathogens of HAIs, particularly multidrug-resistant microorganisms which pose health risks for both patients and physicians, nurses, and other staff [25]. Cleaning and disinfecting is one the best approaches in the inhibition of pathogens and follows the prevention and control of HAIs in the healthcare setting. Our results showed that all hospitals had strategies of good for infection control. Based on our findings, only high-level and intermediate-level disinfectants were used in the inpatient and outpatient as well as administrative departments. The microbial analysis showed that pathogenic microorganisms were observed in 31.6% (286 from 906) of samples. Furlan et al. have previously reported that 407 bacteria were identified from the 528 samples analyzed in Saudi hospitals [26]. The presence of photogenic microorganisms is a sign of defect in infection control programs, especially concerning the growth and proliferation of pathogens, which may be related to cleaning and disinfection processes [27, 28]. The results demonstrated that microorganisms were detected in sterile and unsterile medical instruments (Table 3). All surgical instruments must be sterile for patient safety due to the transmission of infectious disease in hospitals particularly in the ICU, CCU, and NICU for patients with impaired immune response [29]. In contrast to our research, Lena al. reported that microorganism were not identified from surgical instruments sampled in the operation room. However, a high level of microbial contamination was isolated from outer surface of stored sterile packs, possibly due to air contamination of the hospital environment, particularly within the operation room [30].
Our study revealed that the environmental worker service did not perform the disinfection process (e.g. prepared disinfection solution and exposure time) according to the manufacturer’s recommendation. Similarly, Doll et al. study has shown the presence of pathogens in a hospital environment more occurred when the cleaning procedure was not sufficient [31]. In another study, Yean et al.‘s reported that accurate implementation of the disinfectant was one of the most important factors in controlling coronavirus [32]. It seems that providing practical guidelines for cleaning workers can lead to considerable effects on the decrease of pathogens in hospital environments. The result of a study in Japan revealed that 16.8% (51 of 303) of the emergency departments of hospitals had no instruction for the prevention and control of infections [33]. Due to such risks to patients, visitors, and staff, it is suggested that disinfection should be performed with effective methods for decontaminating and precisely monitored by the head of an infection control unit in each hospital. The WHO guidelines indicate that any failure in the infection control program leads to the growth of pathogens and the risk of illness associated with hospital environments [34].
As shown in Fig. 1, out of 20 contaminated wards, ICU, emergency, internal medicine, women’s ward, coronary care unit (CCU), and neonatal intensive care unit (NICU) had the highest rate of microbial contamination. This may be because overcrowding in healthcare institutions [35] and specialized and additional care can affect the incidence rate of pathogens in hospital environments [36]. As mentioned above, Bacillus spp. was the most frequently identified among all isolated microorganisms, following a study reported by Bakri [26]. The Bacillus spp. can cause nosocomial bloodstream infection in patients with lowered immunity and malignancies [37]. Fujita and Nishiura have documented an elevated risk of nosocomial bloodstream infection among hospitalized patients [37]. Mohamed et al. have previously reported that Bacillus cereus was the most commonly isolated organism in the Elkhomes hospital, Libya [38]. A high level of Bacillus spp. may be related to environmental conditions, biofilm information, disinfectants used, resistance to disinfectants, and the procedure of cleaning and disinfecting in a hospital environment [39]. Based on our result (Table 3), the higher rate of Bacillus spp. was isolated from unsterile medical instrument. The presence of Bacillus spp. on the surface of an oxygen manometer, electrocardiogram pedal, stethoscope, dialysis machine, and medication refrigerator can be dangerous to patients and hospital staff. In a research conducted by Hosni et al., they reported that Baillus spores could survive within a biofilm until 6 days after chemical disinfection [40]. Due to the risks of Bacillus spp. and other resistant bacterial spores, it is proposed that hospital wards particularly sensitive environments rigidly cleaned and disinfect to ensure there isnot any concern for patients and medical personel.
The highest rate of S. epidermidis was isolated in 9.3% of samples, and the highest was found in the wards of emergency, ICU, and women’s, respectively. There is a prevalence rate between 27.8 and 58.8% of samples for S. epidermidis in Iran [41]. Most importantly, methicillin-resistant Staphylococcus epidermidis (MRSE) provides more insight for S. epidermidis in the hospital environment [42]. So, an intervention program is required to safe the environmental surfaces from all pathogens, similar to the study Furlan et al. [43]. In the present study, fungal were identified in 6.6% of samples, and the highest rate of contamination was detected in the wards of emergency, ICU, internal, and burn. It is important to indicate that fungal pathogens are known as cross-infection through healthcare workers to their patients [44]. The Chi-square test showed a statistically significant relationship between the presence of Bacillus spp., S. epidermidis and fungal and different hospital wards (Table 2).
In this study, Enterobacter spp., and Enterococcus spp., were found in 3.5% and 2.5% of samples, respectively. Enterococcus spp. is mostly important due to being highly resistant to broad-spectrum antibiotics [45]. Zrinka Todorić et al. reported that 38.0% (165/432) of patients were contaminated with Enterococci spp. in the ICU [46]. The result of a retrospective study also showed an incidence rate 4/10,000 of Enterococcus for patients of blood infections [47]. P. aeruginosa was isolated in samples taken from internal medicine, NICU, CCU, ICU, emergency, womens ward, hematology and oncology, operating room, kitchen, radiology, infection, and burn. A report from Sharifi et al. study showed a high rate (40.4%) of P. aerugino in hospitalized patients in southeast of Iran, which isolates obtained from burn exudates, urinary tract infection isolates and blood samples were 68%, (37.5%) and (17.4%), respectively [48]. Presence of Pseudomonas spp. as an opportunistic bacterium is dangerous for people with lowered immunity [49]. The importance of Pseudomonas spp. is related to colonizing and proliferating in relatively nutrient-poor conditions at a wide range of temperatures in hospital environments [2].
In the present study, Escherichia coli, Staphylococcus aureus and Klebsiella spp., were identified in different wards of investigated hospitals. Our findings showed that Staphylococcus aureus was found in the wards of ICU, infant, emergency, internal, neurology and neroserjury, operating room, and infection. In Weiner-Lastinger et al. study, Escherichia coli was the predominant genera followed by Staphylococcus aureus and Klebsiella spp. [50]. Sula et al. reported Escherichia coli is a remarkable organism in hospital environments due to resistance to co-trimoxazole and ampicillin [51]. The result of Petros Ioannou et al., study demonstrated that Staphylococcus aureus is a severe infection affecting morbidity and mortality [52]. Xiaohui Chi et al. reported that one of the major causes of HAIs in ICUs is carbapenem-resistant Klebsiella [53].
The highest prevalence of citrobacter spp was observed in internal, ICU, NICU, and emergency. In Thompson’s study, P. aeruginosa and Citrobacter spp. were isolated in 41% and 21% of sample [52]. Our finding demonstrated that Corenibacterium spp., isolated from psychiatry, Burn, Urology, infection, and emergency. In the study of Thompson et al., Citrobacter sp., S. epidermidis, and Corynebacterium spp. were detected from surfaces after post-disinfected [52]. The Alcaligenes spp. were detected in NICU, CCU, internal, women, emergency, hematology and oncology, and kitchen. In a study conducted by Adibi et al. in Iran, 52.8% of samples (19 samples from 36) were positive with respect to Alcaligenes spp. [54]. Acinetobacter spp. were isolated from ICU and operating room. Many researchers that environmental cleaning is very important for controlling of MDR Acinetobacter spp. in CCU [2].
The results of interviews showed that many of the hospital staff were worried about risks caused by exposure to disinfectants. It is a fact that respiratory effects e.g. asthma reported in Clausen et al. study as a result of exposure to spray cleaning and disinfection products [55]. In other words, disinfectant substances are effective in reducing pathogen loads, but they might be toxic for humans, especially concerning cytotoxicity, mutagenicity, and carcinogenicity [56]. It is recommended to increase the knowledge make hospital workers about the role of accurate cleaning and disinfection in reducing HAIs through educational intervention. It does require high attention to training, regular monitoring, and education for all hospital staff, particularly nurses and cleaners. Training hospital cleaners regarding the use of disinfectants is known as one of the effective approaches to control hospital infections. Our findings also showed that training courses for workers, paramedics, and nurses were conducted by environmental health experts according to the hospital’s accreditation program. Oliveira et al. reported a high function properly of staff responsible for the cleaning and disinfection of the emergency room after educative action [57]. The results of interviews with hospital personnel also showed that their level of awareness was acceptable, but their performance in the process of controlling hospital infections was not optimal, which was probably due to the lack of sufficient human resources, the large number of patients, and the high workload. Our results were in line with Meyer et al. study that indicates the role of training for hospital staff to improve the quality of the hospital environment and equipment used for the treatment of patients. Attention to training indicated by Meyer et al. [58] and Teker et al. [59] for achieving of acceptable limit of disinfection in the hospital.
Limitation of study
This microbial result was obtained from available data in hospital laboratories based on a current schedule. Therefore, the lack of a standardized sampling program according to the infection prevention and control approach was an important limitation of this study. For this reason, the comparison of microbial results in different wards at the investigated hospital may lead to incorrect and incomplete conclusions. On the contrary, the result of this study provided a current working situation in university hospitals concerning the disinfection process and the growth and proliferation of pathogens. i.e., these results can be useful to anticipate pathogens causing HAIs and the risks that threaten patients and staff in healthcare settings.
Conclusion
The presence of pathogens indicates a defect in the disinfection process, probably due to both little attention to disinfection protocols and resistance to multidrugs. It is not yet possible to eliminate pathogens from the hospital environment, but it can be minimized by education intervention, choice of appropriate disinfectant, standardizing disinfecting processes, and monitoring by the infection control committee.
Acknowledgements
The authors wish to thank all healthcare professionals and service workers at three investigated hospitals of Gorgan, who helped with this work.
Abbreviations
- HAIs
Healthcare associated infection
- WHO
World Health Organization
- VRE
Vancomycin-Resistant Enterococci
- MRSA
Methicillin-Resistant Staphylococcus Aureus
- ICU
Intensive Care Unit
- CCU
Coronary Care Unit
- NICU
Neonatal Intensive Care Unit
Author contributions
A.S.; project administration, supervision, investigation, original draft preparation, writing, review and editing. S.G.; funding acquisition, investigation, original draft preparation, writing, review and editing. F.F.; investigation, data gathering, original draft preparation. A.R.; data curation, analysis and interpretation of data. All authors have read and agreed to the published version of the manuscript.
Funding
This study was supported by Golestan University of Medical Science, Gorgan, Iran, as a thesis of general Practitioner (Cod number: 113594). The funder had no role in the study design, data collection, analyses, and interpretation of the results.
Data availability
The datasets generated during and /or analysed during the current study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
The present study and all research protocols were approved by the Professional Ethics Committee of the Golestan University of Medical Sciences with the ethical code of IR.GOUMS.REC.1402.215, which was performed in accordance with the current and seventh edition of the Declaration of Helsinki. The informed consent was also obtained verbally from all hospitals for the implementation of this project. All the results were later informed to the hospitals professionals so that they could evaluate their practice.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Fateme Fashayi, Email: fateme.fashayi@gmail.com.
Ali Shahryar, Email: dr.shahryari@goums.ac.ir.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated during and /or analysed during the current study are available from the corresponding author on reasonable request.

