Bacteria in Healthcare Units: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Camila Xu and Version 1 by Ana Monteiro.

Healthcare units consist of numerous people circulating daily, such as workers, patients, and companions, and these people are vehicles for the transmission of microorganisms, such as bacteria. Bacteria species may have different allergenic, pathogenic, infectious, or toxic properties that can affect humans.

  • exposure
  • health effects
  • healthcare-associated infections

1. Introduction

Infections associated with healthcare units are a major public health problem that concerns patients, the public, and politicians, since they impact society’s development [1]. These infections lead to significant mortality and financial losses for health systems each year. Therefore, the rate of infection associated with healthcare units is not only an indicator of patient safety but also of the global healthcare quality provided in hospitals [2,3,4][2][3][4]. According to the World Health Organization (WHO), for every 100 hospitalized patients at any given time, 7 in developed countries and 10 in developing countries will acquire at least one healthcare-associated infection [2]. Another survey indicated that 1 in 17 hospitalized patients who received healthcare-associated infections (while being treated for other health issues) died as a result [5].
Healthcare units such as hospitals, maternity centers, blood banks, clinics, medical offices, urgent care centers, or healthcare centers consist of countless people circulating daily, such as workers, patients and their companions, the healthy and the sick. These people are vehicles for transmitting microorganisms, such as bacteria, that can cause infections that are transmitted very easily in this setting due to its population of sick or immunocompromised people [6].
Additionally, bacterial contamination in hospitals is heavily affected by the following important factors: construction characteristics, levels of water and nutrients in the interior environment necessary for the growth and survival of bacteria, people that occupy the space, and the outdoor environment [7]. Medical activities, cleaning procedures and their frequency are crucial factors for the increase in bacterial load [8,9][8][9].
Bacterial species have different allergenic, pathogenic, infectious, or toxic properties that can affect humans [10]. Allergenic bacteria, mainly thermophilic bacteria, may generate a hypersensitivity response (hypersensitivity pneumonitis) in the host [10]. A pathogenic bacterium causes disease in a host and is determined by virulence factors, enabling the replication and dissemination of bacteria in the host organism [11,12][11][12]. Bacteria infect a host, usually from another host/reservoir, through direct contact, airborne transmission, a vector, or a common vehicle [10]. In addition, bacteria can produce toxins, which trigger a harmful process in the host organism, inhibiting protein synthesis, activating immune responses, and damaging cell membranes [13]. Bacterial cell wall constituents, such as endotoxins and peptidoglycans, are referred to as agents with pro-inflammatory properties causative of respiratory symptoms (asthma, bronchitis and byssinosis) [10].
The transmission of bacteria can be promoted because healthcare workers interact physically with different patients, unaware that they are transmitting potentially pathogenic agents. Additionally, the handling/contact with contaminated instruments or surfaces [14,15][14][15] can cause a risk of infection in both workers [16] and patients. In fact, the isolation of microorganisms from the surfaces suggests that some patients acquire bacterial infections in the hospital [17,18,19,20][17][18][19][20].
Hospital-acquired (nosocomial) infections are a concern in terms of patient safety, as they may have a high impact on patient morbidity and mortality [21,22][21][22].
Commonly, most bacteria do not cause adverse health effects and can even benefit useveryone and the environment. The problem arises when the concentration of certain potentially pathogenic bacteria is higher than the infective dose, which varies dramatically across pathogen species [23]. The scale of the severity of the effects on human health depends on many factors such as toxicity, exposure time and microbial load, and even one’s age and nutritional status [24]. For example, bacteria such as Acinetobacter baumannii, Pseudomonas aeruginosa and Stenotrophomonas maltophiliam, which are non-fermenting Gram-negative bacilli, can cause infections and severe health problems. These bacteria have been recognized as multidrug-resistant (MDR) and are associated with higher rates of mortality, increased service costs, and a poorer clinical outcome [25,26,27,28][25][26][27][28]. Additionally, Burkholderia cepacia complex (Bcc), which are a non-fermenting Gram-negative bacillus, consist of 20 species that are similar in phenotype and genetically different [29]. During the last two decades, Bcc were considered the most common bacteria in intensive care units, and recognized as a nosocomial pathogen, associated with several outbreaks in immunocompromised patients [28], such as bloodstream infections, pneumonia, urinary tract infections, septic arthritis, and peritonitis [30,31][30][31].

2. Exposure and Health Effects of Bacteria in Healthcare Units

Numerous studies presented divergent points of view on how bacterial contamination can be observed in different locations within hospital facilities, how seasonal variations affect the concentration, and even how data regarding the most prevalent genera that can be found in healthcare environments and staff due to occupational activities. In the first presented study [34][32], concentrations of airborne bacteria reached a peak in November (436.3 CFU/m3), and the lowest value was identified in December (257.1 CFU/m3). However, the authors did not explain the decrease between these two months or between the other months of the year that were assessed. Another study, conducted in Portugal [45][33], described that most of the departments analyzed presented a high level of bacterial concentration (ranging from 12 to 170 CFU/m3) and concluded that the indoor bacterial concentration was not influenced by outdoor concentration but by indoor air. In another analyzed study [37][34], winter and autumn had the highest concentration levels of bacteria with the increased bioburden associated with the waiting room in autumn and children’s ward in the winter. A possible explanation for the higher load in the waiting room can be attributed to an increase in the number of occupants (200 per day or more). The same hypothesis is suggested in the children’s ward, with the additional factor of the increased number of infections in children during the wintertime. The fact that the rooms in that ward are small, and that more than one parent can accompany the child, is another factor that increases the concentration of bacteria such as airborne actinomycetes, which were the most prevalent in the children’s ward [37][34]. The data from Portuguese studies revealed that Staphylococcus epidermidis [45][33] and Micrococcus spp. [45,46,47][33][35][36] were the most prevalent bacteria identified. However, S. epidermidis is not considered to be a relevant risk of exposure due to its lower infections rates [34][32]. On the other hand, Acinetobacter (species not identified) was found in two studies [32,34][37][32] as a prevalent genus in a university hospital from Ethiopia, justifying its persistence due to its great survival ability in the indoor environment [47][36], which can be a potential cause for hospital infections transmitted via the air [48][38]. Another relevant microorganism is Pantoea agglomerants, which is able to infect hospitalized individuals, particularly immunodeficient patients, through contaminated medical instruments [49][39]. A bacteria genus described in several studies considered of great interest is Staphylococcus spp., which was identified at the highest concentration in a cardiology ward/intensive care room (hospital 5). Once the strains were analyzed, S. saprophyticus was the most predominant, followed by S. warneri, being reported as an important opportunistic pathogen and associated with healthcare-acquired infections [37][34]. Cabo Verde et al. [45][33] also found S. warneri to be a prevalent species in the hospital, but no data were reported regarding S. saprophyticus in contrast to the findings of Sivagnanasundaram et al. [50][40]. S. saprophyticus can infect an individual’s blood through catheters, surgical prostheses, pneumonia, urinary tract infections and more [51,52,53][41][42][43]; therefore, this species is of particular relevance. Moreover, Staphylococcus aureus is one of the most relevant nosocomial pathogens, described as one of the main pathogenic bacteria that cause osteomyelitis (including in children)[54,55,56,57,58,59][44][45][46][47][48][49] septic arthritis [60[50][51][52][53],61,62,63], and prosthetic joint infections [64,65,66,67][54][55][56][57]. S. aureus is a commensal bacterium and a human pathogen; about 30% of all humans are colonized with S. aureus [68][58]. Osteoarticular infections can occur by the direct inoculation of microorganisms into tissues due to penetrating or open trauma [69][59]. In limited settings, infections complicate as many as 44% of open fractures [69][59]. Trauma-related osteoarticular infections among patients with punctures wounds seeking medical care varied from 2–60% depending on the type of the injury [70,71,72][60][61][62]. S. aureus was also prevalent in the studies by Matinyi et al. [38][63] and Thomas et al. [73][64], being detected on door handles, which could be considered a possible source of nosocomial infection [38][63]. Additionally, Staphylococcus epidermidis, as well as Micrococcus luteus and Bacillus subtilis, were common in the studies by Sivagnanasundaram et al. [50][40], Bielawska-Drózd et al. [74][65], and Bolookat et al. [39][66]. The reason for these results could be related to the presence of these bacteria in the skin, mucous membranes, hair of human beings and animals [75,76,77,78][67][68][69][70]. Considering health effects, the identification of Clostridium difficile, a Gram-positive, anaerobic, spore-forming bacillus, must be considered, as it is the principal agent of pseudomembranous colitis in humans [79][71]. In the hospital setting, C. difficile infection is the main cause of healthcare-associated diarrhea [80][72]. Symptoms arise when C. difficile spores germinate in the intestine, and the bacteria start to produce toxins, Toxin A (TcdA) and Toxin B (TcdB), causing the inflammation of the large intestine [81][73]. The clinical presentation can range from mild diarrhea to lethal toxic megacolon [81][73]. Nonetheless, the ingestion of C. difficile spores does not always lead to the development of symptomatic disease, since this bacterium can be silently present in the intestine without manifesting any symptoms, denominated as asymptomatic C. difficile colonization [82][74]. However, the patients with this condition act as a reservoir for further transmissions [83[75][76],84], and they can progress to the infection themselves, especially if they are affected by an underlying illness [85][77]. The infection is transmitted by spores that are environmentally resistant [86][78]. Another microorganism of interest is H. pylori, which is associated with occupational exposure among endoscopy personnel [87][79]. The study by Mastromarino et al. [40][80] aimed to determine if different staff groups of healthcare workers, either with or without direct patient contact, were at equal risk of acquiring H. pylori infection. The authors concluded that direct contact with patients is an important factor for becoming infected, as opposed to simply working in the endoscopy unit. Another study highlighted [87][79] that 24% (9 out of 37) of gastrointestinal endoscopy personnel, and 47% (33 out of 70) of workers in a hospital who care for disabled individuals, tested positive for H. pylori. In this case, direct contact with patients and working in a hospital where disabled individuals reside was associated with H. pylori infections, but the exposure to gastrointestinal secretions of the patients was not [87][79]. This sentudry supports the previous study’s idea that direct contact with patients is a factor to take into consideration. Among Gram-negative bacteria, the most frequently identified pathogens are Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii. E. coli was described to be prevalent in operating beds due to fecal contamination and the lack of efficiency in the cleaning process [88,89][81][82]. Pseudomonas spp., one of the most significant genera of nosocomial pathogens, was the most prevalent bacteria in all operating theatres in the Matinyi et al. study [38][63], and was identified in other studies [73,90][64][83] that referred to antiseptic solutions as a possible source of this contamination [56,57,91,92][46][47][84][85]. Other bacteria, Bacillus spp., can be related to dusty environments, the type commonly found in Uganda [38][63]. This contamination might occur in indoor areas if the windows are open for natural ventilation and could then be transferred to the operating theatres [73][64]. Furthermore, A. baumannii was associated with a vast number of infections, such as those of the bloodstream, respiratory tract, surgical sites, and urinary tract [93][86]. Transmission between patients in hospital settings is difficult to prevent because of the bacterium’s capacity to persist in the environment, particularly in intensive care units [93][86]. These Gram-negative pathogens are associated with the etiology of numerous  weand severe hospital-acquired infections in humans and have the capacity to resist antimicrobial agents, which has become an increasingly relevant problem [94][87]. Currently, antimicrobial-resistant Gram-negative bacteria are expanding worldwide and are considered a significant threat to human health [3].

References

  1. Humphreys, H.; Smyth, E.T.M. Prevalence surveys of healthcare-associated infections: What do they tell us, if anything? Clin. Microbiol. Infect. 2006, 12, 2–4.
  2. World Health Organization. Health Care-Associated Infections Fact Sheet. 2013. Available online: http://www.who.int/gpsc/country_work/gpsc_ccisc_ fact_sheet_en.pdf (accessed on 10 September 2021).
  3. National Nosocomial Infections Surveillance System. National Nosocomial Infections Surveillance (NNIS) system report, data summary from January 1992 through June 2004, issued October 2004. Am. J. Infect. Control 2004, 32, 470.
  4. Menachemi, N.; Yeager, V.A.; Welty, E.; Manzella, B. Are physician productivity and quality of care related? J. Healthc. Qual. 2015, 37, 93–101.
  5. Haque, M.; Sartelli, M.; McKimm, J.; Abu Bakar, M. Health care-associated infections—An overview. Infect. Drug Resist. 2018, 11, 2321–2333.
  6. Levy, S.B. Factors impacting on the problem of antibiotic resistance. J. Antimicrob. Chemother. 2002, 49, 25–30.
  7. National Academies of Sciences, Engineering and Medicine. Microbiomes of the Built Environment: A Research Agenda for Indoor. Microbiology, Human Health, and Buildings; The National Academies Press: Washington, DC, USA, 2017; pp. 95–131.
  8. Qudiesat, K.; Abu-Elteen, K.H.; Elkarmi, A.Z.; Hamad, M.; Abussaud, M. Assessment of airborne pathogens in healthcare settings. Afr. J. Microbiol. Res. 2009, 3, 66–76. Available online: https://www.academicjournals.org/ajmr (accessed on 10 October 2021).
  9. Marchand, G.; Duchaine, C.; Lavoie, J.; Veillette, M.; Cloutier, Y. Bacteria emitted in ambient air during bronchoscopy—A risk to health care workers? Am. J. Infect. Control 2016, 44, 1634–1638.
  10. Douwes, J.; Torne, P.; Pearce, N.; Heederik, D. Bioaerosol health effects and exposure assessment: Progress and prospects. Ann. Occup. Hyg. 2003, 47, 187–200.
  11. Cross, A.S. What is a virulence factor? Crit. Care 2008, 12, 196.
  12. Wu, H.J.; Wang, A.H.; Jennings, M.P. Discovery of virulence factors of pathogenic bacteria. Curr. Opin. Chem. Biol. 2008, 12, 93–101.
  13. Actor, J.A.J. 11—Basic Bacteriology. Elsevier’s Integrated Review; Elsevier/Saunders: Philadelphia, PA, USA, 2012; pp. 93–103.
  14. Huslage, K.; Rutala, W.; Sickbert-Bennett, E.; Weber, D. A quantitative approach to defining “high-touch” surfaces in hospitals. Infect. Control Hosp. Epidemiol. 2010, 31, 850–853.
  15. Weber, D.; Rutala, W.; Miller, M.; Huslage, K.; Sickbert-Bennett, E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: Norovirus, Clostridium difficile, and Acinetobacter species. Am. J. Infect. Control 2010, 38, S25–S33.
  16. Luksamijarulkul, P.; Aiempradit, N.; Vatanasomboon, P. Microbial Contamination on Used Surgical Masks among Hospital Personnel and Microbial Air Quality in their Working Wards: A Hospital in Bangkok. Oman Med. J. 2014, 29, 346–350.
  17. Drees, M.; Snydman, D.; Schmid, C.; Barefoot, L.; Hansjosten, K.; Vue, P.; Cronin, M.; Nasraway, S.; Golan, Y. Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci. Clin. Infect. Dis. 2008, 46, 678–685.
  18. Malamou-Ladas, H.; O’Farrell, S.; Nash, J.; Tabaqchali, S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J. Clin. Pathol. 1983, 36, 88–92.
  19. Neely, A.; Maley, M. Survival of enterococci and staphylococci on hospital fabrics and plastic. J. Clinic. Microbiol. 2000, 38, 724–726.
  20. Shaughnessy, M.; Micielli, R.; DePestel, D.; Arndt, J.; Strachan, C.; Welch, K.; Chenoweth, C. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect. Control Hosp. Epidemiol. 2011, 32, 201–206.
  21. Allegranzi, B.; Bagheri Nejad, S.; Combescure, C.; Graafmans, W.; Attar, H.; Pittet, D.L.D. Burden of endemic health-care-associated infection in developing countries: Systematic review and meta-analysis. Lancet 2011, 377, 228–241.
  22. Burke, J.P. Infection control—A problem for patient safety. N. Engl. J. Med. 2003, 348, 651–656.
  23. Goyer, N.; Lavoie, J.; Lazure, L.; Marchand, G. Bioaerosols in the Workplace: Evaluation, Control and Prevention Guide; Institut de Reserche en Santé et en Sécurité du Travail du Québec: Quebéc, QC, Canada, 2001.
  24. Huff, W.; Kubena, L.; Harvey, R.; Doerr, J. Mycotoxin interactions in poultry and swine. J. Anim. Sci. 1988, 66, 2351–2355.
  25. Dizbay, M.; Tunccan, O.; Sezer, B.; Aktas, F.; Arman, D. Nosocomial Burkholderia cepacia infections in a Turkish university hospital: A five-year surveillance. J. Infect. Dev. Ctries. 2009, 3, 273–277.
  26. Gautam, V.; Singhal, L.; Ray, P. Burkholderia cepacia complex: Beyond pseudomonas and acinetobacter. Indian J. Med. Microbiol. 2011, 29, 4–12.
  27. Gautam, V.; Patil, P.; Kumar, S.; Midha, S.; Kaur, M.; Kaur, S.; Singh, M.; Mali, S.; Shastri, J.; Arora, A.; et al. Multilocus sequence analysis reveals high genetic diversity in clinical isolates of Burkholderia cepacia complex from India. Sci. Rep. 2016, 6, 35769.
  28. Paul, L.; Hegde, A.; Pai, T.; Shetty, S.; Baliga, S.; Shenoy, S. An Outbreak of Burkholderia cepacia Bacteremia in a Neonatal Intensive Care Unit. Indian J. Pediatr. 2016, 83, 285–288.
  29. Sousa, S.; Feliciano, J.; Pita, T.; Guerreiro, S.; Leitão, J.H. Burkholderia cepacia Complex Regulation of Virulence Gene Expression: A Review. Genes 2017, 8, 43.
  30. Antony, B.; Cherian, E.; Boloor, R.S.K. A sporadic outbreak of Burkholderia cepacia complex bacteremia in pediatric inten-sive care unit of a tertiary care hospital in coastal Karnataka, South India. Indian J. Pathol. Microbiol. 2016, 59, 197–199.
  31. Singhal, T.; Shah, S. Naik, R. Outbreak of Burkholderia cepacia complex bacteremia in a chemotherapy day care unit due to intrinsic contamination of an antiemetic drug. Indian J. Med. Microbiol. 2015, 33, 117–119.
  32. Augustowska, M.; Dutkiewicz, J. Variability of airborne micro-flora in a hospital ward within a period of one year. AAEM 2006, 13, 99–106.
  33. Cabo Verde, S.; Almeida, S.; Matos, J.; Guerreiro, D.M.M.; Faria, T.; Botelho, D.; Santos, M.; Viegas, C. Microbiological assessment of indoor air quality at different hospital sites. Res. Microbiol. 2015, 166, 557–563.
  34. Stec, J.; Lenart-Boroń, A. Assessment of microbiological aerosol concentration in selected healthcare facilities in southern Poland. Cent. Eur. J. Public Health 2019, 27, 239–244.
  35. Sivagnanasundaram, P.; Amarasekara, R.; Madegedara, R.; Magana-Arachchi, E.A.D. Assessment of Airborne Bacterial and Fungal Communities in Selected Areas of Teaching Hospital, Kandy, Sri Lanka. Biomed. Res. Int. 2019, 2019, 7393926.
  36. Monteiro, A.; Almeida, B.; Paciência, I.; Cavaleiro Rufo, J.; Ribeiro, E.; Carolino, E.; Viegas, C.; Uva, A.; Cabo Verde, S. Bacterial Contamination in Health Care Centers: Differences between Urban and Rural Settings. Atmosphere 2021, 12, 450.
  37. Montazer, M.; Soleimani, N.; Vahabi, M.; Abtahi, M.; Etemad, K.; Zendehdel, R. Assessment of Bacterial Pathogens and their Antibiotic Resistance in the Air of Different Wards of Selected Teaching Hospitals in Tehran. Indian J. Occup. Environ. Med. 2011, 25, 78–83.
  38. Solomon, F.; Wadilo, F.; Arota, A.; Abraham, Y. Antibiotic resistant airborne bacteria and their multidrug resistance pattern at University teaching referral Hospital in South Ethiopia. Ann. Clin. Microbiol. Antimicrob. 2017, 16, 29.
  39. Allen, K.D.; Green, H. Hospital outbreak of multi-resistant Acinetobacter anitratus: An airborne mode of spread? J. Hosp. Infect. 1987, 9, 110–119.
  40. Dutkiewicz, J.; Mackiewicz, B.; Lemieszek, M.K.; Golec, M.; Milanowski, J. Pantoea agglomerans: A mysterious bacterium of evil and good. Part IV. Beneficial effects. Ann. Agric. Environ. Med. 2016, 23, 206–222.
  41. Dakić, I.; Morrison, D.; Vuković, D.; Savić, B.; Shittu, A.; Jezek, P.; Hauschild, T.; Stepanović, S. Isolation and molecular characterization of Staphylococcus sciuri in the hospital environment. J. Clin. Microbiol. 2005, 43, 2782–2785.
  42. Drozenová, J.; Petrás, P. Vlastnosti koaguláza-negativních stafylokoků izolovaných z hemokultur . Epidemiol. Mikrobiol. Imunol. 2000, 49, 51–58.
  43. Shittu, A.; Lin, J.; Morrison, D.; Kolawole, D. Isolation and molecular characterization of multiresistant Staphylococcus sciuri and Staphylococcus haemolyticus associated with skin and soft-tissue infec-tions. J. Med. Microbiol. 2004, 53, 51–55.
  44. Castellazzi, L.; Mantero, M.; Esposito, S. Update on the Management of Pediatric Acute Osteomyelitis and Septic Arthritis. Int. J. Mol. Sci. 2016, 17, 855.
  45. Taylor, T.A.; Unakal, C.G. Staphylococcus Aureus. . In StatPearls ; StatPearls Publishing: Treasure Island, FL, USA, 2021.
  46. Hodgson, S.H.; Atkins, B.; Bejon, P.; Byren, I.; Whyllic, D.; Athanason, N.A.; Berendt, A.; McNally, M. The microbiology of chronic osteomyelitis: Prevalence of resistance to common empirical anti-microbial regimens. J. Infect. 2010, 60, 338–343.
  47. Inoue, S.; Moriyama, T.; Horinouchi, Y.; Tachibana, T.; Okada, F.; Maruo, K.; Yoshiya, S. Comparison of clinical features and outcomes of staphylococcus aureus vertebral osteomyelitis caused by methicillin-resistant and methicillin-sensitive strains. Springerplus 2013, 2, 283.
  48. Beronius, M.; Bergman, B.; Andersson, R. Vertebral osteomyelitis in Göteborg, Sweden: A retrospective study of patients during 1990–1995. Scand. J. Infect. Dis. 2001, 33, 527–532.
  49. Corrah, T.W.; Enoch, D.A.; Aliyu, S.H.; Lever, A.M. Bacteraemia and subsequent vertebral osteomyelitis: A retrospective review of 125 patients. QJM 2011, 104, 201–207.
  50. Clerc, O.; Prod’hom, G.; Greub, G.; Zanetti, G.; Senn, L. Adult native septic arthritis: A review of 10 years of experience and lessons for empirical antibiotic therapy. J. Antimicrob. Chemother. 2011, 66, 1168–1173.
  51. Stoesser, N.; Pocock, J.; Moore, C.E.; Soeng, S.; Hor, P.; Sar, P.; Limmathurotsakul, D.; Day, N.; Kumar, V.; Khan, S.; et al. The epidemiology of pediatric bone and joint infections in Cambodia, 2007–2011. J. Trop. Pediatr. 2013, 59, 36–42.
  52. Howard-Jones, A.R.; Isaacs, D.; Gibbons, P.J. Twelve-month outcome following septic arthritis in children. J. Pediatr. Orthop. B 2013, 22, 486–490.
  53. Khan, F.Y.; Abu-Khattab, M.; Baagar, K.; Mohamed, S.F.; Elgendy, I.; Anand, D.; Malallah, H.; Sanjay, D. Characteristics of patients with definite septic arthritis at Hamad General Hospital, Qatar: A hospital-based study from 2006 to 2011. Clin. Rheumatol. 2013, 32, 969–973.
  54. Peel, T.N.; Cheng, A.C.; Choong, P.F.; Buising, K.L. Early onset prosthetic hip and knee joint infection: Treatment and outcomes in Victoria, Australia. J. Hosp. Infect. 2012, 82, 248–253.
  55. Westberg, M.; Grøgaard, B.; Snorrason, F. Early prosthetic joint infections treated with debridement and implant retention: 38 primary hip arthroplasties prospectively recorded and followed for median 4 years. Acta Orthop. 2012, 83, 227–232.
  56. Bejon, P.; Berendt, A.; Atkins, B.; Green, N.; Parry, H.; Masters, S.; McLardy-Smith, P.; Gundle, R.; Byren, I. Two-stage revision for prosthetic joint infection: Predictors of outcome and the role of reimplantation microbiology. J. Antimicrob. Chemother. 2010, 65, 569–575, Erratum in J. Antimicrob. Chemother. 2011, 66, 1204..
  57. Byren, I.; Bejon, P.; Atkins, B.L.; Angus, B.; Masters, S.; McLardy-Smith, P.; Gundle, R.; Berendt, A. One hundred and twelve infected arthroplasties treated with ‘DAIR’ (debridement, antibiotics and implant retention): Antibiotic duration and outcome. J. Antimicrob. Chemother. 2009, 63, 1264–1271, Erratum in: J. Antimicrob. Chemother. 2011, 66, 1203; Erratum in: J. Antimicrob. Chemother. 2013, 68, 2964–2965.
  58. Wertheim, H.F.; Melles, D.C.; Vos, M.C.; van Leeuwen, W.; van Belkum, A.; Verbrugh, H.A.; Nouwen, J.L. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect. Dis. 2005, 5, 751–762.
  59. Mathieu, L.; Mottier, F.; Bertani, A.; Danis, J.; Rongiéras, F.; Chauvin, F. Management of neglected open extremity fractures in low-resource settings: Experience of the French Army Medical Service in Chad. Orthop. Traumatol. Surg. Res. 2014, 100, 815–820.
  60. Eidelman, M.; Bialik, V.; Miller, Y.; Kassis, I. Plantar puncture wounds in children: Analysis of 80 hospitalized patients and late sequelae. Isr. Med. Assoc. J. 2003, 5, 268–271.
  61. Laughlin, R.T.; Reeve, F.; Wright, D.G.; Mader, J.T.; Calhoun, J.H. Calcaneal osteomyelitis caused by nail puncture wounds. Foot Ankle Int. 1997, 18, 575–577.
  62. Imoisili, M.A.; Bonwit, A.M.; Bulas, D.I. Toothpick puncture injuries of the foot in children. J. Pediatr. Infect. Dis. 2004, 23, 80–82.
  63. Matinyi, S.; Enoch, M.; Akia, D.; Byaruhanga, V.; Masereka, E.; Ekeu, I.; Atuheire, C. Contamination of microbial pathogens and their an-timicrobial pattern in operating theatres of peri-urban eastern Uganda: A cross-sectional study. BMC Infect. Dis. 2018, 18, 460.
  64. Thomas, S.; Palmer, R.; Chipungu, P.E.G. Reducing bacterial con-tamination in an Orthopedic Theatre ventilated by natural ventilation in a Developing Country. J. Infect. Dev. Ctries. 2016, 10, 518–522.
  65. Bielawska-Drózd, A.; Cieślik, P.; Bohacz, J.; Korniłłowicz-Kowalska, T.; Żakowska, D.; Bartoszcze, M.; Kocik, J. Microbiological analysis of bioaerosols collected from Hospital Emergency Depart-ments and ambulances. Ann. Agric. Environ. Med. 2018, 25, 274–279.
  66. Bolookat, F.; Hassanvand, M.S.; Faridi, S.; Hadei, M.; Rahmatinia, M.; Alimohammadi, M. Assessment of bioaerosol particle characteristics at different hospital wards and operating theaters: A case study in Tehran. MethodsX 2018, 5, 1588–1596.
  67. Azimi, F.; Nabizadeh, R.; Alimohammadi, M.; Naddafi, K. Bacterial Bioaerosols in the Operating Rooms: A Case Study in Tehran Shariati Hospital. J. Air Pollut. Health 2016, 1, 215–218.
  68. Mentese, S.; Rad, A.Y.; Arısoy, M.; Güllü, G. Seasonal and Spatial Variations of Bioaerosols in Indoor Urban Environments, Ankara, Turkey. Indoor Built Environ. 2012, 21, 797–810.
  69. Polednik, B. Aerosol and bioaerosol particles in a dental office. Environ. Res. 2014, 134, 405–409.
  70. Rendon, R.; Garcia, B.C.; Vital, P.G. Assessment of airborne bacteria in selected occupational environments in Quezon City, Philippines. Arch. Environ. Occup. Health 2017, 72, 178–183.
  71. Bartlett, J.G. Antibiotic-associated pseudomembranous colitis. Rev. Infect. Dis. 1979, 1, 530–539.
  72. Miller, B.A.; Chen, L.F.; Sexton, D.J.; Anderson, D.J. Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile Infection and of healthcare-associated infection due to methicillin-resistant Staphylococcus aureus in community hospitals. Infect. Control Hosp. Epidemiol. 2011, 32, 387–390.
  73. Smits, W.K.; Lyras, D.; Lacy, D.B.; Wilcox, M.H.; Kuijper, E.J. Clostridium difficile infection. Nat. Rev. 2016, 2, 16020.
  74. Crobach, M.J.T.; Vernon, J.J.; Loo, V.G.; Kong, L.Y.; Péchiné, S.; Wilcox, M.H.; Kuijper, E.J. Understanding Clostridium difficile Colonization. Clin. Microbiol. Rev. 2018, 31, e00021-17.
  75. Eyre, D.W.; Griffiths, D.; Vaughan, A.; Golubchik, T.; Acharya, M.; O’Connor, L.; Crook, D.W.; Walker, A.S.; Peto, T.E. Asymptomatic Clostridium difficile colonisation and onward transmission. PLoS ONE 2013, 8, e78445.
  76. Kong, L.Y.; Eyre, D.W.; Corbeil, J.; Raymond, F.; Walker, A.S.; Wilcox, M.H.; Crook, D.W.; Michaud, S.; Toye, B.; Frost, E.; et al. Clostridium difficile: Investigating Transmission Patterns Between Infected and Colonized Patients Using Whole Genome Sequencing. Clin. Infect. Dis. Off. Publ. Infect. Dis. Soc. Am. 2019, 68, 204–209.
  77. Zacharioudakis, I.M.; Zervou, F.N.; Pliakos, E.E.; Ziakas, P.D.; Mylonakis, E. Colonization with toxinogenic C. difficile upon hospital admission, and risk of infection: A systematic review and meta-analysis. Am. J. Gastroenterol. 2015, 110, 381–390.
  78. Leffler, D.A.; Lamont, J.T. Clostridium difficile infection. N. Engl. J. Med. 2015, 372, 1539–1548.
  79. Angtuaco, T.; Sharma, V.; Corder, F.; Raufman, J.; Howden, C. Seroprevalence of H. pylori infection and symptoms of up-per gastrointestinal tract disease in two groups of healthcare workers. Dig. Dis. Sci. 2002, 47, 292–297.
  80. Mastromarino, P.; Conti, C.; Donato, K.; Strappini, P.; Cattaruzza, M.; Orsi, G. Does hospital work constitute a risk factor for Helicobacter pylori infection? J. Hosp. Infect. 2005, 60, 261–268.
  81. Napoli, C.; Marcotrigiano, V.; Montagna, M. Air sampling procedures to evaluate microbial contamination: A comparison between active and passive methods in operating theatres. BMC Public Health 2012, 12, 594.
  82. Nasser, A.; Zhang, X.; Yang, L.; Sawafta, F.; Salah, B. Assessment of Surgical Site Infections from Signs & Symptoms of the Wound and Associated Factors in Public Hospitals of Hodeidah City, Yemen. Int. J. Appl. Sci. 2013, 3, 101–110.
  83. Ensayef, S.; Al Shalchi, S.; Sabbar, M. Microbial contamination in the operating theatre: A study in a hospital in Baghdad. East. Mediterr. Health J. 2009, 15, 219–223.
  84. Bellido, F.; Hancock, R. Susceptibility and Resistance of P. aeruginosa to Antimicrobial Agents em in Pseudomona aeruginosa as an Opportunistic Pathogen; Campa, M., Bendinelli, M.F.H., Eds.; Springer: Boston, MA, USA, 1993; pp. 321–348.
  85. Peña, C.; Dominguez, M.A.; Pujol, M.; Vardarguer, R.; Gudiol, F.; Ariza, J. An outbreak of carbapenem-resistant Pseudomonas aeruginosa in a urology ward. Clin. Microbiol. Infect. 2003, 9, 938–943.
  86. Peleg, A.; Seifert, H.; Paterson, D. Acinetobacter baumannii: Emergence of a successful pathogen. Clin. Microbiol. Rev. 2008, 21, 538–582.
  87. Paterson, D. Resistance in gram-negative bacteria: Enterobacteriaceae. Am. J. Med. 2006, 119, S20–S70.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Video Production Service
Feedback