Abstract
Background
Hospital-acquired infection affects hundreds of millions of people worldwide. It is a major global issue for patient safety. Understanding the potential risk factors is important to appreciate the local context. A matched case control study design, which is the first of its kind in the study region, was undertaken to identify risk factors in teaching hospitals of Amhara regional state, Ethiopia.
Method
A matched case control study design matched with age and hospital type was used. The study was conducted in University of Gondar and Felege-Hiwot medical teaching hospital. Cases were patients who fulfilled the criteria based on CDC definition of hospital-acquired infection and controls were patients admitted to the hospital that stayed for more than 48 hours in the ward in the study period, but who did not develop infection. For one case, four controls were selected. Of 545 patients, 109 were cases and 436 were controls. Conditional logistic regression using STATA 13 was used for data analysis.
Result
The median length of stay for cases and controls was 7 and 8 days, respectively. Patients admitted in wards with the presence of medical waste container in the room had 82% less chance of developing hospital-acquired infection (AOR 0.18; 95% CI, 0.03–0.98). The odds of developing hospital-acquired infection among immune deficient patients were 2.34 times higher than their counterparts (95% CI; 1.17–4.69). Patients received antimicrobials, central vascular catheter and surgery since admission had 8.63, 6.91 and 2.35 higher odds of developing hospital-acquired infection, respectively.
Conclusion
Health providers and mangers should consider the provision and availability of healthcare materials and facilities in all of the ward rooms, follow appropriate safe medical procedures for use of external devices on patients, and give attention to the immunocompromised patients for the prevention and control of hospital-acquired infections.
Introduction
Hospitals are the potential source of the risk of acquiring an infection during the healthcare delivery. Hospital-acquired infections(HAIs) are associated with increased attributable mortality, length of stay in the hospital, and healthcare costs incurred by patients and healthcare facilities[1,2]. Hospital-acquired infections are a growing problem at every level of the healthcare system. World Health Organization (WHO) estimated that it affects hundreds of millions of people worldwide and it is a major global issue for patient safety[3]. The prevalence of hospital acquired infections in two teaching hospitals in Ethiopia was 14.9%[4].
Risk of hospital-acquired infections increased with invasive devices used [5] for example, for treatment and monitoring of patient in Intensive Care Units (ICU)[6]. Incidence of device-associated infections(DAIs) as reported by the International Nosocomial Infection Control Consortium(INICC) is higher than reported by the US National Healthcare Safety Network (NHSN)[7,8]. The DAI patients were 5.3% in China[9],12.2% in Colombia[10] and 13% in Peruvians ICU patients[11]. Evidences showed that the device-associated hospital-acquired infections increased the length of stay in hospital [12–14], and increased mortality [10,11,14]. Researches in developing countries showed that the DAIs in intensive care unit were high[15,16] and incurred extra cost for patients[17–19].
Patients admitted to the hospital wards are susceptible to HAIs. Risk factors for such infections vary between different specific site infections, because hospital environments are complex. Previously conducted researches indicated that, longer hospital stays[20,21], gender[22,23], intravascular catheter[24,25], surgery since admission[22,26], intubation[27], mechanical ventilation[28], age of the patient[4,29], type of hospital [4,30], urinary catheter[22,27] were some of the risk factors for hospital acquired infections.
In Ethiopia, though few researches were conducted on specific surgical site infections[31–33] and hospital-acquired infections[4], none of those used strong epidemiological analytical method, to determine important risk factors. Matched case control study also has its own bias during matching[34]. However as compared to cross-sectional design, matched case control design is stronger for risk factor assessment and minimizes bias[35]. There was no such strong evidence generated in the earlier study settings. Therefore, the aim of this study was to identify risk factors of hospital-acquired infections in teaching hospitals of Amhara regional state, Ethiopia. The findings of the study will be used as an input for policy makers, programmers and health care workers to improve the clinical services.
Materials and methods
A matched case control study design, matched by age ± 5 years and hospital, was conducted at the University of Gondar and Felege-Hiwot medical teaching hospitals of Amhara regional State, Ethiopia. Amhara region is the second most populous region in the country. Data was collected in two phases: the first being from 16 March to 02 April 2015 and the second from 01 July to 10 July 2015. All inpatients admitted to the two hospital wards were included in the study. Surgical, Gynecology & Obstetrics, Internal medicine, Pediatrics, Ophthalmology and Intensive Care Unit wards were included. Emergency and Recovery departments and wards were excluded.
Cases were patients who developed a hospital-acquired infection based on Centers for Disease Control’s definition, i.e., patients admitted to the hospitals and presented an infectious agent(s) or its toxin(s), and that occurred 48 h or more after admission to the hospital that were neither present nor incubating on admission[36].
Controls were the patients admitted to the hospital and stayed for more than 48 hours in the ward in the study period and did not developed a hospital-acquired infection. The controls were matched based on age +5 years within the same hospital. A case to control ratio of 1:4 was used.
The outcome variable was presence of hospital-acquired infections. Intrinsic and extrinsic factors, such as immunodeficiency, insertion of a urinary catheter, peripheral vascular catheter, mechanical ventilation, availability of hand washing material, and McCabe score were assessed. Hospital-acquired infections were confirmed if the patient had signs and symptoms which met the Centers for Disease Control and Prevention (CDC, Atlanta, GA, USA) definition at the time of the data collection[36]. The sample size was calculated by assuming a 5% type I error, 80% power to detect exposure difference between cases and controls, a 1:4 ratio of cases to controls, and a design effect of 1.5. Accordingly, 109 cases and 436 controls, a total of 545 subjects were required for the study.
The study was conducted after ethical approval of Addis Ababa University College of Health Science Institutional Review Board. Data were collected after written consent with a brief description on the importance of the study to the participants. In addition to consents taken from the parent/guardian, for children aged between 7–18 years written assents also were taken from each study participants. A pretested standardized questionnaire was used to collect data. Moreover, medical record and consultation with the person in charge of the patient were the gold standard for the identification of the cases. Data collectors were trained for three days about the definitions and the study protocol prior to starting the study. Double data entry was conducted to minimize errors occurred during data entry.
Data was entered and validated using EPI-INFO software version 3.5.3 (Atlanta, USA) and STATA 13 for analysis. After matching cases and controls with a unique identifier, bivariate and multivariable conditional logistic regression was employed to identify independent factors associated with HAI. A bivariate analysis was run for each variable. Then those variables which were significant at the bivariate analysis along with variables that were well known predictors of HAI were included in the multivariable analysis. Odds ratios with the corresponding 95% confidence intervals (CI) were estimated and p values were determined. Variables with P < 0.05 in the multivariable conditional logistic regression analysis were considered as significant independent predictors of HAI in this study.
Results
A total of 545 patients were included in this study. One hundred nine were cases and the remaining 436 were controls. The median age of the cases was 25 years (Interquartile range of 16–35) and, for controls 25 years (Interquartile range of 16–36). Length of stay of patients in the hospital was 8 days with Interquartile range of 4–15 days. The median length of stay for cases and controls was 7 and 8 days respectively (Table 1).
Table 1. Background characteristics of cases and controls, in teaching hospitals in Amhara region, Ethiopia, 2015.
| Characteristics | Cases n = 109 |
Controls n = 436 |
P-Value | |
|---|---|---|---|---|
| hand washing material available in ward | Yes | 45(41.3%) | 238(54.6%) | 0.001 |
| No | 64(58.7%) | 198(45.4%) | ||
| Sex | Male | 64(58.7%) | 201((46.1%) | 0.01 |
| Female | 45(41.2%) | 235(53.9%) | ||
| Age categorized | < = 1 year | 9(8.2%) | 24(5.5%) | |
| 1–14 year | 14(12.84%) | 76(17.43%) | ||
| 15–35 years | 59(54.13% | 255(51.6% | 0.999 | |
| 36–55 years | 22(20.18%) | 90(20.64%) | ||
| > = 56 years | 5(4.6%) | 21(4.8%) | ||
| Ward of admission department | Medicine | 21(19.3%) | 118(27.1%) | |
| pediatrics | 19(17.4% | 79(18.1%) | ||
| surgery | 53(48.6%) | 141(32.3%) | ||
| Gynecology | 16(14.7%) | 93(21.3%) | ||
| Ophthalmology | 0(0%) | 5(1.1%) | ||
| hand rubs available in the ward | Yes | 67(61.5%) | 302(69.3%) | 0.003 |
| No | 42(38.5%) | 134(30.7%) | ||
| Presence of medical waste container in the ward | Yes | 102(93.6%) | 431(98.9%) | 0.04 |
| No | 7(6.4%) | 5(1.1%) | ||
| Diabetics History | Yes | 3(2.8%) | 9 (2.1%) | |
| No | 102 (93.6%) | 402 (92.2%) | 0.400 | |
| Unknown | 4(3.7%) | 25(5.7%) | ||
| Immune deficiency | Yes | 31(28.4%) | 92(21.1%) | 0.018 |
| No | 55(50.5%) | 279 (64.0%) | ||
| Unknown | 23(21.1%) | 65(14.9%) | ||
| McCabe score | Non-Fatal diseases | 47 (43.1%) | 235 (53.9%) | 0.006 |
| Ultimately fatal diseases | 39 (35.8%) | 141 (32.3%) | ||
| Rapidly fatal diseases | 13 (11.9%) | 38 (8.7%) | ||
| Unknown | 10 (9.2%) | 22 (5.0%) | ||
| ASA (American Society of Anesthesiology) classification | Normally health patient | 32 (29.4%) | 146 (33.5%) | 0.494 |
| Patient with mild systemic diseases | 27 (24.8%) | 85 (19.5%) | ||
| Patient with severe systemic disease that is not incapacitating | 32 (29.4%) | 100 (22.9%) | ||
| Patient with incapacitating systemic diseases that is a constant threat to life | 14 (12.8%) | 65 (14.9%) | ||
| Unknown | 4 (3.7%) | 40 (9.2%) | 0.021 | |
| Central Vascular catheter | Yes | 5 (4.6%) | 4 (0.9%) | |
| No | 104 (95.4%) | 432(99.1%) | ||
| Peripheral vascular catheter | Yes | 83 (76.1%) | 291(66.7%) | 0.05 |
| No | 26 (23.9%) | 145(33.3%) | ||
| Urinary catheter | Yes | 33 (30.3%) | 75 (17.2%) | 0.003 |
| No | 76 (69.7%) | 361(82.8%) | ||
| Intubation | Yes | 18 (16.5%) | 29 (6.7%) | |
| No | 91 (83.5%) | 407(93.3%) | 0.001 | |
| Surgery since admission | Yes | 64 (58.7%) | 146(33.5%) | 0.000 |
| No | 45 (41.3%) | 290(66.5%) | ||
| Length of stay categorized | <8 days (below the median | 63 (57.8%) | 209(47.9%) | 0.06 |
| > = 8 days (above or equal to median) | 46 (42.2%) | 227(52.1%) | ||
| The patient received Antimicrobial | Yes | 104 (95.4%) | 294(67.4%) | 0.000 |
| No | 5 (4.6%) | 142(32.6%) | ||
Availability of waste management material, immune status of the patient, central vascular catheter, surgery for admission and the patient received antimicrobial at the time of the survey were the predictors of hospital acquired infection. Patients in wards with the presence of medical waste container in the room were 82% less likely to develop hospital acquired infection compared to the patients in the wards without medical waste container with, AOR 0.18: and 95% CI, (0. 03–0.98). The odds of developing hospital-acquired infection among patients with immune deficiency patients were 2.34 times higher compared to their counterpart patients with 95% CI: (1.17–4.69). The central vascular catheter was a risk factor for hospital-acquired infection with AOR 6.92 and 95% CI: 1.28–37.47. The odds of developing hospital-acquired infection among patients who had surgery since admission in the ward was 2.35 times higher compared with patients without surgery since admission in the ward with 95% CI:1.08–5.09. Antimicrobial use was also a risk factor for hospital-acquired infection with AOR of 8.63with 95% CI: (3. 11–23.95) (Table 2).
Table 2. Risk factors for HAI in teaching hospitals in Amhara region, Ethiopia 2015.
| Characteristics | Cases | Controls | Crude OR (Odds Ratio) (95% CI) |
Adjusted OR (Odds Ratio) (95% CI) |
|
|---|---|---|---|---|---|
| Available hand washing material in ward | Yes | 45(41.3%) | 238(54.6%) | 0.38(0. 21–0.68) ** | 0.81(0.35–1.86) |
| No | 64(58.7%) | 198(45.4%) | 1 | 1 | |
| Presence of medical waste container at room | Yes | 102(93.6%) | 431(98.9%) | 0.12(0.003-.03) ** | 0.18(0.03–0.97) |
| No | 7(6.4%) | 5(1.1%) | 1 | 1 | |
| Sex | Male | 64(58.7%) | 201((46.1%) | 1 | 1 |
| Female | 45(41.2%) | 235(53.9%) | 0.57(0.37–0.89) ** | 0.65(0.37–1.13) | |
| Immune deficiency | No | 55(50.5%) | 279(64.0%) | 1 | 1 |
| Yes | 31(28.4%) | 92(21.1%) | 1. 78(1.03–3.04) * | 2.34(1.17–4.69) ** | |
| Unknown | 23(21.1%) | 65(14.9%) | 1.86(1.03–3.37)* | 1.26(0.61–2.59)) | |
| McCabe score | Non-Fatal diseases | 47 (43.1%) | 235(53.9%) | 1 | 1 |
| Ultimately fatal diseases | 39 (35.8%) | 141(32.3%) | 1.48(0.88–2.48) | 1.34(0.63–2.85)) | |
| Rapidly fatal diseases | 13 (11.9%) | 38 (8.7%) | 1.76(0.86–3.60) * | 2.51(0.84–7.44)) | |
| Unknown | 10 (9.2%) | 22 (5.0%) | 2.54(1.05–6.13) * | 1.04(0.30–3.58)) | |
| ASA classification | Normally health patient | 32 (29.4%) | 146(33.5%) | 1 | 1 |
| Patient with mild systemic diseases | 27 (24.8%) | 85 (19.5%) | 1.68(0.91–3.13) | 0.78(0.36–1.72) | |
| Patient with severe systemic disease that is not incapacitating | 32 (29.4%) | 100(22.9%) | 1.84(0.98–3.47) | 1.08(0.41–2.87) | |
| Patient with incapacitating systemic diseases that is a constant threat to life | 14 (12.8%) | 65 (14.9%) | 1.20(0.55–2.59) | 1.19(0.35–4.11) | |
| Unknown | 4 (3.7%) | 40 (9.2%) | 0.28(0.07–1.03) | 0.09(0.01–0.64) * | |
| Central Vascular catheter | Yes | 5 (4.6%) | 4 (0.9%) | 5.00(1.34–18.61) * | 6.92(1.28–37.47) * |
| No | 104(95.4%) | 432(99.1%) | 1 | 1 | |
| Peripheral vascular catheter | Yes | 83 (76.1%) | 291(66.7%) | 1.61(0.99–2.63) | 1.17(0.59–2.32) |
| No | 26 (23.9%) | 145(33.3%) | 1 | 1 | |
| Urinary catheter | Yes | 33 (30.3%) | 75 (17.2%) | 2.30(1.37–3.87) ** | 1.23(0.59–2.55) |
| No | 76 (69.7%) | 361(82.8%) | 1 | 1 | |
| Intubation | Yes | 18 (16.5%) | 29 (6.7%) | 3.40(1.66–6.97) ** | 0.80(0.28–2.31) |
| No | 91 (83.5%) | 407(93.3%) | 1 | 1 | |
| Surgery since admission | Yes | 64 (58.7%) | 146(33.5%) | 3.31(2.05–5.36) ** | 2.35(1.08–5.09) * |
| No | 45 (41.3%) | 290(66.5%) | 1 | 1 | |
| Patient received Antimicrobial | Yes | 104(95.4%) | 294(67.4%) | 10.69(4.22–27.07) ** | 8.63(3.11–23.95) *** |
| No | 5 (4.6%) | 142(32.6%) | 1 | 1 | |
* Statistically significant association P<0.05
**strong statistically significant p between 0.001 & 0.05
*** Very strong, statistically significant P<0.001.
Discussion
Risk factors for hospital-acquired infection are dynamic and complex phenomena in the hospital. In this matched case control study, availability of waste management material in the room, immune status of the patient, central vascular catheter, surgery since admission and patient received antimicrobial at the time of survey were the predictors of hospital acquired infection.
Most of the studies on risk factors for hospital-acquired infection employed by cross-sectional methods, that has a limitation of statistical power by comparing the groups internally. The introduction of bias in matched case control study is lower than in the cross-sectional design [35]. Matched case control study design is assumed to generate valid data impacting the reduction of bias among main exposure variables.
The availability of hand-washing facilities waste management material in the ward are important to prevent hospital acquired infection[37]. The presence of alcohol- based hand rub material in the ward significantly increases the consumption of alcohol-hand rub material in the ward[38]. Thus availability of hygiene maintenance materials and behaviors of healthcare workers reduced healthcare associated infections[39–41]. In Ethiopia researches showed low level of hand hygiene practice[42] and poor condition of medical waste management in health care facilities [43]. The availability of waste management materials is believed to reduces the exposure of waste to patients and health care workers.
This study found immune deficiency of patients as a risk factor for hospital acquired infection. This finding was also supported by another finding, in which patients with high compromised health status were at risk for hospital acquired infection[44].
In the modern healthcare system, the live saving invasive treatment devices and procedures are found to increasingly threaten patients. For example, while catheters provide lifesaving therapy, they also have an iatrogenic effect, by being a route of transmission of microorganisms to the patient’s body, thereby causing infection. Hospital-acquired infections occur with the devices used in medical procedures[45]. A hospital based research in Poland showed a positive correlation between prevalence of hospital-acquired infection and exposure to invasive procedures[22]. In our study, central vascular catheter used on patients was 7.56 times more likely to be a risk factor compared to non-central vascular catheter patients. This finding was supported by other studies conducted in hospitals in Poland, Morocco and China [22,26,46].
The high risk of central vascular catheter may be due to low level of implementation of a multidimensional infection control strategy in the study setting. Implementation of Nosocomial Infection Control Consortium (INICC) bundles and other infection control measures in some of the developing countries reduced devise-associated infection of CLABSI[47–50], VAP[49,51,52] and CAUTI [53] in ICU patients. Surgery since admission was one of the determining factors for hospital-acquired infection in this finding. This was also supported by other findings of pilot point prevalence study conducted by the European Centre for Disease Prevention and Control (ECDC) [54] and China and Poland[23,26].
A research showed that, antimicrobial prescribing with broad-spectrum antibiotics to patients increased the risk of hospital acquired Drug-Resistant Acinetobacter baumannii infections[44]. A similar finding was also observed in Morocco that; antimicrobial use was associated with hospital-acquired infections[46]. Our study supported the above finding in which a patient received antimicrobial was 9.16 times more likely to acquire hospital-acquired infections compared to those who didn’t take antimicrobials.
This study has limitations. In this research, we focused on a relatively small number of risk factors for hospital-acquired infections. Some of the clinical data in the hospital recording system was incomplete. This may introduce bias in statistical analysis. Evidence for this finding can be generalized to similar resource limited settings. Because, the data were collected from a large proportion of controls to cases, it gives high power to identify the variations in the population. The other limitation in this study was that controls did not match by type of ward and length of stay with cases. This may minimize the power of the study to identify confounders in the study.
Conclusions
Despite the above limitations, the risk factors identified in this study are very important for the prevention and control of hospital-acquired infection in teaching hospitals in Ethiopia. Presence of medical waste container in the room, patients’ immune status, central vascular catheter, surgery since admission and patients received antimicrobials were the independent predictors for hospital acquired infections. The managers and medical workforce should consider the availability of healthcare facilities. Hospitals and clinicians need to follow the appropriate safe medical procedures for use of external devices and give attention to the immunocompromised patients for the prevention and control of hospital-acquired infections.
Supporting information
(ZIP)
Acknowledgments
We would like to thank Addis Ababa University and University of Gondar for their material support. We also acknowledge patients and their families for their participation in this study.
Data Availability
All relevant data are within the paper and its Supporting Information file.
Funding Statement
The authors received no specific funding for this work.
References
- 1.Sheng W-H, Chie W-C, Chen Y-C, Hung C-C, Wang J-T, Chang S-C. Impact of nosocomial infections on medical costs, hospital stay, and outcome in hospitalized patients. J Formos Med Assoc Taiwan Yi Zhi. 2005;104: 318–326. [PubMed] [Google Scholar]
- 2.Yang C-C, Shih N-C, Chang W-C, Huang S-K, Chien C-W. Long-term medical utilization following ventilator-associated pneumonia in acute stroke and traumatic brain injury patients: a case-control study. BMC Health Serv Res. 2011;11: 289 doi: 10.1186/1472-6963-11-289 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.WHO. WHO Guidelines on Hand Hygiene in Health Care: a Summary [Internet]. WHO; 2009. Available: www.who.int/patientsafety/en/ [Google Scholar]
- 4.Yallew WW, Takele AK, Yehuala FM. Point prevalence of hospital-acquired infections in two teaching hospitals of Amhara region in Ethiopia. Drug Healthc Patient Saf. 2016;Volume 8: 71–76. doi: 10.2147/DHPS.S107344 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Deptuła A, Trejnowska E, Ozorowski T, Hryniewicz W. Risk factors for healthcare-associated infection in light of two years of experience with the ECDC point prevalence survey of healthcare-associated infection and antimicrobial use in Poland. J Hosp Infect. 2015;90: 310–315. doi: 10.1016/j.jhin.2015.03.005 [DOI] [PubMed] [Google Scholar]
- 6.Madani N, Rosenthal VD, Dendane T, Abidi K, Zeggwagh AA, Abouqal R. Health-care associated infections rates, length of stay, and bacterial resistance in an intensive care unit of Morocco: Findings of the International Nosocomial Infection Control Consortium (INICC). Int Arch Med. 2009;2: 29 doi: 10.1186/1755-7682-2-29 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Dudeck MA, Edwards JR, Allen-Bridson K, Gross C, Malpiedi PJ, Peterson KD, et al. National Healthcare Safety Network report, data summary for 2013, Device-associated Module. Am J Infect Control. 2015;43: 206–221. doi: 10.1016/j.ajic.2014.11.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Rosenthal VD, Al-Abdely HM, El-Kholy AA, AlKhawaja SAA, Leblebicioglu H, Mehta Y, et al. International Nosocomial Infection Control Consortium report, data summary of 50 countries for 2010–2015: Device-associated module. Am J Infect Control. 2016;44: 1495–1504. doi: 10.1016/j.ajic.2016.08.007 [DOI] [PubMed] [Google Scholar]
- 9.Tao L, Hu B, Rosenthal VD, Gao X, He L. Device-associated infection rates in 398 intensive care units in Shanghai, China: International Nosocomial Infection Control Consortium (INICC) findings. Int J Infect Dis IJID Off Publ Int Soc Infect Dis. 2011;15: e774–780. doi: 10.1016/j.ijid.2011.06.009 [DOI] [PubMed] [Google Scholar]
- 10.Moreno CA, Rosenthal VD, Olarte N, Gomez WV, Sussmann O, Agudelo JG, et al. Device-associated infection rate and mortality in intensive care units of 9 Colombian hospitals: findings of the International Nosocomial Infection Control Consortium. Infect Control Hosp Epidemiol. 2006;27: 349–356. doi: 10.1086/503341 [DOI] [PubMed] [Google Scholar]
- 11.Cuellar LE, Fernandez-Maldonado E, Rosenthal VD, Castaneda-Sabogal A, Rosales R, Mayorga-Espichan MJ, et al. Device-associated infection rates and mortality in intensive care units of Peruvian hospitals: findings of the International Nosocomial Infection Control Consortium. Rev Panam Salud Pública. 2008;24: 16–24. doi: 10.1590/S1020-49892008000700002 [DOI] [PubMed] [Google Scholar]
- 12.Rai Vineya, Yuet-Meng Cheong, Rosenthal, Daniel Victor, Shahnaz Hasan Mohd, Kamarul Zaman Mazuin, Mansor Marzida, et al. Device-associated infection and mortality rates, bacterial resistance, and length of stay in hospitals of Malaysia: International Nosocomial Infection Control Consortium (INICC)’s findings. Can J Infect Control. 2016;31: 107–112. [Google Scholar]
- 13.Al-Mousa HH, Omar AA, Rosenthal VD, Salama MF, Aly NY, El-Dossoky Noweir M, et al. Device-associated infection rates, bacterial resistance, length of stay, and mortality in Kuwait: International Nosocomial Infection Consortium findings. Am J Infect Control. 2016;44: 444–449. doi: 10.1016/j.ajic.2015.10.031 [DOI] [PubMed] [Google Scholar]
- 14.Hu B, Tao L, Rosenthal VD, Liu K, Yun Y, Suo Y, et al. Device-associated infection rates, device use, length of stay, and mortality in intensive care units of 4 Chinese hospitals: International Nosocomial Control Consortium findings. Am J Infect Control. 2013;41: 301–306. doi: 10.1016/j.ajic.2012.03.037 [DOI] [PubMed] [Google Scholar]
- 15.Jahani-Sherafat S, Razaghi M, Rosenthal VD, Tajeddin E, Seyedjavadi S, Rashidan M, et al. Device-associated infection rates and bacterial resistance in six academic teaching hospitals of Iran: Findings from the International Nocosomial Infection Control Consortium (INICC). J Infect Public Health. 2015;8: 553–561. doi: 10.1016/j.jiph.2015.04.028 [DOI] [PubMed] [Google Scholar]
- 16.Rasslan O, Seliem ZS, Ghazi IA, El Sabour MA, El Kholy AA, Sadeq FM, et al. Device-associated infection rates in adult and pediatric intensive care units of hospitals in Egypt. International Nosocomial Infection Control Consortium (INICC) findings. J Infect Public Health. 2012;5: 394–402. doi: 10.1016/j.jiph.2012.07.002 [DOI] [PubMed] [Google Scholar]
- 17.Rosenthal VD, Udwadia FE, Kumar S, Poojary A, Sankar R, Orellano PW, et al. Clinical impact and cost-effectiveness of split-septum and single-use prefilled flushing device vs 3-way stopcock on central line-associated bloodstream infection rates in India: a randomized clinical trial conducted by the International Nosocomial Infection Control Consortium (INICC). Am J Infect Control. 2015;43: 1040–1045. doi: 10.1016/j.ajic.2015.05.042 [DOI] [PubMed] [Google Scholar]
- 18.Higuera F, Rangel-Frausto MS, Rosenthal VD, Soto JM, Castañon J, Franco G, et al. Attributable cost and length of stay for patients with central venous catheter-associated bloodstream infection in Mexico City intensive care units: a prospective, matched analysis. Infect Control Hosp Epidemiol. 2007;28: 31–35. doi: 10.1086/510812 [DOI] [PubMed] [Google Scholar]
- 19.Rosenthal VD, Guzman S, Migone O, Crnich CJ. The attributable cost, length of hospital stay, and mortality of central line-associated bloodstream infection in intensive care departments in Argentina: A prospective, matched analysis. Am J Infect Control. 2003;31: 475–480. doi: 10.1016/j.ajic.2003.03.002 [DOI] [PubMed] [Google Scholar]
- 20.Al-Rawajfah OM, Cheema J, Hewitt JB, Hweidi IM, Musallam E. Laboratory-confirmed, health care-associated bloodstream infections in Jordan: a matched cost and length of stay study. Am J Infect Control. 2013;41: 607–611. doi: 10.1016/j.ajic.2012.08.014 [DOI] [PubMed] [Google Scholar]
- 21.Gravel D, Taylor G, Ofner M, Johnston L, Loeb M, Roth V, et al. Point prevalence survey for healthcare-associated infections within Canadian adult acute-care hospitals☆☆☆. J Hosp Infect. 2007;66: 243–248. doi: 10.1016/j.jhin.2007.04.008 [DOI] [PubMed] [Google Scholar]
- 22.Deptuła A, Trejnowska E, Ozorowski T, Hryniewicz W. Risk factors for healthcare-associated infection in light of two years of experience with the ECDC point prevalence survey of healthcare-associated infection and antimicrobial use in Poland. J Hosp Infect. 2015;90: 310–315. doi: 10.1016/j.jhin.2015.03.005 [DOI] [PubMed] [Google Scholar]
- 23.Durlach R, McIlvenny G, Newcombe RG, Reid G, Doherty L, Freuler C, et al. Prevalence survey of healthcare-associated infections in Argentina; comparison with England, Wales, Northern Ireland and South Africa. J Hosp Infect. 2012;80: 217–223. doi: 10.1016/j.jhin.2011.12.001 [DOI] [PubMed] [Google Scholar]
- 24.Gailienė G, Gierasimovič Z, Petruševičienė D, Macijauskienė A. The prevalence of health care-associated infections and risk factors in a university hospital. Med Kaunas Lith. 2012;48: 399–403. [PubMed] [Google Scholar]
- 25.Humphreys H, Newcombe RG, Enstone J, Smyth ETM, McIlvenny G, Fitzpatrick F, et al. Four country healthcare associated infection prevalence survey 2006: risk factor analysis. J Hosp Infect. 2008;69: 249–257. doi: 10.1016/j.jhin.2008.04.021 [DOI] [PubMed] [Google Scholar]
- 26.Liu JY, Wu YH, Cai M, Zhou CL. Point-prevalence survey of healthcare-associated infections in Beijing, China: a survey and analysis in 2014. J Hosp Infect. 2016;93: 271–279. doi: 10.1016/j.jhin.2016.03.019 [DOI] [PubMed] [Google Scholar]
- 27.Phu VD, Wertheim HFL, Larsson M, Nadjm B, Dinh Q-D, Nilsson LE, et al. Burden of Hospital Acquired Infections and Antimicrobial Use in Vietnamese Adult Intensive Care Units. PloS One. 2016;11: e0147544 doi: 10.1371/journal.pone.0147544 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Oldfield MM, El-Masri MM, Fox-Wasylyshyn SM. Examining the association between chest tube-related factors and the risk of developing healthcare-associated infections in the ICU of a community hospital: a retrospective case-control study. Intensive Crit Care Nurs. 2009;25: 38–44. doi: 10.1016/j.iccn.2008.07.001 [DOI] [PubMed] [Google Scholar]
- 29.Zhang X, Tong M-M, Zhang M-Z, Zhu H-P. Risk factors of nosocomial bloodstream infections in surgical intensive care unit. Int J Clin Exp Med. 2015;8: 16682–16687. [PMC free article] [PubMed] [Google Scholar]
- 30.Xie D, Xiong W, Xiang L, Fu X, Yu Y, Liu L, et al. Point prevalence surveys of healthcare-associated infection in 13 hospitals in Hubei Province, China, 2007–2008. J Hosp Infect. 2010;76: 150–155. doi: 10.1016/j.jhin.2010.04.003 [DOI] [PubMed] [Google Scholar]
- 31.Amenu D, Belachew T, Araya F. Surgical Site Infection Rate and Risk Factors Among Obstetric Cases of Jimma University Specialized Hospital, Southwest Ethiopia. Ethiop J Health Sci. 2011;21: 91–100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Endalafer N, Gebre-Selassie S, Kotiso B. Nosocomial bacterial infections in a tertiary hospital in Ethiopia. J Infect Prev. 2011;12: 38–43. doi: 10.1177/1757177410376680 [Google Scholar]
- 33.Mulu W, Kibru G, Beyene G, Damtie M. Postoperative Nosocomial Infections and Antimicrobial Resistance Pattern of Bacteria Isolates among Patients Admitted at Felege Hiwot Referral Hospital, Bahirdar, Ethiopia. Ethiop J Health Sci. 2012;22: 7–18. [PMC free article] [PubMed] [Google Scholar]
- 34.Moyses Szklo, F. Javier Nieto. Epidemiology: Beyond the Basics. 3rd ed. USA: Jones & Bartlett Learning; 2014.
- 35.Jiménez-Romano E, Blanco JI, Delgado-Rodríguez M, Bueno-Cavanillas A, Gálvez-Vargas R. Validity of the cross-sectional study for the ascertainment of nosocomial infection risk factors. Eur J Epidemiol. 1993;9: 263–268. [DOI] [PubMed] [Google Scholar]
- 36.Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control. 2008;36: 309–332. doi: 10.1016/j.ajic.2008.03.002 [DOI] [PubMed] [Google Scholar]
- 37.World Health Organization. WHO guidelines on hand hygiene in health care: first global patient safety challenge e clean care is safer care. WHO; 2009. [PubMed] [Google Scholar]
- 38.Hansen S, Schwab F, Gastmeier P, PROHIBIT study group, Pittet D, Zingg W, et al. Provision and consumption of alcohol-based hand rubs in European hospitals. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2015;21: 1047–1051. doi: 10.1016/j.cmi.2015.09.019 [DOI] [PubMed] [Google Scholar]
- 39.Savolainen-Kopra C, Haapakoski J, Peltola PA, Ziegler T, Korpela T, Anttila P, et al. Hand washing with soap and water together with behavioural recommendations prevents infections in common work environment: an open cluster-randomized trial. Trials. 2012;13: 10 doi: 10.1186/1745-6215-13-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Stiller A, Salm F, Bischoff P, Gastmeier P. Relationship between hospital ward design and healthcare-associated infection rates: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2016;5 doi: 10.1186/s13756-016-0152-1 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Monistrol O, Calbo E, Riera M, Nicolás C, Font R, Freixas N, et al. Impact of a hand hygiene educational programme on hospital-acquired infections in medical wards. Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis. 2012;18: 1212–1218. doi: 10.1111/j.1469-0691.2011.03735.x [DOI] [PubMed] [Google Scholar]
- 42.Abdella NM, Tefera MA, Eredie AE, Landers TF, Malefia YD, Alene KA. Hand hygiene compliance and associated factors among health care providers in Gondar University Hospital, Gondar, North West Ethiopia. BMC Public Health. 2014;14: 96 doi: 10.1186/1471-2458-14-96 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Tadesse ML, Kumie A. Healthcare waste generation and management practice in government health centers of Addis Ababa, Ethiopia. BMC Public Health. 2014;14 doi: 10.1186/1471-2458-14-1221 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Chan M-C, Chiu S-K, Hsueh P-R, Wang N-C, Wang C-C, Fang C-T. Risk factors for healthcare-associated extensively drug-resistant Acinetobacter baumannii infections: a case-control study. PloS One. 2014;9: e85973 doi: 10.1371/journal.pone.0085973 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 45.Type of Healthcare-Associated Infections | HAI | CDC [Internet]. [cited 31 Aug 2016]. Available: https://www.cdc.gov/HAI/infectiontypes.html
- 46.Razine R, Azzouzi A, Barkat A, Khoudri I, Hassouni F, Chefchaouni AC, et al. Prevalence of hospital-acquired infections in the university medical center of Rabat, Morocco. Int Arch Med. 2012;5: 26 doi: 10.1186/1755-7682-5-26 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Rosenthal VD, Maki DG, Rodrigues C, Alvarez-Moreno C, Leblebicioglu H, Sobreyra-Oropeza M, et al. Impact of International Nosocomial Infection Control Consortium (INICC) strategy on central line-associated bloodstream infection rates in the intensive care units of 15 developing countries. Infect Control Hosp Epidemiol. 2010;31: 1264–1272. doi: 10.1086/657140 [DOI] [PubMed] [Google Scholar]
- 48.Rosenthal VD, Ramachandran B, Villamil-Gómez W, Armas-Ruiz A, Navoa-Ng JA, Matta-Cortés L, et al. Impact of a multidimensional infection control strategy on central line-associated bloodstream infection rates in pediatric intensive care units of five developing countries: findings of the International Nosocomial Infection Control Consortium (INICC). Infection. 2012;40: 415–423. doi: 10.1007/s15010-012-0246-5 [DOI] [PubMed] [Google Scholar]
- 49.Rosenthal VD, Rodríguez-Calderón ME, Rodríguez-Ferrer M, Singhal T, Pawar M, Sobreyra-Oropeza M, et al. Findings of the International Nosocomial Infection Control Consortium (INICC), Part II: Impact of a multidimensional strategy to reduce ventilator-associated pneumonia in neonatal intensive care units in 10 developing countries. Infect Control Hosp Epidemiol. 2012;33: 704–710. doi: 10.1086/666342 [DOI] [PubMed] [Google Scholar]
- 50.Leblebicioglu H, Öztürk R, Rosenthal VD, Akan ÖA, Sirmatel F, Ozdemir D, et al. Impact of a multidimensional infection control approach on central line-associated bloodstream infections rates in adult intensive care units of 8 cities of Turkey: findings of the International Nosocomial Infection Control Consortium (INICC). Ann Clin Microbiol Antimicrob. 2013;12: 10 doi: 10.1186/1476-0711-12-10 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51.Tao L, Hu B, Rosenthal VD, Zhang Y, Gao X, He L. Impact of a multidimensional approach on ventilator-associated pneumonia rates in a hospital of Shanghai: findings of the International Nosocomial Infection Control Consortium. J Crit Care. 2012;27: 440–446. doi: 10.1016/j.jcrc.2011.12.018 [DOI] [PubMed] [Google Scholar]
- 52.Rosenthal VD, Álvarez-Moreno C, Villamil-Gómez W, Singh S, Ramachandran B, Navoa-Ng JA, et al. Effectiveness of a multidimensional approach to reduce ventilator-associated pneumonia in pediatric intensive care units of 5 developing countries: International Nosocomial Infection Control Consortium findings. Am J Infect Control. 2012;40: 497–501. doi: 10.1016/j.ajic.2011.08.005 [DOI] [PubMed] [Google Scholar]
- 53.Rosenthal VD, Todi SK, Álvarez-Moreno C, Pawar M, Karlekar A, Zeggwagh AA, et al. Impact of a multidimensional infection control strategy on catheter-associated urinary tract infection rates in the adult intensive care units of 15 developing countries: findings of the International Nosocomial Infection Control Consortium (INICC). Infection. 2012;40: 517–526. doi: 10.1007/s15010-012-0278-x [DOI] [PubMed] [Google Scholar]
- 54.Zarb P, Coignard B, Griskeviciene J, Muller A, Vankerckhoven V, Weist K, et al. The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use. Euro Surveill Bull Eur Sur Mal Transm Eur Commun Dis Bull. 2012;17. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
(ZIP)
Data Availability Statement
All relevant data are within the paper and its Supporting Information file.