infections in Italy Rossella Abbate, MD, a Gabriella Di Giuseppe, MD, b Paolo Marinelli, MD, a Italo F. Angelillo, DDS, MPH, a and the Collaborative Working Group Naples and Catanzaro, Italy Background: Hospital-associated infections are associated with morbidity, extended hospital stay, mortality, and attributable costs to the health care sector. Methods: A survey of 450 patients admitted to hospitals in Italy determined knowledge, attitudes, and behaviors regarding hospital- associated infections. A face-to-face interview sought information about: patients sociodemographic characteristics; hospital ad- missions and examinations; knowledge, understanding, attitudes, and experience of health careassociated infections; and sources for information. Results: Patients who were higher educated, unmarried, rst-time admitted, and who have received information about hospital- associated infections were more likely to know denition, risk groups, and risk factors of such infections. Respondents levels of perceived risk of contracting a hospital-associated infection were signicantly higher in those who were married, unemployed, in medical wards, who overestimated the incidence rate, and who believed that health care professionals cannot infect patients. Pa- tients willing to stop a health care worker who is not using gloves and mask were females, higher educated, those who believed that health care professionals can infect patients, who overestimated the incidence rate, who have never been exposed to such infections, who have never had received information, and who do not need information about hospital-associated infections. Conclusions: Actions aimed at improving knowledge are crucial to the development and implementation of effective public health preventive strategies. (Am J Infect Control 2008;36:39-47.) It is well documented in several countries that hos- pital-associated infections represent one of the most common adverse events affecting patients admitted to acute care hospitals, and these infections are associ- ated with morbidity, extended hospital stay, mortality, and attributable costs to the health care sector. 1,2 Assessment of patients attitudes and opinions con- cerning the risk of the transmission of infections in health care settings deserve attention, because the perception of risk of acquiring these infections may exceed or be disproportionate to the actual risks. As a result, some people may avoid seeking health care ser- vices or discriminate among providers on the basis of that perceived risk, a detriment to both provider and patient. Furthermore, public health education may be needed to promote focused efforts in prevention and control, especially when compliance with infection control policies and procedures, such as the routine use of universal precautions and handwashing, varies and frequently is below ideal levels. At present there has been little assessment about patients knowledge andexperiences concerning hospi- tal-acquired infections and in particular on procedures for prevention and control. 3-5 One hopes that gaining a better understanding on attitudes and opinions from the patients perspective will cause effective changes in public health policy and infection-control proce- dures. Therefore, the objectives of this survey were to concurrently document the level of knowledge, atti- tudes, and behavior and to identify their determinants regarding hospital-associated infections among medi- cal and surgical patients admitted to hospitals in Italy. MATERIAL AND METHODS The target population for this cross-sectional survey, carried out during the period between June and Octo- ber 2006, was a random sample of patients hospital- ized at three randomly selected nonacademic public acute care hospitals in the area of Naples (Italy). From the Department of Public, Clinical and Preventive Medicine, a Second University of Naples, Naples, Italy; and Chair of Hygiene, b Med- ical School, University of Catanzaro Magna Grcia, Catanzaro, Italy. Address correspondence to Italo F. Angelillo, DDS, MPH, Department of Public, Clinical and Preventive Medicine, Second University of Naples, Via Luciano Armanni, 5, 80138 Naples, Italy. E-mail: italof.angelillo@ unina2.it. Members of the Collaborative Working Group are as follows: Andrea De Stefano, MD (Hospital Santa Maria della Pieta`, Nola, Naples), Maur- izio di Mauro, MD (Hospital San Giovanni Bosco, Naples), Antonio Sciambra, MD (Hospital Evangelico Villa Betania, Naples). 0196-6553/$34.00 Copyright 2008 by the Association for Professionals in Infection Control and Epidemiology, Inc. doi:10.1016/j.ajic.2007.01.006 39 In all medical (general medicine, cardiology, geriat- rics, nephrology, pulmonary) and surgical wards (ENT [ear, nose, throat], general surgery, gynaecology, oncol- ogy surgery, orthopaedics/traumatology, neurosur- gery), except psychiatric, a condential face-to-face interview with each patient, after obtaining verbal in- formed consent from participants, was administered for data collection by two previously well-trained phy- sicians. The interviewers provided to the participants details on the study purpose and assurance about the anonymity and condentiality of the interview. The anonymous questionnaire was divided into a number of areas that sought information about the following: patients social and demographic characteristics; previ- ous hospital admissions and examinations; current knowledge, understanding, attitudes, and experience of health careassociated infections; and sources for information (Appendix A). The answers to all of the knowledge questions about transmission and risk fac- tors were arranged as yes, no, and do not know choices. The response choices for all statements relat- ing to general attitudes to ascertain level of agreement or disagreement were given on a 3-point Likert-type scale (i.e., agrees, uncertain, disagrees). Respondents were also asked to report their own perceived risk of hospital-associated infections on a 10-point Likert- type scale with options ranging from 1 (impossible) to 10 (very likely). Participants were asked in behav- iors questions whether or not they have been exposed to hospital-associated infections related to the level of compliance of health care workers with standard precautions and the answers were given on a 5-point Likert-type scale, with options ranging from never to always. We have asked whether the patient has been exposed to a health care worker who did not wear gloves when touching blood, body uids, mucous membranes, or nonintact skin, and did not wear a mask during procedures and patient-care activities that may pose risk for contamination by nasal and/or oral ora of the health care worker. Patients were also asked their willingness to stop a health care worker who is not using such precautions during these activities and the main reasons for their decision. All items in the original version of the questionnaire were assessed to ensure practicability, validity, and interpretation of answers in a pilot test among a con- venient group of patients. On the basis of the com- ments obtained, the questionnaire was revised in item, wording, and format before distribution to the study sample. STATISTICAL ANALYSIS Multiple stepwise logistic and linear regression analyses were performed. In the models developed, we included variables that we considered likely to be associated with the following outcomes of interest: knowledge (denition, risk groups, risk factors) about hospital-associated infections (Model 1); willingness to stop a health care worker who is not wearing gloves when touching blood, body uids, mucous membranes or nonintact skin, and mask during procedures and pa- tient-care activities that may pose risk for contamina- tion by nasal and/or oral ora of the health care worker (Model 2); perception of risk of contracting a hospital-associated infection (Model 3). The following independent variables were included in all models: gender (male50, female51), age (continuous, in years), marital status (single/separated/divorced/widowed50, married51), educational level (ve categories: ,5 years51, 5-7 years52, 8-12 years53, 13-17 years54, .17 years55), occupational position (unemployed50, employed51), rst-time hospital admitted (yes50, no51), overall number of surgical procedures already received (050, $151), hospital ward (surgical50, med- ical51), length of hospital stay of the present admis- sion (continuous, in days), information received about hospital-associated infections (no50, yes51), health professionals as source of information about hospital- associated infections (no50, yes51), and need of additional information regarding hospital-associated infections (no50, yes51). The following variables were also included: knowledge of the incidence rate of hospital-associated infections (three categories: underestimation50, correct estimation51, over- estimation52), and belief that health care professionals can infect patients (no50, yes51) in models 2 and 3; knowledge of risk factors of hospital-associated infec- tions (no50, yes51), perception of risk of contracting a hospital-associated infection (continuous), and pa- tients who have been exposed at least once to a health care worker who did not wear gloves, when touching blood, body uids, mucous membranes or nonintact skin of all patients, and mask during procedures and patient-care activities that may pose risk for contamina- tion by nasal and/or oral ora of the health care worker (no50, yes51) in model 2; and knowledge (denition, risk groups, risk factors) about hospital-associated infections (no50, yes51) in model 3. Before testing multivariable logistic regression models assessing predictors of the outcomes of inter- est, we examined correlations to assess collinearity among the independent variables and bivariate rela- tions between the independent variables and the de- pendent variable. The criterion to be met before any independent variable was considered for entry into an initial multivariable logistic regression model was a P-value of .25 or less obtained for each outcome var- iable in the univariate analysis and noncollinear with other predictors. Furthermore, the signicance level for 40 Vol. 36 No. 1 Abbate et al variables entering the logistic regression model was set at .2 and for removing from the model at .4. The mag- nitude of the association between predictors of interest and outcomes was measured by odds ratios (ORs) and their corresponding 95% condence intervals (CIs). When building linear regression model, we have rst included only one possible variable at a time. Then, us- ing the variables that were signicant at P-value #.25, we constructed a stepwise multivariate linear regres- sion model, and the signicance level for variables entry the model was set at .2 and for removal at .4. All tests were two-tailed and a P-value of .05 or less was dened as statistically signicant. The data were analyzed using the statistical software Stata. 6 RESULTS Of the 475 patients approached to participate in the study, a total of 450 agreed to be interviewed with an overall response rate of 94.7%. The distribution of rel- evant socio-demographic characteristics and selected information on hospital admissions and examinations of participants are summarized in Table 1. Overall, 57.8%of the patients interviewed were women, the av- erage age was 51 years (range 16-87), and one-third had some high school or higher level of education and were rst-time admitted in a hospital ward. Table 2 shows the distribution of patients who cor- rectly mentioned each of the possible hospital-associ- ated infections denition, incidence rate, risk groups, risk factors, and preventive measures. Only one third (35.1%) correctly dened hospital-associated infection as an infection acquired in hospital that was not pre- sent or incubating at the time of admission, whereas a large percentage of survey respondents agreed that elderly (89.6%), children (88.9%), and patients in sur- gical wards (75.8%) were at risk of contracting hospi- tal-associated infections. However, there were some misconceptions with respondents that overestimated the risk, because 43.8% believed that smokers were a risk group. Regarding the most likely causes of hospi- tal-associated infections, 97.1% identied poor hospi- tal hygiene, 59.1% extrinsic host factors such as invasive procedures or devices, and 48.4% the length of hospital stay. Moreover, only 12% of the respon- dents were able to indicate the incidence rate of hospi- tal-associated infections with a vast majority (77.1%) that overestimated the rate. To identify the independent effect of the variables on knowledge and others out- come of interest, we created several multivariate models, and Table 3 presents the results from the nal multiple logistic and linear regression analyses for which variables with an association of P # .25 at the univariate analysis were selected. After multivariate lo- gistic adjustments, the results suggest that, among all variables tested, several of these signicantly predicted the knowledge. Indeed, patients with higher educa- tional level (OR52.85; 95% CI 2.1-3.85), unmarried status (OR50.48; 95% CI 0.28-0.82), rst-time hospital admitted (OR50.38; 95% CI 0.23-0.64), and those who have received information about hospital-associated infections (OR54.01; 95% CI 2-8.05) were more likely to knowdenition, risk groups, and risk factors of such infections (Model 1 in Table 3). More than two thirds (68.9%) of the patients per- ceived that hospital-associated infections are serious, 88.2% that they are preventable, and 63.8% believed that health care professionals cannot infect patients. More than three fourths (79.8%) perceived some risk of contracting a hospital-associated infection, and the mean total score resulted of 4.7, with only 2.7% having reported feeling very much at risk by answering 10. A stepwise multivariate linear regression model Table 1. Socio-demographic characteristics and selected information on hospital admission and examinations of the study population n % Gender Female 260 57.8 Male 190 42.2 Age group (years) 50.8 6 18.6* #30 93 20.7 31-40 58 12.9 41-50 58 12.9 51-60 87 19.3 61-70 80 17.8 .70 74 16.4 Marital status Married 289 64.2 Single 86 19.1 Other 75 16.7 Educational level (years) ,5 58 12.9 5-7 73 16.2 8-12 169 37.5 13-17 124 27.6 .17 26 5.8 Occupational position Unemployed 286 63.5 Employed 164 36.5 First-time hospital admitted No 303 67.3 Yes 147 32.7 Number of surgical procedures already received 0 122 27.1 $1 328 72.9 Hospital ward General surgery 120 26.7 Specialist surgery 146 32.4 General medicine 100 22.2 Specialist medicine 84 18.7 Length of hospital stay (days) 6.2 6 9.9* *Mean 6 Standard deviation. Abbate et al February 2008 41 was constructed aiming at understanding which varia- bles had stronger associations with the perception of risk of contracting a hospital-associated infection by the patient. Respondents levels of perceived risk were signicantly higher in those married, unem- ployed, in medical wards, in those who overestimated the incidence rate of hospital-associated infections, and in those who believed that health care profes- sionals cannot infect patients (Model 3 in Table 3). Patients were asked whether or not they have a history of exposure to hospital-associated infections related to the level of compliance of health care workers with standard precautions. Of those surveyed, 71.1% reported that they have been exposed at least once to a health care worker who did not wear gloves when touching blood, body uids, mucous membranes or nonintact skin, and mask during procedures and pa- tient-care activities that may pose risk for contamina- tion by nasal and/or oral ora of the health care worker, and almost all of them(90.3%) did not say any- thing, whereas of those who have never been exposed, 30.8% reported that they would stop the health care worker if he/she started the activity without gloves and mask. Overall, 15.1% of the respondents stated that they were more willing to stop a health care worker who is not wearing gloves and mask. The results of the multivariate logistic regression analysis indicated that those patients willing to stop were females (OR52.39; 95% CI 1.28-4.47), higher educated (OR51.51; 95% CI 1.11-2.07), those who believed that health care professionals can infect patients (OR52.42; 95% CI 1.16-5.05), who overestimated the incidence rate (OR53.12; 95%CI 1.39-7.01), who have never been ex- posed to such infections (OR50.17; 95% CI 0.09-0.31), who have never had received information (OR50.46; 95% CI 0.23-0.9), and who do not need information about hospital-associated infections (OR50.39; 95% CI 0.19-0.83) (Model 2 in Table 3). The most common reasons reported by the respondents for not stopping a health care worker who is not wearing gloves and mask was the conviction that such behavior is not dangerous for them. When asked about the main sources of informa- tion, by which knowledge and awareness of hospital- associated infections was acquired, 68.7% of patients recorded that they had indeed received some informa- tion: the media were the most frequently mentioned (53.6%) andonly15.1%fromhealthprofessionals; how- ever, 86.9% of the patients required more information. DISCUSSION To the authors knowledge, this is the rst published survey that depicts a mosaic of opinions outlining the stated knowledge, attitudes, and self-reported behavior patterns concerning hospital-associated infections among a large random sample of patients in Italy. Despite the novelty and signicance level of these ndings, some methodological considerations ought to be highlighted when interpreting our results. First, all variables used in this analysis were gathered using patients self-reports and self-perceptions, and the pos- sibility exists that patients responses will give answers intended to please the interviewer rather than reect- ing the particular truth regarding the behavior in the case of exposure to the risk of hospital-associated infections. The problem with self-reporting is that par- ticipants responses may attempt intentionally or unin- tentionally to inate or minimize reports of behaviors. However, it has been demonstrated that means of im- proving the validity of self-report data include the as- surance of condentiality and establishment of good relationship. In our study, interviews were conducted in a condential setting, and interviews were carried out by interviewers trained for the task, which included the need to establish a good relationship. Second, the survey was conducted on admitted patients and it is possible that they underestimated risk perception, since they are selected among those who do not avoid health care services. Third, since the study was cross- sectional in design, there was no temporal separation of the explanatory variables from the outcomes, so that it was not possible to distinguish whether those variables preceded the outcome or vice versa. Despite the potential limitations, there were strong advantages of the present study. First, because the study was not conducted with volunteers but rather with a random sample, we believe that our results are representative of the patients in the area studied. Second, we were able to utilize a very large sample and the high Table 2. Knowledge about hospital-associated infections of the study population Correctly answered n % Denition 158 35.1 Incidence rate (5-8%) 54 12 Risk groups Elderly 403 89.6 Children 400 88.9 Patients in surgical wards 341 75.8 Risk factors Hospital hygiene 437 97.1 Health care worker behavior 408 90.7 Invasive procedures or devices 266 59.1 Length of hospital stay 218 48.4 Preventive measures Hospital hygiene 313 69.6 Health care worker behavior 135 30 Patient behavior 38 8.4 42 Vol. 36 No. 1 Abbate et al response rate excludes one major potential source of sample bias in the results. We believe that this high re- sponse rate was made possible through the extreme importance of the topic surveyed. Third, we have used the multivariable analysis that is essential for determining which are, among a number of factors, the most signicant predictors of an outcome. Fourth, the combination of quantitative and qualitative data provides a comprehensive picture of the overall knowl- edge, attitudes, and behaviors towards hospital-associ- ated infections. Most patients were condent about their knowledge of hospital-associated infections, and most recognized the well-known risk groups and risk factors for these infections, although it was also quite noteworthy that there are some misconceptions about risk groups and only one third of patients were able to provide the correct denition. The respondents to our question- naire exhibited similar levels of knowledge when com- pared with those reported in a previous survey conducted in France, because among the 65 surgical patients, only 26.2% were able to describe a nosoco- mial infection. 4 A higher value has been observed in 329 subjects selected from the general population in Germany with 66.9% that claimed to know about nos- ocomial infections. 7 When viewed from the perspec- tive of informed decision-making, patients who have misconceptions are clearly not in a position to play a role in the implementation of change in public health policy and infection control procedures, and such mis- conceptions can also impair the quality of communica- tion between clinicians and their patients more generally. Indeed, it is notable that in our study the main source of information through which awareness Table 3. Logistic and linear regression models results Variable OR SE 95% CI P Model 1. Knowledge (denition, risk groups, risk factors) about hospital-associated infections Log likelihood 5 2194.09, x 2 5 151.05 (7 df), P ,.0001 Information received about hospital-associated infections 4.01 1.43 2-8.05 ,.001 Educational level 2.85 0.44 2.1-3.85 ,.001 First-time hospital admitted 0.38 0.1 0.23-0.64 ,.001 Marital status 0.48 0.13 0.28-0.82 .007 Hospital ward 1.69 0.48 0.98-2.94 .06 Need of additional information about hospital-associated infections 1.74 0.68 0.8-3.76 .16 Gender 0.76 0.21 0.45-1.3 .32 Model 2. Willingness to stop a health care worker who is not wearing gloves and mask Log likelihood 5 2152.91, x 2 5 76.36 (9 df), P ,.0001 Exposed at least once to a health care worker who did not wear gloves and mask 0.17 0.05 0.09-0.31 ,.001 Knowledge of the incidence rate of hospital-associated infections: Correct* 1.0 - - - Overestimation 3.12 1.29 1.39-7.01 .006 Gender 2.39 0.76 1.28-4.47 .006 Educational level 1.51 0.24 1.11-2.07 .009 Need of additional information about hospital-associated infections 0.39 0.15 0.19-0.83 .014 Belief that health care professionals can infect patients 2.42 0.91 1.16-5.05 .019 Information received about hospital-associated infections 0.46 0.16 0.23-0.9 .023 Health professionals as source of information about hospital-associated infections 0.42 0.22 0.15-1.16 .09 Surgical procedures already received 1.68 0.61 0.83-3.42 .15 Variable Coeff. SE t P Model 3. Perception of risk of contracting a hospital-associated infection F(7,442) 5 16.77, P ,.0001, R 2 5 21%, adjusted R 2 5 19.7% Knowledge of the incidence rate of hospital-associated infections: Correct* - - - - Overestimation 1.14 0.28 4.05 ,.001 Belief that health care professionals can infect patients 21.38 0.25 25.46 ,.001 Hospital ward 20.67 0.26 22.61 .009 Marital status 0.53 0.24 2.16 .031 Occupational position 20.5 0.25 21.98 .048 Age 0.01 0.01 1.92 .055 Need of additional information about hospital-associated infections 0.64 0.34 1.87 .06 Constant 4.92 *Reference category. Abbate et al February 2008 43 was attained was the media and not by qualied health care representatives. We believe that although media campaigns may have a positive impact, they appear to have limited impact on long-term behavioral changes, thereby necessitating the implementation of educational and policy strategies. These ndings sug- gest that it is crucial for infection control professionals to disseminate information to patients in the context of routine medical care and this is also supported by our nding that health care workers are viewed by almost all respondents as useful resources that can be used to provide patient information and patient education. With regard to attitudes and opinions expressed dur- ing this survey, a vast majority of patients believe that hospital-associated infections are preventable, but the study discovered that more than three-quarters of re- spondents (79.8%) were worried about contracting such infections, and 2.7% said that they were very much concerned about this. In this scenario, whereby poor knowledge coexists with high perceived risk, one may argue that hospital-associated infections educa- tional programs are not needed, but also very likely to be welcomed. Results of this study agree with those of a previous mail survey conducted in the late 1980s in the United States, in that 83% of those responding believed that nosocomial infections were preventable, and 70% were concerned about their risk of acquiring such infections if future hospitalization was required. 3 A lower value was observed in Nigeria with 54% of the patients attending dental clinics felt they could con- tract an infection. 8 Data from our study suggest that, although 71.1% of the patients self-reported having had at least one expo- sure to hospital-associated infections related to the compliance of health care workers with standard pre- cautions, a large proportion did not say anything when the worker did not wear gloves, when touching blood, body uids, mucous membranes, or nonintact skin, and mask during procedures and patient-care activities that may pose risk for contamination by nasal and/or oral ora of the health care worker. The implication of this nding is that, despite increasedconcerns about the risk of hospital-associated infections, exposure continues to be frequent. Therefore, there is a special need to reinforce information to health care workers about personal and patients exposure and to follow standard precautions in order to prevent such infections. The results of the regression models, it is worth men- tioning, revealed that patient knowledge of hospital- associated infections signicantly inuences percep- tion of risk. Specically, patients who overestimate the incidence rate, perceived their own risk as signi- cantly higher than that of those more knowledgeable. Furthermore, it has been well established that worried individuals were, although not signicantly, more likely to seek more information. Such ndings suggest that patients would both welcome and benet from tools and strategies that would help reduce fear because it is important in whether or not they adhere to these procedures. It is also evident from the survey that the perception that health care workers can transmit a hospital-associated infection was related to precau- tionary behaviors among respondents. Those patients who have this perception were more likely to practice precautionary behaviors, because they were more will- ing to stop a health care worker who is not using gloves and face mask during the activity. In conclusion, our results indicate signicant oppor- tunities for improving current levels of knowledge about hospital-associated infections among the general public that it is crucial to the development and imple- mentation of effective public health preventive strate- gies. Close monitoring of the population-specic impacts of these interventions is required to assess the efcacy of these efforts. The authors would like to thank all patients who participated in the study. References 1. Sheng WH, Wang JT, Lu DCT, Chie WC, Chen YC, Chang SC. Com- parative impact of hospital-acquired infections on medical costs, length of hospital stay and outcome between community hospitals and medical centres. J Hosp Infect 2005;59:205-14. 2. Stone PW, Braccia D, Larson E. Systematic review of economic analyses of health care-associated infections. Am J Infect Control 2005;33:501-9. 3. Miller PJ, Farr BM. Survey of patients knowledge of nosocomial infec- tions. Am J Infect Control 1989;17:31-4. 4. Merle V, Van Rossem V, Tavolacci MP, Czernichow P. Knowledge and opinions of surgical patients regarding nosocomial infections. J Hosp Infect 2005;60:169-71. 5. Tuboku-Metzger J, Chiarello L, Sinkowitz-Cochran RL, Casano-Dicker- son A, Cardo D. Public attitudes and opinions toward physicians and dentists infected with bloodborne viruses: results of a national survey. Am J Infect Control 2005;33:299-303. 6. Stata Corporation. Stata Reference Manual Release 8.1. College Station, TX, USA, 2003. 7. Mattner F, Mattner C, Zhang I, Gastmeier P. Knowledge of nosocomial infections and multiresistant bacteria in the general population: results of a street interview. J Hosp Infect 2006;62:524-5. 8. Sofola OO, Uti OG, Onigbinde OO. Public perception of cross-infec- tion control in dentistry in Nigeria. Int Dent J 2005;55:383-7. 44 Vol. 36 No. 1 Abbate et al APPENDIX A Abbate et al February 2008 45 46 Vol. 36 No. 1 Abbate et al Abbate et al February 2008 47