Healthcare-associated infections in a tunisian university hospital: from analysis to action

Healthcare-associated infections in a tunisian university hospital: from analysis to action

 

Mohamed Mahjoub^1,&, Nebiha Bouafia¹, Waadia Bannour¹, Tasnim Masmoudi², Rym Bouriga³, Radhia Hellali¹, Asma Ben Cheikh¹, Olfa Ezzi¹, Amel Ben Abdeljellil¹, Njah Mansour¹

 

¹Hospital Hygiene Service, University Hospital Centre Farhat Hached, Sousse, Tunisia, ²Forensic Medical Service, University Hospital Centre Farhat Hached, Sousse Tunisia, ³Hematology Service, University Hospital Centre Farhat Hached, Sousse, Tunisia

 

 

^&Corresponding author
Mohamed Mahjoub, Hospital Hygiene Service, University Hospital Centre Farhat Hached, Sousse, Tunisia

 

 

 

 

Healthcare-associated infections (HAI) represent a universal public health problem due to their frequency, their seriousness and their additional cost. They increase hospital stay and engender morbidity and mortality with heavy economic and legal burden, everywhere in the world. It is certain that prevention of HAI is well organized in developed countries ; however, it is much less in countries with a low socio-economic level who suffer, in majority, from lack of legislations organizing prevention plans in addition to deficiencies of representative data that are essential for monitoring control actions [1, 2].

 

Epidemiological surveillance (ES) represents a central axe in any HAI prevention strategy. There are different methods of ES, especially prevalence surveys which constitute one of the most common methods adopted, in most countries, allowing follow of HAI’ frequency and epidemiological particularities’ evolution [3]. We have carried out our study, in 2012, at university hospital centre (UHC) Farhat Hached of Sousse, according to HAI ES program based on regular prevalence surveys that have started since 2000 in order to better direct prevention axes. Last investigation is dating back to 2007.

 

The aims of our study were, in a first time, to estimate HAI prevalence at our hospital and to describe HAI distribution according to anatomical sites, services at risk and germ types; then, in a second time, to identify risk factors associated with HAI occurrence, in order to reorient prevention strategies.

 

 

We have carried out our study at UHC Farhat Hached of Sousse which has a suburban structure with a medical vocation composed of 26 medical services, 4 surgical services and 9 laboratories. It is equipped with a hospital capacity regarding 698 beds, in 2012. Total staff practicing, at this hospital, is 1661; among them 1354 health professionals with different ranks: 1134 paramedics and 220 doctors. There is an operational hygiene team that defines hygiene policy and formalizes programs that will be adopted then achieved, at hospital. This team works in collaboration with hospital HAI control committee (HAICC). HAI’s control and prevention include training, awareness raising, monitoring and assessment of professional practices; and contribute to improvement of quality and safety care.

 

It is a descriptive transverse survey, conducted in 2012, over a period of 10 days including all patients who had been hospitalized for at least 48 hours, in 16 clinical services of our UHC which are: general surgery , ENT (Ear-nose-throat), ophthalmology, dermatology, hematology, rheumatology, pediatrics, cardiology, medical intensive care, anesthesia-reanimation, pneumology, gynecology (with high-risk and post-operative pregnancies), oncology, psychiatry, internal medicine and infectious diseases, and endocrinology. A single passage has been carried out by service. Criteria of Centers for Disease Control (CDC) Atlanta USA, Prevention National Nosocomial Infection Surveillance (NNIS) and National Healthcare Safety Network (NHSN) system, were used and adapted to our context to define HAI [4].

 

Study was performed using a questionnaire completed by the investigator in its passage by each service. Finished questionnaires have been daily validated to ensure data completeness. Main sources of data were patients’ medical records, treating physicians and hygiene referents of each service.

 

Variables measured were related to: patients’ general characteristics, clinical profiles, exposure to invasive devices or a surgical procedure and possible presence of one or several active HAI the day of survey. Data seizure and analysis were carried out anonymously, using software Epiinfo 6.0.

 

In order to identify HAI risk factors, we have proceeded by a uni-varied analysis comparing patients who have presented at least one HAI to those who do not have, in relation with different variables measured, using chi2 and student tests (t-test). Variables whose p<0.25 in uni-varied analysis have been included in a logistic regression model stepwise descending. Degree of significance was fixed at p<0.05 [5].

 

 

Descriptive results

 

Population characteristics

 

A total of 312 patients were observed at the day of survey. Patients’ median age was 47 years. 72.7% of patients were hospitalized in medical services (including 2.5 % hospitalized in intensive care unit) and 27.2% in surgical services. Diabetes (20.5%) and immunosuppression (20.5%) were main intrinsic risk factors found in patients included in the study, followed by obesity (16.7%). Peripheral venous catheter (PVC) was the most frequently encountered medical device (65.7%) followed by exposure to surgical procedure (15,7%) and urinary probe (9.6%).

 

Among the 49 operated patients, 17 have received a prophylactic antibiotic treatment, which corresponds to 34.7%. Thus, 10 patients (10/17) received a single antibiotic and 7 (7/17) have received a double antibiotherapy. Predominant prescribed prophylactic antibiotics were association of amoxicillin and clavulanic acid (664.7%), then Nitroimidazoles (41.1%).

 

Relatively to profile of patients undergoing surgery, 85.7% had an ASA grade of 1 or 2; and 81.6% were operated for a clean or clean-contaminated surgery; and intervention duration was less than 2 hours in 83.7%. In addition, NNIS grade was equal to 0 or 1 in 83.7% of patients; lastly, only 77.66% of the operated were programmed.

 

Characteristics of healthcare-associated infections

 

Among a total of 312 patients included in this study, 39 have submitted at least one HAI which corresponds to a prevalence rate of 12.5% (CI 95% (0.08 -0.16)). HAI number identified in these patients is 45, meaning a prevalence rate of 14.4% (CI 95% (0.10 - 0.18)). Among these 39 patients with HAI, 22 were hospitalized in medical services (56.4 %) and 17 were hospitalized in surgical services (43.66%). Calculation of infected patients’ prevalence rate by service has helped to identify HAI high risk services where HAI prevalence rate varied between 12% and 45%. These services were: hematology, general surgery, medical intensive care unit, gynecology-obstetrics/maternity, ENT and pneumonology.

 

According to infection site, infections on PVC were predominant (42.2%) followed by respiratory infections (15.6%), then ENT infections (13.4%). Among these 45 HAI detected, 13 microbiological samples have been done representing only 28.8% of the HAI identified; 6 samples were positive (HAI bacteriologically documented), 4 of them to negative Gram Bacilli (NGB).

 

Analytical results

 

We proceeded with a uni-varied analysis comparing infected patients to those not infected according to their general characteristics and clinical profile, at admission. Among factors related to patient, only neutropenia frequency is revealed significantly higher beyond those having presented a HAI, against those who did not have it (Table 1). As for invasive care exposure, our study showed that PVC exposure frequency was significantly higher in infected patients (Table 2). Subsequent to multivariate analysis, three variables have been proved as independent risk factors of HAI occurrence, as to know: PVC, gastric tube and neutropenia (Table 3).

 

 

Prevalence surveys constitute the best monitoring method in several countries, especially when there is lack of mechanisms assuring continuous HAI monitoring [6]. They were even recommended by World Health Organisation for national or international studies, allowing estimation of problem’s magnitude and definition of actions’ priority [7]. In fact, this type of survey, has the advantage of being simple and less costly compared to other methods of surveillance. In addition, it has an advantage of providing quick information for an immediate reaction. It, also, able staff to be aware of risks related to HAI. Moreover, distribution of these investigations at a regular interval, allows us to measure secular trends and to assess global impact of prevention policy.

 

Discussion of results

 

Our investigation revealed an infected patients’ prevalence of 12.5% and a HAI prevalence of 14.5%. This figure is at the same range of rates published in literature. In fact, a number of studies, conducted in different countries, found prevalence rates that vary between 3.3% and 19.9%. Indeed, in United Kingdom HAI prevalence has decreased between 1994 et 2006 from 9% to 7,59 % [8, 9]. This prevalence, in 1996, was 5.9% in Greece [10] and 3.5% in Germany [11]. In France HAI prevalence has changed between 1996 and 2007 from 6.7% to 3.3% [12- 14]. It was in Norveege 6.1% in 1997 [15] and 6,8% in 2005 [16], it was 8% in Denmark in 1999 [17], 4,6% in Slovenia in 2001 [18] and 6,9% in Indonesia in 2002 [19]. HAI prevalence has a regressing tendency in Algeria in 1993, 2001 and 2005 it went respectively from 16,2% [20] to 9,8% then to 4% [21]. In Morocco HAI prevalence was 6,7% in 2005 [22]. In Tunisia, HAI prevalence has regressed between 1999 and 2005 from 14,1% [23] to 6,9% [24] then it has increased and reached 13%, in 2006 [25]. Finally, HAI prevalence was in Senegal 10,9% in 2007 [26].

 

In developed countries, reported records in literature are, commonly, considerably lower than in our survey. In fact, comparison is difficult because of methodological differences. These disparities concern criteria for HAI definition, mode of data collection, number of infective site investigated, as well as type of hospital activity or service size studied [27, 28]. Quenon clarified that rates comparison could only be worthwhile if similar methodologies have been adopted [29]. Multi-centric study conducted in 27 hospitals in Mediterranean region, in 2010, involving 4634 patients, has recorded a HAI prevalence of 10.5 % [6].

 

At Tunisian national level, HAI prevalence was significantly lower than that found in our study [24]. However, at a regional level, when comparing results with other Tunisian hospitals, we noted different rates. That can be explained by deficiency of national strategy to prevent HAI, and additionally by lack of standardized prevention methodology.

 

In literature, nature of service activities contributed to HAI occurrence. Indeed, the highest rate of HAI prevalence was noted in intensive care service [6, 11, 18, 24, 30], as our results revealed. Reasons for that could be attributed to diseases severity, patients’ hospitalization lengthiness and more frequent indications of invasive therapeutic or diagnostic acts [6, 31].

 

Risk of developing a HAI depends on a number of factors widely described in studies conducted everywhere in the world [4]. Regarding to age and gender, same as a study conducted at UHC Hassan II of Fes, our study has not revealed a significant association between HAI occurrence and these factors, despite a female predominance of 66.7% (p= 0.18) [22]. However, investigations results carried out in Turkey [32], Slovenia [18] and in Albania [33] had objected a significant predominance of HAI among men. As well, it is proved that diabetes and obesity promote occurrence of respiratory and surgical site infections [34, 35]. NosoTun study in Tunisia showed a statistically significant association between HAI prevalence and diabetes (p=0,009), malnutrition (p<10^-4), immunosuppression and neutropenia (p<10-4) [24]. According to mainstream studies, immunosuppression has been recognized as a predisposing factor to HAI [13, 34, 36-39]. Other studies, as ours, did not note association between this factor and HAI [40, 41]. This could be attributed to better healthcare quality delivered to these patients since their admission. Nevertheless, presence of patients’ classification bias, due to different diagnostic criteria could not be formally eliminated in such study. In fact, neutropenia which can be regarded as a good indicator of immunosuppression has been identified as significant HAI risk factor in our study (OR= 10.28 (IC95% (3.00 - 35.17)) and p< 10^-4). According to Lass-Florl, neutropenia (<500 white elements /mm3) is a significant HAI risk factor in blood-oncology services of Austria [42]. This factor is also linked to HAI bacteraemia [34, 37, 43].

 

Many extrinsic risk factors may take part in genesis of HAI. Unfortunately, more than half (65.7%) of our patients, were exposed to PVC. Also, results of multi-varied analysis notified that risk of developing a HAI is multiplied by 3.48 when patients are exposed to PVC (OD = 3.48 (1.29 - 9.37)). These results concord with those of a prevalence survey conducted in Morocco [44].  Several other studies have shown that central and peripheral catheters are potential risks factors of HAI occurrence [15, 35, 36, 39, 40, 45, 46]. Frequently, venous catheters devices give often local infections; moreover, central venous catheters are involved in 90% of bacteraemia [46]. Infection on catheter is, in fact, a matter of its installation quality, maintenance care and ablation delay [34, 45-47].

 

Although, 15.7% of our patients were exposed to a surgical intervention, proportion of operatory site infection (OSI) was low, about 4.4% (2 OSI on 49 surgery); this could be explained by patients clinical profile; more than 80% had a score NNIS equal to 0 or 1. Generally, association between exposure to a surgical intervention and HAI occurrence (regardless of anatomical site) was not regularly established [10, 11, 36-38].  Furthermore, 34.7% of our patients have received a prophylactic antibiotic treatment; the most frequently prescribed antibiotics were association of amoxicillin and clavulanic acid (64.7 %) followed by Nitroimidazoles (41.1 %), as reported in literature [27]. Association between parenteral feeding and HAI occurrence has been demonstrated in a Mexican study [48]; this association could not be tested in our study because of exposed patients’ few number.  Multi-varied analysis have revealed that gastric tube is an independent risk factor of HAI occurrence (OR= 5.17 (IC95% (1.13 - 23.68)); p= 0.03). In this same sense, a study carried out at Fann university hospital has confirmed association between gastric tube and pulmonary HAI’ occurrence [26].

 

Comparison of HAI distribution according to anatomical site, between countries and even between establishments of the same country, must consider type of institution activities on one hand, and on the other methodology of data collection, such as: adopted definitions, compendium completeness, study period and investigators expertise [49]. Nevertheless, our study revealed a high proportion of vascular infection particularly on PVC about 42.2 %, a result far higher than that was reported in literature; indeed, NosoTun investigation in Tunisia revealed only 8.6 % of infections on PVC [24]. These infections deemed preventable in more than one third of cases, unless hygiene rules compliance when installing, manipulating and removing PVC. These infections should managed by a specific prevention action strategy.  Microbiological documentation has been the main limitation of our study, since that among the 45 HAI found, only 13 samples have been carried out, among them 6 are returned positive, predominantly to NGB. Predominance of NGB in HAI is common to most of studies, despite variability of bacterial species from one country to another [12, 22, 24].

 

Prevention strategy

 

Considering HAI preventive methods, leads us to discuss these infections avoidability and interventions efficacy on their risk factors. As known, approximately one third of HAI is avoidable, regarding results of NNIS survey dating from some thirty years [50]. Besides, HAI prevention should take part of a risk management program including prevention axes which are defined periodically and previously by hospital HAI control committee. Further, establishment of an ES system at hospital, targeting services at risk, is widely recommended. HAI prevention program includes, relating to health-carers: information and awareness, continues training, insisting on action priorities and evaluation of professional practices. These measures are effective when grouped together within the same global strategy recognized under the name of bundle.

 

 

Ultimately, at our hospital, there is a predominance of infections related to PVC, even though they are judged in majority of cases as avoidable HAI. That is why they should be managed with a specific prevention strategy, in which many approaches are included. They are, mainly: retro information of results to each service in order to raise awareness of problem magnitude; prospective ES of infections related to PVC; and finally, evaluation of professional practices in the field of PVC installation, maintenance and withdrawal. Implication of health professionals gets better, by encouraging their commitment and adherence to hygiene measures, as well as, by developing patient safety’s culture, which guarantees the best HAI prevention. Elsewhere, prospective studies are desirable in order to describe more accurately incidence as risk factors in each context.

 

 

The authors declare no competing interest.

 

 

MOHAMED MAHJOUB : substantial contributions to conception and design, acquisition of data, analysis and interpretation of data; drafting the article and revising it critically for important intellectual content; Final approval of the version to be published. NEBIHA BOUAFIA : substantial contributions to conception and design, acquisition of data, analysis and interpretation of data; drafting the article and revising it critically for important intellectual content; final approval of the version to be published. WAADIA BANNOUR : substantial contributions to conception and design, acquisition of data; drafting the article and revising it critically for important intellectual content. TASNIM MASMOUDI : drafting the article and revising it critically for important intellectual content; final approval of the version to be published. RYM BOURIGA : substantial contributions to conception and design, acquisition of data, analysis and interpretation of data; drafting the article revising it critically for important intellectual content. RADHIA HELLALI : final approval of the version to be published. ASMA BEN CHEIKH : final approval of the version to be published. OLFA EZZI : final approval of the version to be published. AMEL BEN ABDELJELLIL : final approval of the version to be published. NJAH MANSOUR : final approval of the version to be published. All authors read and agreed to the final version of this manuscript and equally contributed to its content and to the management of the case.

 

 

Table 1: comparison according to general characteristics and clinical profile of patients (N= 312)

Table 2: comparison depending on exposure to invasive care (N= 312)

Table 3: independent risk factors of HAI

 

 

1. Bailly P, Haore HG, Crenn D, Talon D. Mortalité hospitalière imputable aux infections nosocomiales: mise en place d’un observatoire dans un centre hospitalier universitaire. Médecine et maladies infectieuses. 2004;34(2):76-82. PubMed | Google Scholar


2. Vosylius S, Sipylaite J, Ivaskevicius J. Intensive care unit acquired infection: a prevalence and impact on morbidity and mortality. Acta anaesthesiologica scandinavica. 2003;47(9):1132-7. PubMed | Google Scholar


3. Hygie V. Hygiène hospitalière : manuel de lutte contre les infections nosocomiales. 1988. Edition La Madeleine: Crouan et Roques. PubMed | Google Scholar


4. Allegranzi B, Nejad SB, Combescure C, Graafmans W, Attar H, Donaldson L, et al. Burden of endemic health-care-associated infection in developing countries: systematic review and meta-analysis. The Lancet. 2011;377(9761):228-41. PubMed | Google Scholar


5. Falissard Bruno. Comprendre et utiliser les statistiques dans les sciences de la vie. 200 3ème edition. Paris. Masson. Google Scholar


6. Amazian K, Rossello J, Castella A, Sekkat S, Terzaki S, Dhidah L, et al. Prévalence des infections nosocomiales dans 27 hôpitaux de la région méditerranéenne. Eastern Mediterranean Health Journal. 2010;16(10). PubMed | Google Scholar


7. Avril J, Donnio P. Surveillance of nosocomial infections. La Revue du praticien. 1989;39(16):1381-5. PubMed | Google Scholar


8. Emmerson A, Enstone J, Griffin M, Kelsey M, Smyth E. The Second National Prevalence Survey of infection in hospitals—overview of the results. Journal of hospital infection. 1996;32(3):175-90. PubMed | Google Scholar


9. Smyth E, McIlvenny G, Enstone J, Emmerson A, Humphreys H, Fitzpatrick F, et al. Hospital infection society prevalence survey steering group: four country healthcare associated infection prevalence survey 2006: overview of the results. Journal of Hospital Infection. 2008;69:230-48. PubMed | Google Scholar


10. Gikas A, Pediaditis I, Roumbelaki M, Troulakis G, Romanos J, Tselentis Y. Repeated multi-centre prevalence surveys of hospital-acquired infection in Greek hospitals: CICNet (Cretan Infection Control Network). The Journal of hospital infection. 1999 Jan;41(1):11-8. PubMed | Google Scholar


11. Gastmeier P, Kampf G, Wischnewski N, Hauer T, Schulgen G, Schumacher M et al. Prevalence of nosocomial infections in representative German hospitals. Journal of Hospital infection. 1998;38(1):37-49. PubMed | Google Scholar


12. Carlet J. L'infection nosocomiale sous surveillance. Lettre de l'infectiologue. 2002; XVII(7):199-200. PubMed | Google Scholar


13. Floret N, Bailly P, Bertrand X, Claude B, Louis-Martinet C, Picard A, et al. Results from a four-year study on the prevalence of nosocomial infections in Franche-Comté: attempt to rank the risk of nosocomial infection. Journal of Hospital Infection. 2006;63(4):393-8. PubMed | Google Scholar


14. Institut de Veille Sanitaire (InVS) CClin Est, CClin Ouest, CClin Paris-Nord, CClin Sud-Est, CClin Sud-Ouest. Enquête nationale de prévalence des infections nosocomiales 2006 : Résultats préliminaires au 12.01.2007. 2007. http://www.invs.sante.fr/publications/2007/enp2006_resultats_preliminaires/enp_2006_synthese.pdf. Consulté le 02.03.2015. Google Scholar


15. Scheel O, Stormark M. National prevalence survey on hospital infections in Norway. Journal of hospital infection. 1999;41(4):331-5. PubMed | Google Scholar


16. Nilsen R, Dalheim A, Harthug S. FP3 05 Trends and Predictors of Nosocomial Infections in a Large Norwegian Hospital. Journal of Hospital Infection. 2006;64:S7. PubMed | Google Scholar


17. Christensen M, Jepsen O. Reduced rates of hospital-acquired UTI inmedical patients: prevalence surveys indicate effect of active infection control programmes. Journal of Hospital Infection. 2001;47(1):36-40. PubMed | Google Scholar


18. Klavs I, Lužnik TB, Škerl M, Grgic-Vitek M, Zupanc TL, Dolinšek M, et al. Prevalance of and risk factors for hospital-acquired infections in Slovenia-results of the first national survey, 2001. Journal of hospital infection. 2003;54(2):149-57. PubMed | Google Scholar


19. Duerink D, Roeshadi D, Wahjono H, Lestari ES, Hadi U, Wille J et al. Surveillance of healthcare-associated infections in Indonesian hospitals. Journal of Hospital Infection. 2006;62(2):219-29. PubMed | Google Scholar


20. Bezzaoucha A, Makhlouf F, Dekkar N, Lamdjadani N. Prévalence des infections nosocomiales au centre hospitalo-universitaire de Bab El Oued-Alger. Médecine et maladies Infectieuses. 1994;24(2):96-101. PubMed | Google Scholar


21. Atif M-L, Bezzaoucha A, Mesbah S, Djellato S, Boubechou N, Bellouni R. Évolution de la prévalence des infections nosocomiales dans un centre hospitalier universitaire en Algérie (2001 à 2005). Médecine et maladies infectieuses. 2006;36(8):423-8. PubMed | Google Scholar


22. El Rhazi K, Elfakir S, Berraho M, Tachfouti N, Serhier Z, Kanjaa C, et al. Prévalence et facteurs de risque des infections nosocomiales au CHU Hassan II de Fès (Maroc). Eastern Mediterranean Health Journal. 2007;13(1):56. PubMed | Google Scholar


23. Ennigrou S, Ben Redjeb S, Zouari B. Prévalence des infections nosocomiales à l'hôpital Charles-Nicolle de Tunis. Tunisie médicale. 1999;77(3):127-33. PubMed | Google Scholar


24. Annabi Attia T, Dhidah L, Hamza R, Kibech M, Lepoutre-Toulemon A. Première enquête nationale tunisienne de prévalence de l’infection nosocomiale: principaux résultats. Hygiènes. 2007;15:144-9. PubMed | Google Scholar


25. Dridi E, Chetoui A, Zaoui A. Prévalence de l'infection nosocomiale dans un hôpital régional tunisien. Santé publique. 2006;18(2):187-94. PubMed | Google Scholar


26. Dia N, Ka R, Dieng C, Diagne R, Dia M, Fortes L, et al. Résultats de l’enquête de prévalence des infections nosocomiales au CHNU de Fann (Dakar, Sénégal). Médecine et maladies infectieuses. 2008;38(5):270-4. PubMed | Google Scholar


27. Malvy D, Sirvain A, Bortel H, Drucker J. Enquête de prévalence des infections nosocomiales au CHU de Tours / Seconde partie: résultats-Discussion. Médecine et maladies infectieuses. 1993;23(8):607-19. PubMed | Google Scholar


28. Leth R, Moller J. Surveillance of hospital-acquired infections based on electronic hospital registries. Journal of Hospital Infection. 2006;62(1):71-9. PubMed | Google Scholar


29. Quenon J, Brücker G. Enquête de prévalence des infections nosocomiales. Les infections nosocomiales et leur prévention. 1998. Paris. Ellipses. Pages : 62-77. PubMed | Google Scholar


30. Comité technique national des infections nosocomiales, CIN, CCLIN Est, CCLIN Ouest, CCLIN Paris-Nord, CCLIN Sud-Est, CCLIN Sud-Ouest, avec la participation de 830 établissements de santé. Enquête nationale de prévalence des infections nosocomiales 1996. 1996. (Bulletin épidémiologique Hebdomadaire du 02 septembre 1997 Numéro : 36/1997.) (http://www.invs.sante.fr/beh/1997/9736/beh_36_1997.pdf). Consulté le 02.03.2015. Google Scholar


31. Sligl W, Taylor G, Brindley PG. Five years of nosocomial Gram-negative bacteremia in a general intensive care unit: epidemiology, antimicrobial susceptibility patterns, and outcomes. International journal of infectious diseases. 2006;10(4):320-5. PubMed | Google Scholar


32. Metintas S, Akgun Y, Durmaz G, Kalyoncu C. Prevalence and characteristics of nosocomial infections in a Turkish university hospital. American journal of infection control. 2004;32(7):409-13. PubMed | Google Scholar


33. Faria S, Sodano L, Gjata A, Dauri M, Sabato A, Bilaj A et al. The first prevalence survey of nosocomial infections in the University Hospital Centre ‘Mother Teresa’ of Tirana, Albania. Journal of Hospital Infection. 2007;65(3):244-50. PubMed | Google Scholar


34. Ogeer-Gyles JS, Mathews KA, Boerlin P. Nosocomial infections and antimicrobial resistance in critical care medicine. Journal of Veterinary Emergency and Critical Care. 2006;16(1):1-18. PubMed | Google Scholar


35. Pittet D, Allegranzi B, Storr J, Donaldson L. ‘Clean care is safer care’: the global patient safety challenge 2005–2006. International Journal of Infectious Diseases. 2006;10(6):419-24. PubMed | Google Scholar


36. Maugat S, Carbonne A, Astagneau P. Réduction significative des infections nosocomiales: analyse stratifiée des enquêtes nationales de prévalence conduites en 1996 et 2001 dans l’inter-région Nord. Pathologie Biologie. 2003;51(8):483-9. PubMed | Google Scholar


37. Branger B. Enquête de prévalence nationale 2001 des infections nosocomiales chez les nouveau-nés et des enfants et adolescents de moins de 18 ans. Archives de pédiatrie. 2005;12(7):1085-93. PubMed | Google Scholar


38. Michalopoulos A, Geroulanos S, Rosmarakis ES, Falagas ME. Frequency, characteristics, and predictors of microbiologically documented nosocomial infections after cardiac surgery. European journal of cardio-thoracic surgery. 2006;29(4):456-60. PubMed | Google Scholar


39. Kenny H, Lawson E. The efficacy of cotton cover gowns in reducing infection in nursing neutropenic patients: An evidence-based study. International journal of nursing practice. 2000;6(3):135-9. PubMed | Google Scholar


40. Appelgren P, Hellström I, Weitzberg E, Söderlund V, Bindslev L, Ransjö U. Risk factors for nosocomial intensive care infection: a long-term prospective analysis. Acta anaesthesiologica scandinavica. 2001;45(6):710-9. PubMed | Google Scholar


41. Girard R, Mazoyer M, Plauchu M, Rode G. High prevalence of nosocomial infections in rehabilitation units accounted for by urinary tract infections in patients with spinal cord injury. Journal of hospital infection. 2006;62(4):473-9. PubMed | Google Scholar


42. Lass-Flörl C, Griff K, Mayr A, Petzer A, Gastl G, Bonatti H et al. Epidemiology and outcome of infections due to Aspergillus terreus: 10-year single centre experience. British journal of haematology. 2005;131(2):201-7. PubMed | Google Scholar


43. Timmers GJ, Van Der Zwet WC, Simoons-Smit IM, Savelkoul PH, Meester HH, Vandenbroucke-Grauls CM et al. Outbreak of vancomycin?resistant Enterococcus faecium in a haematology unit: risk factor assessment and successful control of the epidemic. British journal of haematology. 2002;116(4):826-33. PubMed | Google Scholar


44. Hassoune S, Nani S, El Menzhi O. Prévalence des infections nosocomiales dans les hôpitaux préfectoraux de la région du Grand Casablanca. Hygiènes. 2010/05;XVIII(3):209-213. PubMed | Google Scholar


45. Dettenkofer M, Wilson C, Ebner W, Norgauer J, Rüden H, Daschner F. Surveillance of nosocomial infections in dermatology patients in a German university hospital. British Journal of Dermatology. 2003;149(3):620-3. PubMed | Google Scholar


46. Bosseray A, Micoud M. Infections nosocomiales. EMC 8-001-F-10, 2000. Google Scholar


47. Çelik SA. Nosocomial infections in neurosurgery intensive care units. Journal of clinical nursing. 2004;13(6):741-7. PubMed | Google Scholar


48. Sánchez-Velázquez LD, de León Rosales SP, Frausto MSR. The burden of nosocomial infection in the intensive care unit: effects on organ failure, mortality and costs (A nested case-control study). Archives of medical research. 2006;37(3):370-5. PubMed | Google Scholar


49. Sartor C, Sambuc R, Bimar M, Gulian C, De Micco P. Enquêtes de prévalence sur les infections nosocomiales à l'Assistance Publique de Marseille en 1992: méthodologie. Médecine et Maladies Infectieuses. 1995;25(2):121-6. PubMed | Google Scholar


50. Haley RW, Culver DH, White JW, Morgan WM, Emori TG, Munn VP, et al. The efficacy oe infection surveillance and control programs in preventing nosocomial infections in us hospitals. American journal of epidemiology. 1985;121(2):182-205. PubMed | Google Scholar