View of Influenza outbreak in patients and healthcare professionals of the Jesenice General Hospital in 2017

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1 National Laboratory of Health, Environment and Food, Maribor, Slovenia

2 National Institute of Public Health, Ljubljana, Slovenia

3 Community health centre Kranj, Kranj, Slovenia

4 Jesenice General Hospital, Jesenice, Slovenia

Correspondence/

Korespondenca:

Irena Grmek Košnik, e:

irena.grmek.kosnik@nlzoh.

si

Key words:

flu; influenza; outbreak;

hospital Ključne besede:

gripa; influenca; izbruh;

bolnišnica

Received: 28. 9. 2018 Accepted: 28. 8. 2019

en article-lang

10.6016/ZdravVestn.2877 doi

28.9.2018 date-received

28.8.2019 date-accepted

Microbiology and immunology Mikrobiologija in imunologija discipline

Original scientific article Izvirni znanstveni članek article-type

Influenza outbreak in patients and healthcare professionals of the Jesenice General Hospital in 2017

Izbruh gripe v Splošni bolnišnici Jesenice v letu 2017 pri bolnikih in zdravstvenih delavcih

article-title

Influenza outbreak in patients and healthcare professionals of the Jesenice General Hospital in 2017

Izbruh gripe v Splošni bolnišnici Jesenice v letu 2017 pri bolnikih in zdravstvenih delavcih

alt-title

flu, influenza, outbreak, hospital gripa, influenca, izbruh, bolnišnica kwd-group The authors declare that there are no conflicts

of interest present. Avtorji so izjavili, da ne obstajajo nobeni

konkurenčni interesi. conflict

year volume first month last month first page last page

2019 88 11 12 517 528

name surname aff email

Irena Grmek Košnik 1 irena.grmek.kosnik@nlzoh.si

name surname aff

Edita Eberl Gregorič 1

Helena Ribič 1

Monika Ribnikar 2

Kristina Orožen 2

Jana Lavtižar 3

Matej Dolenc 4

Janez Poklukar 4

Maja Sočan 2

eng slo aff-id

National Laboratory of Health, Environment and Food, Maribor, Slovenia

Nacionalni laboratorij za zdravje, okolje in hrano, Maribor, Slovenija

1

National Institute of Public

Health, Ljubljana, Slovenia Nacionalni inštitut za javno

zdravje, Ljubljana, Slovenija 2 Community health centre Kranj,

Kranj, Slovenia Zdravstveni dom kranj, Kranj,

Slovenija 3

Jesenice General Hospital,

Jesenice, Slovenia Splošna bolnišnica Jesenice,

Jesenice, Slovenija 4

Influenza outbreak in patients and

healthcare professionals of the Jesenice General Hospital in 2017

Izbruh gripe v Splošni bolnišnici Jesenice v letu 2017 pri bolnikih in zdravstvenih delavcih

Irena Grmek Košnik,¹ Edita Eberl Gregorič,¹ Helena Ribič,¹ Monika Ribnikar,² Kristina Orožen,² Jana Lavtižar,³ Matej Dolenc,⁴ Janez Poklukar,⁴ Maja Sočan²

Abstract

Background: Influenza is a seasonal viral respiratory disease that occurs during winter months.

It is caused by type A and type B influenza viruses. Influenza outbreaks in hospitals are particularly unfavourable as it is the vulnerable population that falls ill. Many complications occur, hospital treatment is prolonged and mortality increases. Healthcare professionals (HP) may also become ill and because of their absenteeism problems arise in the organization of work.

Methods: We present a retrospective cohort study of an influenza outbreak in a General Hos- pital Jesenice which occurred in a period from 1 January to 16 February 2017. A case definition was as follows: A patient or a healthcare professional (HP) who had signs of influenza-like illness (fever above 37.77 °C with coughing or sore throat) in the absence of other causes of infection and either influenza A or B virus confirmed in the nasopharyngeal swab, or in whom an epidemiological link with a confirmed case (hospitalisation in the same room) was established. Patients who developed these symptoms and signs 72 hours or later after admission were classified as nosocomial cases. We asked the affected HP about demographic data, any previous vaccination against influenza, and their subjective assessment of the severity of the disease.

Results: Of the approximately 250 exposed people, 117 (46.8%) fell ill. The first cases occurred in the internal medicine department, followed by the surgical and nursing departments. The ma- jority of patients were aged 65 and over. We took nasopharyngeal swabs from 74 patients and employees who complied with the definition of a case in the outbreak. Influenza A (87%) or B (13%) was confirmed in 68 (87%) samples. The remaining 49 cases that were not laboratory-confirmed have met the epidemiological link criteria. In the discharge letters of all 13 deceased patients one of the discharge diagnoses was influenza, while in four it was also listed as the direct cause of death. Six patients died of pneumonia that followed the flu. Forty-five patients received oseltamivir, 61 hospitalized patients, and HP took oseltamivir as chemoprophylaxis. The outbreak of influenza had an adverse effect on the work plan of the surgical department - due to the outbreak, the number of elective surgeries decreased and a part of the surgical beds were allocated to the overburdened internist department.

Conclusion: At an early stage of an outbreak in a hospital, a high degree of compliance with pre- ventive measures is required. Patients’ comorbidities and poor general condition contribute to more severe clinical presentation of influenza. Problems in ensuring isolation, non-compliance with the recommendations for personal hygiene of patients, non-vaccination against influenza and poor response of the immune system of elderly patients to vaccination contribute to outbreaks.

Slovenian Medical

Journal

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1 Introduction

Influenza affects 5–15% of the world’s population each year, causing 250,000 to 500,000 deaths; it is a seasonal viral respiratory disease that occurs in the winter months and is caused by influenza viruses of type A and type B. Influenza seasons vary in severity and are the result of the Izvleček

Izhodišče: Gripa je sezonska virusna bolezen dihal, ki se pojavlja v zimskih mesecih. Povzročajo jo virusi influence tipa A in B. Izbruhi gripe v bolnišnicah so posebno neugodni, saj zboli ranljiva populacija. Pojavijo se številni zapleti, podaljša se bolnišnično zdravljenje, poveča se umrljivost.

Hkrati lahko zbolijo tudi zdravstveni delavci (ZD). Zaradi njihovega absentizma se pojavijo težave pri organizaciji dela.

Metode: Izvedli smo retrospektivno kohortno preiskavo izbruha gripe v Splošni bolnišnici Jesenice (SBJ), ki smo ga zaznali v januarju 2017. Kot primer izbruha je bil opredeljen vsak bolnik ali zaposleni (ZD) v SBJ, ki je od 01. 01. 2017 do 16. 02. 2017 imel simptome gripi podobne bolezni (temperaturo nad 37,7 °C s kašljanjem ali bolečinami v žrelu), v brisu nosno-žrelnega prostora potrjen virus influence A ali B ali epidemiološko povezavo s potrjenimi primeri (hospitalizacija v isti sobi) ter odsotnosti ostalih vzrokov za okužbo. Primer smo opredelili kot bolnišničen pri os- ebah, ki so bile v bolnišnico sprejete zaradi drugih vzrokov in pri katerih so se simptomi in znaki v dihalih razvili kasneje kot 72 ur po sprejemu. Obolele zdravstvene delavce smo spraševali o demografskih podatkih, predhodnem cepljenju proti gripi in o subjektivni oceni poteka bolezni.

Rezultati: Med 250 izpostavljenimi je zbolelo 117 oseb (46,8 %). Primeri obolelih so se najprej začeli kopičiti na internem oddelku, sledil je kirurški in negovalni oddelek SBJ. Največ zbolelih je bilo starejših od 65 let. Pri 74 zbolelih bolnikih in zaposlenih, ki so ustrezali definiciji primera v izbruhu, smo odvzeli brise nosno-žrelnega prostora. V 68 (87 %) vzorcih smo dokazali influenco A (87 %) ali B (13 %). Ostalih 49 zbolelih, ki niso bili laboratorijsko potrjeni, so zadostili merilu epidemiološke povezanosti. Ob pregledu dokumentacije 13 umrlih bolnikov smo ugotovili, da je bila pri vseh ena od diagnoz gripa, pri 4 od njih tudi navedena kot neposredni vzrok smrti. 6 umrlih bolnikov je prebolevalo pljučnico, ki je sledila gripi. 45 zbolelih je prejelo oseltamivir, 61 hospitaliziranih oseb in ZD pa je jemalo oseltamivir kot kemoprofilakso. Izbruh gripe je neugod- no vplival na načrtovano delo kirurškega oddelka – zaradi izbruha so v bolnišnici zmanjšali šte- vilo elektivnih operacij, del kirurških postelj pa so namenili preobremenjenemu internističnemu oddelku.

Zaključek: V zgodnji fazi izbruha gripe v bolnišnici je potrebna visoka stopnja upoštevanja pre- ventivnih ukrepov. K zbolevanju bolnikov namreč prispevajo predhodne bolezni in slabo zdravst- veno stanje, težave pri zagotavljanju izolacije, neupoštevanje priporočil za osebno higieno, nece- pljenost proti gripi in slaba odzivnost imunskega sistema starejših bolnikov na cepljenje.

Cite as/Citirajte kot: Grmek Košnik I, Eberl Gregorič E, Ribič H, Ribnikar M, Orožen K, Lavtižar J, et al.

Influenza outbreak in patients and healthcare professionals of the Jesenice General Hospital in 2017. Zdrav Vestn. 2019;88(11–12):517–28.

DOI: https://doi.org/10.6016/ZdravVestn.2877

constant change of influenza viruses to which the population isn’t resistant (1). In a hospital setting where the virus comes through healthcare professionals, patients, relatives and other people who come into contact with patients, it poses an important problem as it increases patient mor-

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bidity and mortality, thereby incurring additional treatment costs. The reason for this is, in addition to the flu itself, secondary bacterial infections and exacerbation of the underlying disease, which triggers the use of additional drugs (e.g. antibiot- ics, antiviral drugs) and prolonged hospital stay (2). Due to the employees getting the flu, their absence and related problems in the organization of performing regular work and tasks increase.

As an outbreak of influenza we regard two or more cases (patients or employees) with symptoms and signs of acute respiratory infection over a period of 72 hours that are epidemiologically related, with the influenza virus being laboratory confirmed in at least one case. Epidemi- ologically, we report any person with influenza-like illness and at least one of the symptoms, such as fever, malaise, head- ache, muscle aches, and at least one of the respiratory symptoms, such as a cough, sore throat, and shortness of breath (1,3).

Laboratory criteria are met if one of the laboratory tests is positive: isolation of influenza virus from a clinical sample, confirmation of the presence of influenza virus nucleic acid in a clinical sample, identification of influenza virus antigen in a clinical sample by direct immunoflu- orescence technique, increase of specific antibodies against influenza virus. The epidemiological link means human-to-human transmission. All cases are classified as possible (clinical criteria only), proba- ble (clinical criteria and epidemiological link) or confirmed (clinical criteria, epidemiological link and laboratory confirmation) (1). We inform the epidemiological service at the regional unit of the National Institute of Public Health (NIPH) of the outbreak of influenza or suspicion of an outbreak and they inform the epidemiolo- gist at the Centre for Infectious Diseases of the National Institute of Public Health (3).

To confirm the flu virus, nasopharyngeal swabs must be taken from the first patients. In the event of an outbreak, it makes sense to determine the subtype of influen-

za virus (molecular testing or typing of the influenza virus isolate). Subtyping is provided by the Public Health Virology Laboratory of the National Laboratory for Health, Environment and Food (NLHEF).

Once the influenza virus has been laboratory confirmed in an outbreak, further laboratory confirmation is no longer required. Reconfirmation is required only exceptionally if new cases of influenza symptoms occur more than 72 hours after initiation of antiviral therapy; it is possible that the causative agent is another virus that causes a respiratory infection. In the case of confirmation of influenza virus, the cause may be insensitivity of the virus to the antiviral drug or another type of influenza virus (4,5).

The percentage of influenza infections without or with mild symptoms in the hospital ranges between 28 and 59%

(6,7). Influenza in hospitalized patients is also more difficult to identify due to the medications they receive (antipyretics, an- algesics, etc.) and the belief that most respiratory infections are bacterial (2,7,8,9).

The short incubation period (less than 72 hours) further complicates the distinction between nosocomial infection and infection acquired in the home environment.

Healthcare professionals, who are the most important source of influenza virus infection, become infected at home or at work (2,7). Other patients and relatives may also be a source of infection (2,7,8).

In most otherwise healthy people, the flu goes away without complications.

Complications such as secondary bacterial pneumonia often occur in the elderly and in patients with chronic diseases. In chil- dren, the most common complication is otitis media (1,3,4,5,7). Influenza is an important cause of morbidity and mortality in people over the age of 65 and in patients with chronic diseases. Elderly patients who die of pneumonia or exacerbation of previous lung or heart disease account for as much as 90% of deaths from influenza (8). Influenza mortality is 16% in acute and geriatric hospitals and 33-66% in in-

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tensive care units (8).

The World Health Organization (WHO) and most national guidelines con- tain recommendations for the annual vaccination of as many patients with chronic diseases, the elderly and pregnant women in the community as possible, consistent implementation of preventive measures in hospitals, vaccination of healthcare professionals, all to reduce the burden of nosocomial infections during the flu season.

The average efficacy of influenza vaccine in the group of people over 65 years old is 36%; and it decreases slightly with age (9). Due to the poorer efficacy of the influenza vaccine in the elderly population, it is recommended that persons who have frequent contact with this population be vaccinated against influenza as well. Re- search has shown that, despite numerous recommendations, influenza vaccination coverage remains low in vulnerable popu- lations and very low in healthcare professionals (4,10,11,12,13).

The JGH performs health care activities at the secondary level. According to the Statistical Office of Slovenia (SURS), about 200,000 people come to the hospital from all over the Gorenjska region. In early 2017, during the flu season, we detected a more extensive outbreak at the hospital.

The course of the outbreak, the measures to limit it and the consequences it had on the operation of the hospital are presented in the article.

2 Methods

2.1 Outbreak description

From 1 January 2017 to 10 January 2017, the NIPH Regional Unit (RU) Kranj received 39 reports of laboratory-confirmed cases of influenza in patients treat- ed at the JGH. In cooperation with the responsible doctor for managing nosocomial infections (DMNI), we started col- lecting epidemiological information. An epidemiological inquiry revealed that the number of patients with signs and symp-

toms in the respiratory tract was increas- ing in the hospital. Patients in an acute care hospital move between wards. Thus, it happened that a patient was transferred from the internal medical department to surgery due to an emergency procedure.

Employees also transferred because there was fluctuation between wards due to staff shortage. The hospital was fully occupied all through the outbreak, with acute cases of patients coming all the time. Due to the nature of the operation, acute hospitals cannot be temporarily closed. The influenza vaccination coverage amongst employees was low. The hospital is 71 years old and in many places the equipment is not spatially adapted to the needs of today.

There are only two single rooms in the internal medical ward.

2.2 Preventive measures

During the outbreak, a number of preventive measures were introduced, including a reduction in elective interventions for operations. The JGH authorities were informed about the instructions for preventing the spread of acute respiratory infections.

2.3 Survey of affected healthcare professionals

All healthcare professionals who fell ill were asked to complete a questionnaire and consent to process anonymized data.

Due to emergency situations of the patients, we were not able to interview the patients. In the questionnaire, we asked the affected employees demographic questions, questions about vaccination and about the severity of the disease that affected them. The severity of the disease was defined by the following criteria: as an easier course we defined patients who only had signs of a cold, felt unwell for a few days, fever did not exceed 37.5°C, they were able to perform daily activities, despite not feeling healthy; as a moderate course we defined cases that had a fever

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above 38°C, coughed, could not work for at least two days, daily activities were lim- ited due to fatigue and malaise; as a more difficult course we defined cases that had a fever above 38°C, could not work for more than two days, were lying down most of the time for several days and felt weak and fatigued for at least a week.

2.4 Taking samples for

microbiological investigation Samples of nasopharyngeal swab were received by the Department for Medical Microbiology Kranj NLHEF by 6 Febru- ary 2017.

2.5 Epidemiological methods The case in the outbreak was any patient or employee (HP) in the JGH who from 1 January 2017 to 16 February 2017 had symptoms of influenza-like illness (temperature above 37.7°C with a cough or sore throat), influenza A or B virus confirmed in the nasopharyngeal swab, or an epidemiological link to confirmed cases (hospitalization in the same room) and the absence of other causes of infection.

The case was defined as nosocomial in persons admitted to the hospital for other

reasons and in whom respiratory symptoms and signs developed no later than 72 hours after admission. An outbreak is the occurrence of more cases of an infectious disease than is expected in a certain population, in a certain geographical area and in a certain period. For a proper assessment, we need to know the size of the endangered population (denominator) and the number of cases (numerator) or the incidence rate of cases in a particular population. When a disease (cases) is less common and we do not have information on the denominator, we can compare the absolute number of cases in a given period and in a given geographical area with cases in a previous period in that area (3). The nurse managing nosocomial infection (NMNI) systematically followed the cases. Viral diagnostics were ordered by doctors in the ward for most patients with clinical symptoms. All positive cases were followed until dismissal or death. In the outbreak, the affected healthcare professionals were also recorded separately.

NMNI and DMNI assisted us in obtaining data for epidemiological analyses, providing us with lists of data on patients, their dates of birth, the date of onset of the disease, gender and the ward in which the patient lay.

2.6 Obtaining consent to conduct research

We submitted an application to the Medical Ethics Commission of the Repub- lic of Slovenia for the consent to carry out the research and obtained the consent no.

0120–529–2018.

3 Results

3.1 Epidemiological research Patients were getting sick with influenza in almost all JGH wards (Figure 1).

In the outbreak from 1 January 2017 to 16 February 2017, a total of 117 cases of influenza were detected, namely 62 (53%) Figure 1: Distribution of infected persons by departments of Jesenice

General Hospital, 2017.

Departments

Number of Patients

Department of

Internal Medicine Obstetrics and

Gynaecology Surgery Other

Patients Employees

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women and 55 (47%) men. Among the patients were also 17 healthcare professionals, of whom 9 people were vaccinated against influenza.

The number of people falling ill by day, individually for men (M), women (W) and employees (E), was shown in the form of a histogram (Figure 2). We wanted to determine whether the onset of the disease was related to the ward in which the patients were accommodated, and thus indirectly presume the infection was spreading. Based on the epidemiological connection, clinical picture and course of the outbreak, we concluded that the cause in all patients was one of the two proven causative agents, influenza A or influenza B virus.

The outbreak took place between 1 Jan- uary and 16 February 2017 at the Jesenice General Hospital.

The age structure of patients is shown in Figure 3. We found that most people became ill in the age group over 65 years.

The definition of a case in the outbreak was met by 117 patients. The attack rate in the outbreak was 117/250 = 46.8%. 13 patients classified as a case in the outbreak died (8 in January, 3 in February, and 2 in March 2017). Of these, 9 were diagnosed Figure 2: Histogram of the outbreak of influenza (patients/employees) in Jesenice General Hospital, 2017.

Age Groups

Number of People

Men Women

Figure 3: Age distribution of patients in Jesenice General Hospital, 2017.

Onset Date

Number of Patients Male Patients

Male Employees Female Patients Female Employees

according to ICD with J10.0 (influenza with pneumonia, influenza virus proven), two with J10.1 (influenza with other mani- festations on the respiratory tract) and two with J11.0 (influenza with pneumonia, virus not proven). Among the deceased were 7 women and 6 men, the average age of the deceased was 84 years (age range 69 to 92 years). Of the deceased, 8 received oseltamivir, 4 did not, for 1 this cannot be determined from the documentation.

Among the patients were 17 healthcare professionals, of whom 9 people (52.9%) were vaccinated against influenza. Influ- enza A virus was laboratory confirmed in 6 healthcare professionals, and 11 were diagnosed with influenza on the basis of the clinical picture and the epidemiological link. The affected healthcare professionals were asked to complete a questionnaire, which was answered by 10 employees (4 men, 6 women), of which 7 were vaccinated against influenza in the 2016/2017 season. The affected employees were asked in a questionnaire about a subjective assessment of the severity of the disease. Of the vaccinated persons, 2 had a severe course of the disease (28.6%), both received oseltamivir, 4 had a moderately severe course (57.1%), of which as many as 3 received oseltamivir, and 1 employee had a mild course of the disease (14.3%) and received oseltamivir. Of the unvaccinated, 1 person had a severe course and 2 a moderate course of the disease. All the surveyed affected healthcare professionals took antipyretics, 5 out of 10 took oseltamivir preventively. All healthcare professionals presumably became infected in the hospital and not in the home environment, because none of the respondents stated in the answers that they had relatives with the flu at home.

45 patients (38.5%) received oseltamivir for the treatment of influenza. To prevent transmission, 61 (24.4%) people who came in contact with patients took oseltamivir, most of whom were healthcare professionals (50) who cared for patients and had not been vaccinated as well as

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women and 55 (47%) men. Among the patients were also 17 healthcare professionals, of whom 9 people were vaccinated against influenza.

The number of people falling ill by day, individually for men (M), women (W) and employees (E), was shown in the form of a histogram (Figure 2). We wanted to determine whether the onset of the disease was related to the ward in which the patients were accommodated, and thus indirectly presume the infection was spreading. Based on the epidemiological connection, clinical picture and course of the outbreak, we concluded that the cause in all patients was one of the two proven causative agents, influenza A or influenza B virus.

The outbreak took place between 1 Jan- uary and 16 February 2017 at the Jesenice General Hospital.

The age structure of patients is shown in Figure 3. We found that most people became ill in the age group over 65 years.

The definition of a case in the outbreak was met by 117 patients. The attack rate in the outbreak was 117/250 = 46.8%. 13 patients classified as a case in the outbreak died (8 in January, 3 in February, and 2 in March 2017). Of these, 9 were diagnosed Figure 2: Histogram of the outbreak of influenza (patients/employees) in Jesenice General Hospital, 2017.

Age Groups

Number of People

Men Women

Figure 3: Age distribution of patients in Jesenice General Hospital, 2017.

Onset Date

Number of Patients Male Patients

Male Employees Female Patients Female Employees

healthcare professionals who had the flu themselves. All patients took oseltamivir for 5 days and preventively for 10 days as determined by the algorithm (3).

3.2 Microbiological investigations 74 nasopharyngeal swab samples from patients and employees were sent to NL- HEF, the Department of Medical Micro- biology Kranj. Influenza virus antigen was proven in 68 samples, influenza A virus in 59 samples and influenza B virus in 9 samples. In the remaining 49 cases (42% of all cases in the outbreak), no laboratory diag- nosis was performed, however, they were epidemiologically linked to a confirmed case.

During the outbreak, other causative agents of respiratory infections (respiratory syncytial virus, parainfluenza, coro- navirus, rhinovirus) were also detected in 6 sent samples, but these individuals were not considered as cases in the influenza outbreak according to the case definition.

13 samples with a proven genome of influenza virus were typed using the Film Array test, which allows more accurate typing of the virus. The presence of A/H₂H₃ virus type was confirmed in all 13 samples. The data is important because, like at the level of the whole of Slovenia, in this outbreak we proved only the type of influenza A virus that caused seasonal flu and was con- tained in the current season vaccine.

4 Discussion

We were alerted to the beginning of the flu outbreak by laboratory reports of influenza from JGH at the end of December 2016 and at the beginning of January 2017.

The first patients with respiratory symptoms and signs began to appear in JGH at the end of December 2016. After consul- tation with DMNI and NMNI, we chose 1 January 2017 as the beginning of the outbreak, because the first cases in December 2016 were cases of individual patients with influenza admitted to the hospital, from

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which the disease did not spread further.

Most patients and employees fell ill from 8 January 2017 to 13 January 2017 and in the second wave from 16 January 2017 to 23 January 2017. During the outbreak, 117 people became ill among approximately 250 exposed people, including 55 men and 62 women. In total, the proportion of patients among the exposed (attack rate) was 46.8%, which is comparable to the data in the literature, when in outbreaks of influenza in hospitals the number of clinical cases ranges between 11% and 59%, and laboratory-confirmed cases is 32%

and 53% of all patients in the hospital (7).

A particularly high proportion of patients, up to 60%, is described in nursing homes with a high proportion of elderly care-re- cipients and geriatric hospitals (14).

The mortality of patients in our outbreak was 11.1%, as many as 69% of patients who died were diagnosed with influenza with pneumonia with a proven influenza virus, and the average age of the deceased was 84 years. Of the deceased, 61.5% of patients received oseltamivir.

According to available NIPH data for the eleven-year period (from 2007 to 2017), 268 outbreaks were reported in nursing homes (NH), of which 42 (15.7%) were outbreaks of influenza. In the same period, Slovenian hospitals reported 66 outbreaks, of which 16 (24.2%) were outbreaks of influenza. The highest number of outbreaks of influenza was reported in the NH and in hospitals in 2017, namely 11 in the NH and 5 in hospitals (NIPH, Annual Reports on Communicable Diseases from 2007 to 2017).

Individual nosocomial outbreaks of influenza have been described in the literature. Most of these outbreaks are caused by strains of seasonal influenza A circulating in the community. Previous outbreak studies have confirmed, using advanced molecular methods, that the incidence of outbreaks is also influenced by the match between vaccine strains and circulating influenza strains in the population (15). Ac- cording to research, a weakened immune

response, a low proportion of vaccinated and thus at least partially protected people, and a possible change in circulating influenza viruses in the population contribute to the more severe course of influenza in the elderly population. In addition, it is difficult to achieve basic hygiene norms in the elderly population due to poorer par- ticipation and personality changes of the aging population (16,17,18).

Elderly people are at higher risk of de- veloping serious complications and func- tional incapacities after recovering from the flu. Influenza vaccination in the elderly is recommended to reduce the incidence of complications and death (19).

Around the world, they are facing the problem of the proportion of elderly people being vaccinated against influenza and pneumococcal pneumonia being too low. The proportion of people vaccinated against influenza, over the age of 65, living in the home environment varies greatly between countries; more than 70% of the elderly were vaccinated against influenza in Great Britain and the Netherlands in the 2013/14 season, and in many other European countries they came close to a half of the elderly population being vaccinated (18), in the neighbouring Italy the influenza vaccination coverage amongst the elderly is over 60% as well (20).

According to the NIPH, in the 2015/16 season only 10.4% of people over the age of 65 were vaccinated against influenza (this is more than in the general population, in which the share of vaccinated was 3.2%), but this is one of the lowest proportions in Europe, which is worrying (21).

This particular outbreak affected 17 healthcare professionals, of which 9 people were vaccinated against influenza. In the 2016-2017 season, 60 employees of the JGH were vaccinated against influenza, most of them doctors. As some healthcare professionals who were vaccinated against influenza also became ill during the outbreak, we wanted to objectify the clinical condition of healthcare professionals. We sent a survey questionnaire to the affected

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healthcare professionals and asked them for answers. Despite the intervention, we received only 12 completed questionnaires (70.6%), of which 7 people were vaccinated, which is 58.3%. Of the vaccinated sick healthcare professionals, 71.4% recovered from a moderate and a mild form of the disease, and among the unvaccinated, we do not have this data due to insufficiently completed surveys. There is no concrete evidence in the literature on the effectiveness of vaccination of healthcare professionals in reducing the nosocomial spread of influenza. Numerous studies confirm the benefits for patients when the staff have a high level of protection. Low vaccination coverage of healthcare professionals plays an important role in the maintenance of the outbreak (22).

At the NIPH, we obtained data on influenza vaccination coverage amongst healthcare professionals from the 2009- 2010 season onwards. From these data we understand that the highest influenza vaccination coverage of healthcare professionals was achieved in the 2009-2010 season, namely 21.3%, or in the season when the pandemic flu appeared. After this season, the percentage of those vaccinated decreased, to 17.3% in the 2010-2011 season;

to 15.9% in 2011-2012; to 13.8% in 2012- 2013; to 13.3% in 2013-2014; to 11.4% in 2014-2015; to 8.1% in 2015-2016; to 9.1%

in 2016-2017. In the 2017-2018 season, we are noticing an increase in the percentage of vaccinated healthcare professionals to 14.3%.

45 patients (38.5%) received oseltamivir for the treatment of influenza. To prevent transmission, oseltamivir was used for 10 days by 61 (24.4%) individuals who were in contact with those who were ill, most of whom were healthcare professionals. Among the surveyed vaccinated healthcare professionals who had the flu, as many as 5 out of 6 (85.7%) were taking oseltamivir. 2 of these had a severe course, 4 moderate and 1 a mild course. By sur- veying individuals, we found that the drug was taken relatively late, between 48 and

72 hours from the onset of the disease.

There is statistically calculated evidence in the literature on the efficacy of the preventive effect of oseltamivir, both pre- and post-exposure (23,24).

During the outbreak, members of the Commission for the Prevention of Nos- ocomial Infections and other employees, following our advice, carried out a number of prevention activities to limit the outbreak, such as complete closure of the hospital for visitors, interruption of stu- dent internships, isolation, relocation of unvaccinated employees, a more rigorous hygiene regime, use of masks and chemoprophylaxis. In spite of this, the outbreak was very extensive. The most common reasons for such a large-scale outbreak were that the hospital was fully occupied throughout the outbreak, the hospital was not closed for the duration of the outbreak, so acute patients came all the time.

Acute hospitals cannot be closed. Employ- ees were not sufficiently vaccinated. In- frastructurally, the hospital is mostly old and in many places it is not adapted to the needs of today. There are only two single rooms in the internal medicine ward of 24 rooms, 1 room in the gynaecology ward of 10 rooms and 1 in the day ward. The hospital has a total of 263 beds.

It is also written in the literature that a high degree of adherence to preventive measures is required in the early stage of an outbreak. Previous illnesses and weak- ness of patients, difficulties in providing isolation, non-compliance with the recommendations of personal hygiene of patients and poor response of the immune system of elderly patients to vaccination contribute to the disease. An important problem in the spread of influenza is also posed by infected patients and healthcare professionals, who do not have more pro- nounced clinical signs.

There is an example of good practice in the literature on how to curb nosocomial influenza infection in an overcrowd- ed emergency room. The authors see the solution in rapid molecular microbiologi-

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cal diagnostics, which distinguishes influenza from other respiratory viruses, and simultaneous action such as patient isolation, early treatment, and redistribution.

During the study, influenza-related factors were identified by multivariate logistic re- gression. It has been statistically confirmed that the presence of myalgia, the absence of gastrointestinal signs and blood oxy- gen saturation ≥ 97% are associated with influenza and are helpful in differentiating other respiratory diseases (25).

There is no solid evidence in the literature that preventive measures can prevent the spread of influenza in institutions with elderly patients. The lack of evidence on the effectiveness of individual preventive measures is mainly due to in-depth molecular analyses and the effect of grouping.

New approaches to outbreak research have refuted the original hypothesis that a single strain affects an entire institution during an outbreak. Conversely, phylogenetic analyses revealed several different group- ings of influenza viruses circulating in individual wards depending on close contact with index cases. These results suggest that during an outbreak of influenza in a larger establishment, there are a large number of clusters of influenza A (H₃N₂) viruses of different genetic group variants circulating in the community (26).

A limitation of our study was that we did not perform virus diagnostics in all patients. Diagnostics were performed mainly at the beginning of the outbreak, also in healthcare professionals. We also did not perform diagnostics at the very

beginning of the disease in those patients who were hospitalized in rooms remote from the index case. Influenza virus was typified only in a certain proportion because we mostly performed a cheaper test that determines whether it is influenza A or B, but does not determine subtypes of the virus. We also did not check the data on influenza vaccination in the research, we only took into account the statements of patients and employees. The limitation was also that the epidemiological analysis covered only those who were ill, which makes it impossible to draw any conclu- sions about risk factors.

The article presents the first major outbreak described in a Slovenian hospital.

There was a shortage of isolation rooms during the outbreak and a lack of nursing staff due to sick leave. The article points out that the flu is a serious and real threat to elderly patients in hospitals. The paper also highlights the need for early detec- tion and proactive control of nosocomial infections and emphasizes the importance of good cooperation between regional ep- idemiologists, microbiologists and clinics and all users.

5 Acknowledgment

We, the authors, thank the employees of JGH, NLHEF and NIPH for their dedi- cated assistance in dealing with and managing the outbreak. Special thanks to Katja Krnc and Mateja Blaško Markič for data processing.

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