key: cord-0878261-yxa85hiz
authors: Bludau, Anna; Heinemann, Stephanie; Mardiko, Amelia A.; Kaba, Hani E.J.; Leha, Andreas; von Maltzahn, Nicole; Mutters, Nico T.; Leistner, Rasmus; Mattner, Frauke; Scheithauer, Simone
title: Infection control strategies for patients and accompanying persons during the COVID-19 pandemic in German hospitals – Results from a cross-sectional study in March-April 2021
date: 2022-04-09
journal: J Hosp Infect
DOI: 10.1016/j.jhin.2022.03.014
sha: cbe35af736f61e0b2d8a444e264258da8289fa8d
doc_id: 878261
cord_uid: yxa85hiz

BACKGROUND: Patients are at risk of nosocomial COVID-19 infection. The role of accompanying persons/visitors as potential infection donors is not yet well-known, but the risk will be influenced by prevention measures recommended by infection control practitioners. AIM: The aim of the study is to collect information about COVID-19 infection control strategies for patients and accompanying persons from infection control practitioners in German hospitals. METHODS: A cross-sectional questionnaire was developed, ethically-approved, pre-tested and formatted as an online tool. We invited infection control practitioners in 987 randomly-selected German hospitals in March and April 2021 to participate. For statistical analysis, the hospitals were categorised as small (0-499 beds) or large (≥500 beds). FINDINGS: 100 surveys were completed (response rate: 10%). More large (71%) than small hospitals (49%) let patients decide freely whether to wear medical or FFP2 masks. Most hospitals reported spatial separation for COVID-19 patients and non-COVID-19 cases (38%) or additionally for suspected COVID-19 cases (53%). A separation of healthcare teams for these areas existed in 54% of the hospitals. Accompaniment bans were more prevalent in large (52%) than in small hospitals (29%), but large hospitals granted more exemptions. CONCLUSION: The possibility to separate areas and teams seemed to depend on the hospital's structural conditions, therefore impairing the implementation of recommendations. Accompaniment regulations differ between hospital sizes and may depend on patient numbers, case type/severity and patient’s requirements. In the dynamic pandemic, it can be difficult to stay up to date with findings and recommendations about infection control.

On 27th January 2020, the first known COVID-19 cases occurred in Germany. In March and April 2021, more than one year after the beginning of the pandemic, there was sufficient knowledge about the transmission routes of COVID-19 [1, 2] and how to minimise transmissions [1, 3] available. The shortage of personal protective equipment (PPE) at the beginning of the pandemic was overcome [4] . In German hospitals, well-established hygiene regimes for pathogens that transmit analogously were already in place before the pandemic [5, 6, 7, 8] and could be quickly adapted to SARS-CoV-2. Furthermore, the German Public Health Authority Robert-Koch-Institute (RKI) had issued recommendations for handling COVID-19 outbreaks in healthcare facilities [9] and how to prioritise vaccinations in hospitals [10] .

There is daily fluctuation of healthcare workers (HCW), patients, accompanying persons and visitors in hospitals. Often, individuals infected with COVID-19 are not detected in time because they are asymptomatic [11, 12, 13] or presymptomatic [14, 15, 16] . HCW are at risk of severe disease progression when infected [17] . But especially patients are vulnerable and a study showed that the mortality rate was higher than in the general population [18] . Not only direct contact with COVID-19 cases, but also simply staying in the same ward was identified as a risk factor for nosocomial infections in patients [19, 20] . Furthermore, nosocomial infections can particularly be caused by inadequate isolation of infected patients and improper use of PPE [21] .

Our study collected data from infection control practitioners in Germany and aimed to provide an overview about the infection control strategies used during the SARS-CoV-2 pandemic in March and April 2021. Here we focused on patients and accompanying persons as possible sources of nosocomial COVID-19 infections. Therefore, we particularly report on hygiene behaviour promotion, PPE, the separation of confirmed, suspected and non-COVID-19 cases as well as HCW teams. 

The participants were the hospital infection control practitioners in German hospitals. We invited a random sample of hospitals stratified according to hospital size. A detailed description of the sampling process can be found in the supplementary materials 1.

The questionnaire was developed in collaboration with the (vice-)speaker of the Scientific Working Group "Hospital Hygiene: Prevention of Infection and Antibiotic Resistance" and Standing Committee "General and Hospital Hygiene" of the German Society for Hygiene and Microbiology (Deutsche Gesellschaft für Hygiene und Mikrobiologie, DGHM). The aim of the questionnaire was to collect information about infection control strategies in German hospitals.

The questionnaire was pre-tested by an interdisciplinary team of local researchers, adapted accordingly and re-tested. The final questionnaire can be found in the supplementary materials 2.

We used the LimeSurvey platform (https://www.limesurvey.org/) to provide the questionnaire. The anonymous online survey was conducted in March and April 2021. Infection control practitioners from 987 hospitals across Germany received an invitation email to participate in the survey. This project received positive ethical consent by the local committee under the file no. 5/2/21 An.

All the data obtained from completed questionnaires were analysed with SPSS 26 (IBM Deutschland GmbH, Ehningen, Germany). The hospital categories were combined into small hospitals with 0-499 beds and large hospitals with a capacity of over 499 beds. Fisher's exact test was used to test statistical significance of differences between small and large hospitals. For multiple choice questions, the test was performed per item. For single choice questions, the test was performed for the entire question. If the result was significant, Fisher's exact tests were used for post hoc analysis. Statistical significance was defined as p < .05.

100 of 987 sent out questionnaires were completed by infection control practitioners across Germany (response rate: 10%). As seen in Table I , about two third of the participants were either director or deputy of a department responsible for infection control. 93% of the participants were qualified in hospital hygiene and infection control. There is a reasonable distribution of responding hospitals across the regions, which also reflects the distribution of the population, resulting in an even response rate of 4-5% per region. The distribution between small and large hospitals was almost equal.

Before the start of the pandemic most hospitals already provided hand sanitizer dispensers in the entrance (88%) and waiting areas (84%). Nearly two third of the hospitals hung up hygiene promotion posters before the pandemic and after the pandemic started almost all of the hospitals used this intervention.

Information for patients about desired hygiene behaviour distributed by oral briefing prior to admission was the most prevalent form in the hospitals (62%), followed by written information (42%) and distribution of brochures (29%) and posters (28%) in patients` rooms. This applies to all hospitals regardless of size (supplementary materials 3).

As shown in Table II , 60% of hospitals allowed their patients to decide on whether to wear a medical or FFP2 mask (small: 49%, large: 71%, p=0.082).

In the presence of medical staff, patients were recommended to wear a mask in 73% of the hospitals. Patients were also recommended to wear masks in rooms when visitors were present in 65% of the hospitals. This was more prevalent in large (77%) than in small hospitals (53%; p=0.021).

38% of the hospitals reported spatial separation for COVID-19 and non-COVID-19 patients (Table III) . A separation for these groups and additionally for suspected COVID-19 cases was reported by 53% of the hospitals. In the area for suspected COVID-19 cases, single rooms were available in 43% of the hospitals. Separation mostly occurred in the form of separate wards (66%). However, there were also separations that occurred within the same ward (22%). Separation strategies were applied mostly in normal wards (78%). In intensive care units separation was more prevalent in large (59%) than small hospitals (39%; p=0.049). One fourth of the hospitals had completely separated areas in the emergency room. Separate HCW teams for COVID-19 and non-COVID-19 areas were prevalent in 54% of the hospitals. 15% separated the teams only if a nosocomial infection was suspected or confirmed. 61% of the hospitals left incidentally occurring suspected cases in the non-COVID area but in isolation or single rooms until clarification. Most hospitals separated confirmed, suspected and non-COVID-19 cases by scheduling the interventions at different times. Large hospitals (88%) did this more often than small hospitals (69%; p=0.027).

J o u r n a l P r e -p r o o f 84% of hospitals had patient restrictions in the waiting areas and distancing between patients was mostly accomplished by maintaining at least 1.5 metre of distance (77%). Some hospitals used one (24%) or two empty chairs (27%) to indicate the required distance. Table IV shows that prohibition of accompaniment was more prevalent in large (53%) than in small hospitals (29%; p=0.016). In return small hospitals (69%) allowed one accompanying person more often than large hospitals (47%; p=0.027). Some situations (e.g. childbirth) and characteristics of the patients (e.g. senior) were approved as reasons for exceptions. Large hospitals were granting more exemptions than small hospitals in the following situations: need for translation (p=0.03), childbirth (p<0.001) as well as senior or underaged patients (p=0.005).

All hospitals with a paediatric department allowed accompanying persons for underaged patients. Accompaniment was restricted to only one guardian in 79% of all hospitals. However, large hospitals (55%) allowed alternating between guardians more often than small hospitals (25%; p=0.002).

Most hospitals (57%) let the accompanying persons decide whether to wear a medical or FPP2 mask.

Hand hygiene is one of the most important measures in infection prevention and control [22] and almost every hospital in our study provided hand sanitizer dispensers in the entrance and waiting areas, even before the pandemic started. However, despite an increase in the beginning of the pandemic [23, 24, 25] , previous studies showed that sanitizer dispensers are rarely used [26, 27] . After the start of the SARS-CoV-2 pandemic, posters of hygiene behaviour were distributed in nearly every hospital. It is important to note that the effect which information has on human behaviour can highly depend on the way it is communicated [28, 29, 30] . All educational material, including posters, especially in the accompanying, widely acknowledged informationpandemic [31] , should therefore be soundly designed. Oral briefings might be a good solution, considering that they are more personal and therefore might have a bigger effect.

At the time of the survey, there was no fixed regulation in Germany specifying whether patients had to wear a FFP2 or medical mask [32] . Both mask types significantly reduce the risk of SARS-CoV-2 infection compared to social distancing [33] . This is also reflected in the data since most hospitals left the choice of mask to the patients and accompanying persons. Just a small percentage recommended only FFP2 masks. When worn correctly, FPP2 masks offer more protection against infection [33] , but are also more expensive and restricting than the commonly used medical mask. The latter could also lead to more patients not wearing the FFP2 mask correctly and therefore reducing the protective effect. Especially at times when FFP2 masks are scarce, it makes sense to allocate the limited number of masks only to particularly vulnerable and exposed persons. Additional analysis (supplementary materials 4) showed that two third of the hospitals in the south of Germany recommended FFP2 masks for accompanying persons and therefore more frequently than other regions (12-28%, p≤0.001). In contrast to other federal states, Bavaria had already introduced mandatory FFP2 masks in public spaces in January 2021 [34] . This may have fuelled the expectation of FFP2 mask recommendations in Bavarian hospitals and explain the high recommendation rate in south Germany. When visitors enter the patient's room, patients were recommended to wear a medical mask more often in large hospitals than in small hospitals. Conversely, it seems that small hospitals more often recommended patients to wear masks in shared rooms. This might explain why further recommendations to wear face masks upon receiving visitors was less frequent in small hospitals.

Especially with a high case number, the RKI recommended avoiding the treatment of COVID-19 cases and other patients in the same building so that patient and staff routes do not overlap. For a smaller number of cases or if this is not possible, a separate ward or ward area should be set up for the care of COVID-19 cases. In the suspected case area, contact between patients must be largely prevented [32] . This was in line with recommendations of the World Health Organization (WHO) [35] , the Centers for Disease Control and Prevention (CDC) [36] and the European Centre for Disease Prevention and Control (ECDC) [37] . COVID-19 areas were often located in a separate ward or a separate unit within the same ward rather than a separate building. Possibilities for spatial separation of COVID-19 cases, suspected COVID-19 cases and non-COVID-19 cases seem to highly depend on the structural conditions of the hospitals. For example, large hospitals provided normal wards with J o u r n a l P r e -p r o o f COVID-19 infection control for patients completely separated areas for COVID-19 cases more frequently, indicating that they had more financial, structural and staffing leeway. Data from other countries show similar situations. A cross-sectional study involving the heads of 57 emergency departments (ED) in France (May/June 2020) showed that, while around half of the ED had a triage area for suspected cases, ca. 26% of the ED could not be expanded or moved to another space [38] . In the Netherlands, 89% of the surveyed 66 ED (80% of total number of ED) had a completely separated area for COVID-19 cases, which was however usually located in the original ED unit (July-September 2020) [39] . Around one third of the heads of 283 Spanish ED stated in a survey conducted in March/April 2020 that missing space was a challenge, still 80% had areas specifically for patients suspected of having COVID-19 [40] . The data for the intensive care units should be interpreted with caution, since small hospitals mainly provide primary care.

Most of the hospitals in our study left incidentally occurring suspected cases in non-COVID-19 areas in isolation/single rooms until clarification. A proportion of these hospitals did not have an area for suspected cases as seen in the data. If the suspicion is not confirmed this strategy might be safer and associated with less logistical effort. This especially applies to severely ill or immunocompromised patients and considering that not all of the hospitals provided single rooms in the suspected case area. On the other hand, keeping the patient on the same ward as non-infected patients can be more labour-intensive since HCW have to apply more comprehensive infection control measures. In addition, the risk of infection among HCW and, consequently, other patients on the ward is always present. One of the great advantages that an area for suspected cases provides is that it reduces the logistical problem of patient location and isolation. This improves the utilisation of staff and structural resources by concentrating potential cases at a defined point in the hospital. Especially the new Variant of Concern Omicron (B.1.1.529) with high transmissibility and possibly less severe symptoms than previous variants [41, 42, 43] leads to a high rate of accidental cases. Therefore, transferring suspected COVID-19 cases to a separate area, when existing and single rooms are available, seems reasonable and is also in line with RKI recommendations [32] .

Another important aspect of our survey was the separation and restructuring of HCW teams for COVID-19 and non-COVID-19 areas. The RKI recommended assigned staff to each of the areas. At least within a shift, HCW should not change between areas and if possible work should always be done in fixed teams [32] . Despite the fact that interaction between different departments can not be totally avoided and cross-contamination is therefore possible, segregating teams can be one of the interventions to effectively prevent transmission between personnel in contact with COVID-19 cases, their colleagues and hence, other patients. However, only half of the hospitals in our study had a separate team for suspected and/or confirmed COVID-19 cases. One possible reason for this could be the high staff shortage in nursing, which makes it difficult to set up flexible duty rosters, especially when staff are absent at short notice. Interestingly, next to a few case studies [44, 45, 46] no other multi-centre study could be found on this topic. It would also be interesting to see two years into the pandemic to see if the regulations in March/April 2021 were transitional or long-term solutions.

Regarding the regulation of accompanying persons, larger hospitals had a stricter policy in general but at the same time granted more exceptions than smaller hospitals. Firstly, larger hospitals naturally have more patients and therefore more accompanying persons and also visitors, which present a high infection risk and also a higher need to be monitored. A general restriction for accompanying persons and visitors could be safer, easier to implement and less labour-intensive. Secondly, the higher rate of exceptions could be attributed to more severe cases, where relatives were given the chance to be present. Thirdly, larger hospitals also tend to have more cases with translational needs etc. Therefore more tailored rules are necessary.

In addition, small hospitals in Germany are often specialised hospitals which offer care for specific diseases or medical specialisation, such as psychiatric, orthopaedic or paediatric hospitals. In these types of hospitals, patients might need more assistance from their relatives, because of their mental health, mobility or age. Therefore, small hospitals can seem to be more permissive than large hospitals. Due to few studies on the topic of accompanying persons and a thematically very close overlap, we will also look at visitor regulations in the following. A look at practices in North America show that a general restriction with exceptions for special circumstances seemed common [47, 48, 49] . No comparisons were made between hospital sizes. While visitor regulation can have a positive effect on the prevention of viral respiratory infections [50, 51] , reviews show that they can also have negative consequences for the mental and physical health of patients, the wellbeing of family members and the workload of care providers [52, 53] . Our data indicate that regulations for minor patients were generally less strict as all hospitals allowed at least one guardian to accompany the child. In the case of alternating guardians, it would be interesting to see in which frequency a switch was allowed and whether this only applied to special departments. A retrospective examination of visitor guidelines in 239 children hospitals in the USA shows that half of the hospitals restricted the visitation to one guardian, but other than that a wide range of different regulations [54] . There is a lack of primary research regarding the impact of visitor restrictions on children during the pandemic [55] , but one can assume that it causes similar or worse consequences compared to adults. Therefore, restrictions for accompanying persons and visitors should only be implemented when necessary and effective. Healthcare providers should prepare for a higher demand for coping and communication with as well as support of patients, especially underaged patients, and family members, when introducing such restrictions.

The questionnaire was developed in collaboration with an interdisciplinary expert group and distributed across a randomised sample of all German hospitals. The comparably low response could be explained by the following considerations. First, the questionnaire was relatively long with a minimum completion time of 15 minutes. Second, the second wave of the pandemic peaked during the survey period, which expectedly rendered the target group confronted by many pandemic-related commitments. 

Possibilities for separation of COVID-19, suspected COVID-19 and non-COVID-19 cases as well as segregation of HCW teams seem to depend on the structural conditions of the hospitals and separation recommendations were not always implemented. Regulations for accompanying persons differed between small and large hospitals and therefore possibly depend on overall patient numbers, case type and severity as well as patients requirements. The age of the patient might have an impact since regulations for underage patients were generally less strict. When implementing visitor regulations, possible consequences for the wellbeing of patients and family members as well as the workload of care providers should be considered. Wearing masks was recommended for patients and accompanying persons, but recommendations differed between medical and FFP2 masks. This could depend on regional regulations as well as different assessments of necessity and safety. Due to the dynamic pandemic development, knowledge and recommendations on infection control measures might quickly change. Keeping up to date and filtering out the important and correct information can be difficult, especially for hospitals with few highly skilled infection control staff. Information and counselling services can be useful here. Further studies are necessary to evaluate the impact of infection control and prevention strategies of the hospitals and their repercussions not only on the organisational level but also on the compliance to the given recommendations. All values in percent. For multiple choice questions, Fisher's exact test was performed per item. For single choice questions, the test was performed for the entire question. If the result was significant, Fisher tests were used for post hoc analysis. Statistical significance was defined as p < .05 and significant results are presented in bold.

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