Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

SARS-CoV-2 nosocomial infection acquired in a French university hospital during the 1st wave of the Covid-19 pandemic, a prospective study

SARS-CoV-2 nosocomial infection acquired in a French university hospital during the 1st wave of... Background: In healthcare facilities, nosocomial transmissions of respiratory viruses are a major issue. SARS‑ CoV‑2 is not exempt from nosocomial transmission. Our goals were to describe COVID‑19 nosocomial cases during the first pandemic wave among patients in a French university hospital and compliance with hygiene measures. Methods: We conducted a prospective observational study in Grenoble Alpes University Hospital from 01/03/2020 to 11/05/2020. We included all hospitalised patients with a documented SARS‑ CoV‑2 diagnosis. Nosocomial case was defined by a delay of 5 days between hospitalisation and first symptoms. Hygiene measures were evaluated between 11/05/2020 and 22/05/2020. Lockdown measures were effective in France on 17/03/2020 and ended on 11/05/2020. Systematic wearing of mask was mandatory for all healthcare workers (HCW ) and visits were prohibited in our institu‑ tion from 13/03/2021 and for the duration of the lockdown period. Results: Among 259 patients included, 14 (5.4%) were considered as nosocomial COVID‑19. Median time before symptom onset was 25 days (interquartile range: 12–42). Eleven patients (79%) had risk factors for severe COVID‑19. Five died (36%) including 4 deaths attributable to COVID‑19. Two clusters were identified. The first cluster had 5 cases including 3 nosocomial acquisitions and no tested HCWs were positive. The second cluster had 3 cases including 2 nosocomial cases and 4 HCWs were positive. Surgical mask wearing and hand hygiene compliance were adequate for 95% and 61% of HCWs, respectively. Conclusions: The number of nosocomial COVID‑19 cases in our hospital was low. Compliance regarding mask wear ‑ ing, hand hygiene and lockdown measures drastically reduced transmission of the virus. Monitoring of nosocomial COVID‑19 cases during the first wave enabled us to determine to what extent the hygiene measures taken were effec‑ tive and patients protected. Trial registration Study ethics approval was obtained retrospectively on 30 September 2020 (CECIC Rhône‑Alpes‑ Auvergne, Clermont‑Ferrand, IRB 5891). Keywords: SARS‑ CoV‑2, COVID ‑19, Outbreak, Healthcare ‑associated infection, Mask, Hand hygiene Background *Correspondence: caroline.landelle@gmail.com Severe Acute Respiratory Syndrome coronavirus 2 Hospital Hygiene Department, Pavilion E ‑ Grenoble Alpes University (SARS-CoV-2), responsible for Coronavirus disease 19 Hospital, CS 10217, 38043 Grenoble Cedex 9, France (COVID-19), rapidly spread all around the world and Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 2 of 8 was declared a pandemic on 11/03/2020 by the World contact precautions (surgical mask, gloves, gown) were Health Organization (WHO) [1, 2]. Given that the elderly required. FFP2 masks were also used, during aerosol- or persons with comorbidities are more likely to develop generating procedures and in accordance with national serious disease [3], preventing the acquisition of SARS- French recommendations [7]. Visits in our institution CoV-2 within healthcare facilities rapidly became a major were prohibited from 13/03/2021 and for the duration challenge. of the lockdown period. A maximum of 157 beds were During the first wave, the French government chose available in ICU and 186 in other COVID-19 dedicated to apply strict containment measures and massive lock- units. When a case of COVID-19 was suspected in a non- down from 17/03/2020 to 11/05/2020. Isolation and COVID area, the patient was tested and transferred to a social distancing measures were established such as the COVID area in case of positivity. CHU-GA hospitalised closing of schools and public spaces and the prohibition only seriously ill patients or those with comorbidities. All of travel, and different barrier measures (washing hands others remained home and followed up by regular phone regularly, coughing inside the elbow, etc.) were strongly calls in accordance with a special and dedicated protocol. recommended. Despite these measures, by 31/05/2020 The testing criteria were not only clinical symptoms com - in France, SARS-CoV-2 had resulted in almost 150,000 monly suggestive of COVID-19 such as fever, dry cough cases, more than 28,000 deaths and about 17,000 hos- and tiredness, but also a suspicious computed tomog- pitalisations [4]. While SARS-CoV-2 is spread primarily raphy scan (CT-scan) [8]. All HCWs with suspected through droplets, transmission by contact with contami- COVID-19 were tested as well. The first-line approach nated objects and surfaces or aerosols can also occur [5]. for testing was nasopharyngeal swab. In case of doubt or A number of measures were taken to prevent nosoco- negative result with strong clinical suspicion, clinicians mial transmission, including: strict ban on hospital visits, used imagery or clinical evidence to confirm or refute strengthened hand hygiene, and systematic wearing of a the assumption, which was possibly corroborated by a surgical mask by healthcare workers (HCWs) [6]. deeper sample such as tracheal or bronchoalveolar-lav- In this study, we sought to describe nosocomial cases age fluid. Samples were analysed in the virology labora - and clusters of COVID-19 cases acquired in a French tory by real-time reverse transcription polymerase chain university hospital during the first wave of the COVID- reaction (RT-PCR) assay for SARS-CoV-2. Contact cases 19 epidemic. A secondary aim was to assess compliance were defined as HCWs or patients with close contact with hygiene measures implemented during the epidemic (< 1  m, ≥ 15  min) to clinical cases without mask (room- period. mates, shared activities etc.). Contact cases were moni- tored closely but tested only if symptomatic. Methods Generalities The patients included We conducted a prospective observational study dur- All hospitalised patients with positive RT-PCR results ing the first wave of the COVID-19 epidemic period in for SARS-CoV-2 or CT-scan signs suggestive or typical Grenoble Alpes University Hospital (CHU-GA), from of COVID-19 (levels 4 and 5 of CO-RADS score) were 01/03/2020 to 11/05/2020. CHU-GA is the largest hos- included. Non-hospitalised patients (i.e. emergency stay, pital of Grenoble city (France) with more than 9500 consultation, etc.), even those with a positive result (posi- employees, over 2100 beds in 149 units (86 medical units, tive RT-PCR or radiologic evidence), were excluded. A 47 surgery units and 16 intensive care units (ICU)/pos- COVID-19 case was considered as nosocomial if onset tICU) with 65% of double rooms; approximately 2400 of symptoms occurred more than 5  days after hospi- patients are admitted every day. talisation, considering that 5  days is the median incuba- tion time for COVID-19 [9]. Cases attributable to other General measures at Grenoble Alpes University Hospital healthcare facilities were not considered in our study as During the epidemic period CHU-GA was designated as nosocomial cases. At that time there was no consensual the COVID-19 reference hospital for the department of nationwide definition for nosocomial clusters. We used Isère. Overall organisation was modified so as to reduce the following definition: ≥ 2 nosocomial cases among normal hospital activity, including a ban on elective sur- patients and HCWs with fewer than 7  days between gery for the duration of the lockdown period, the objec- cases. tive being to cope with a massive influx of COVID-19 patients. Surgical mask wearing within the hospital Data collection was mandatory for HCWs and for patients when mov- Patient data were collected from their electronic medi- ing outside of their room or during care. Units reserved cal records by residents of the hospital hygiene unit. for COVID-19 patients were set up, where droplets and They included age, sex, hospitalisation unit, onset of Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 3 of 8 symptoms, co-infection, risk factors for severe COVID- Table 1 Nosocomial COVID‑19 case characteristics 19 (overweight, obesity with Body Mass Index > 30, Characteristics Nosocomial hypertension, diabetes, pulmonary disease, cardiac dis- COVID-19 cases (n = 14) ease, neuromuscular disease, kidney disease, immunode- ficiency), ICU stay, clinical evolution, origins of infection Gender, n (%) (community-acquired or nosocomial). For nosocomial Male 8 (57) cases, investigations were extensive, collecting informa- Median age in years (IQR) 63.7 (45.8–83.3) tion concerning the acquisition unit and patient room Median time between hospitalization and symp‑ 24.5 (11.5–42.0) setting (double or single room) and all nosocomial con- tom onset in days (IQR) tact generated (patients and HCWs). The study complied Patient 1 23 with the Outbreak Reports and Intervention studies Of Patient 2 21 Nosocomial infection (ORION) reporting guidelines Patient 3 41 [10]. Patient 4 10 Between 11/05/2020 and 22/05/2020, audits were car- Patient 5 13 ried out in all non-COVID acute care units (88 units) to Patient 6 18 assess compliance with hygiene measures. Observations Patient 7 26 were carried out by nurses from the hygiene unit and Patient 8 33 pertained to the following items: correct mask wearing Patient 9 49 by HCWs and patients when needed, hand hygiene, phys- Patient 10 77 ical distancing, screen deployment in double occupancy Patient 11 6 rooms and disinfection of shared equipment. Patient 12 43 Patient 13 32 Analyses and ethical aspects Patient 14 9 Qualitative variables were expressed in absolute number Risk factors, n (%)* 11 (78.6) and in percentage. Quantitative variables were expressed Overweight (25 < BMI** < 30) 2 (14.3) as median and interquartile range (IQR). Groups were Obesity (BMI** > 30) 0 (0.0) compared by means of Fisher’s exact test. Ethics approval Hypertension 6 (42.9) was obtained on 30 September 2020 (CECIC Rhône- Diabetes 4 (28.6) Alpes-Auvergne, Clermont-Ferrand, IRB 5891). Pulmonary disease 7 (50.0) Cardiac Disease 5 (35.7) Results Neuromuscular disease 1 (7.1) From 01/03/2020 to 11/05/2020, 4811 samples from Kidney Disease 2 (14.3) suspected patients and HCWs were analysed in the Immunodeficiency 1 (7.1) virology laboratory in search of SARS-CoV-2, and 259 Co infection, n (%) 0 (0.0) hospitalised patients with COVID-19 were identified. Intensive Care Unit stay, n (%) 1 (7.1) Among them, 62 (23.9%) were transferred to the ICU; Vital status, n (%) 215 (83.0%) were discharged and 37 (14.3%) died. All in Dead 5 (35.7) all, 245 (94.6%) cases were community-acquired and 14 * Other than age > 65 years; ** BMI: Body Mass Index (5.4%) were considered as nosocomial COVID-19 cases. Concerning nosocomial COVID-19 patients, 8 (57.0%) were male; median age was 63.7  years (IQR: 45.8–83.3) was higher (13.1% vs 35.7%; p < 0.005); in 4 out of the 5 (Table  1). Median time between hospitalisation and (80%) cases, it was attributable to COVID-19. As regards symptom onset was 24.5  days (IQR: 11.5–42), four the 14 nosocomial cases, they were found in 9 units: 7 patients had symptoms between 5 and 14 days after hos- with isolated cases, and 2 where clusters were identified pitalization. Eleven (78.6%) had risk factors other than (Table  2). All nosocomial cases of COVID-19 involving age exceeding 65  years. In this population, 2 (14.3%) the patient and caregivers had cycle threshold (Ct) values patients were overweight, but neither was clinically below 33 and 27 respectively, which confirmed conta - obese. However, half of them had a past history of pul- gious status and recent acquisition. In the forensic medi- monary disease such as asthma or chronic obstructive cine unit (social medicine, suicidology), the first case pulmonary disease, 6 (42.9%) had hypertension, 5 (35.7%) was community-acquired and identified on 16/03/2020. had cardiovascular disease and 4 (28.6%) presented with Starting with this case, 2 nosocomial cases were identi- diabetes. Five of them (35.7%) died. In comparison with fied. The 3 patients had shared a room for about 2  days community cases, mortality among nosocomial cases Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 4 of 8 Table 2 Distribution of nosocomial cases among units and number of healthcare workers (HCWs) tested Unit Nosocomial COVID-19 cases out of N of positive HCW out Patient or HCW Ct** Acquisition total COVID-19 cases in each unit of total HCW sample* Neurology 1/1 0/3 Patient 33.48 HA Geriatric 2/2 1/5 Patient 20.08 HA Patient Missing data HA HCW 27.5 – Forensic Medicine 3/5 0/3 Patient 29.13 CA (cluster 1) Patient Negative CA Patient Start of curve HA Patient 25.85 HA Patient 31.65 HA Pediatric surgery 1/1 2/5 Patient 33.49 HA HCW 18.97 – HCW 25.78 – Thoracic oncology 2/2 0/1 Patient 12.52 HA Patient 15.66 HA Endocrine Vascular Thoracic Surgery 1/1 1/4 Patient 20.46 HA HCW 23.63 – Hepatology and Gastroenterology 1/3 0 Patient 18.15 HA Patient 29.45 CA Patient Missing data CA Nephrology 1/1 0/3 Patient 16.65 HA Mood disorder unit (cluster 2) 2/5 4/7 Patient 18.53 CA Patient 20.22 HA Patient 17.73 HA Patient 22.24 CA Patient Negative CA HCW 17.99 – HCW 23.52 – HCW 17.36 – HCW 20.47 – HCWs healthcare workers, Ct cycle threshold. HA Hospital-acquired, CA Community-acquired *Sampled between 5 and 15 days after the first symptoms of the first case **The lowest Ct value between the 2 targets was chosen during each of their hospitalisations. The first noso - the Mood Disorder unit, the first case was considered comial case appeared 3  days after the index case. After as community-acquired insofar as he was hospitalised 6  days of hospitalization, fever was ascertained on on 27/03/2020 and his first symptoms were declared on 19/03/2020 and a nasopharyngeal swab on 20/03/2020 29/03/2020. This case was linked to 2 nosocomial cases, was positive for SARS-CoV-2. The second nosocomial the first of which had been hospitalised since 14/02/2020, case was hospitalised for 10  days, with the first symp - while the first symptoms were declared on 03/04/2020. toms appearing on 23/03/2020. A nasopharyngeal swab The second nosocomial case presented symptoms on the was sampled on 24/03/2020. On 02/04/2020, the unit same day and had been hospitalised for about 3 months. received another patient, whose first symptoms were Seven HCWs from this unit were tested for SARS-CoV-2, declared on 06/04/2020, and the case was considered as a 4 of whom tested positive (57.1%). community-acquired. The virus had probably been trans - Figure  1 represents the distribution of nosocomial and mitted a roommate who was admitted on 25/03/2020 community-acquired cases and underscores the fact that and presented a positive sample on 10/04/2020. All in all the nosocomial cases were grouped in time and suc- all, 3 out of the 5 COVID-19 cases were nosocomial and cessive; they occurred in weeks 12, 13 and 14, the first none of the HCWs tested positive for SARS-CoV-2. In 3 weeks of the lockdown. Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 5 of 8 Lockdown period -visits forbidden -wearing of amasksystematic 100 -limited journeys 5 13 12 12 9 8 89 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Week number Number of COVID+ communitycases Number of COVID+ nosocomial cases Fig. 1 Time distribution of nosocomial‑acquired cases among community‑acquired cases of COVID ‑19 As regards observation of hygiene measures (Table  3), the mask (FFP2 or surgical) was correctly worn by 94.7% Table 3 Hygiene measures observed during audit in 88 units of of HCWs. FFP2 mask use was justified for 99.0% of Grenoble Alpes University Hospital HCWs. Concerning hand hygiene, 60.6% of HCWs car- ried it out when necessary, 15.5% achieved sufficiently Hygiene measures observed Compliance (%) long friction and 13.7% performed it correctly. Disinfec- Wearing of mask (FFP2 or surgical) by HCWs N = 693 tion of shared equipment took place in 78.6% of obser- Adequate 94.7% vations. In 45.5% of observations, HCWs were too close Inadequate* 3.0% to each other during breaks. Concerning hygiene meas- Not wearing mask 2.3% ures for patients, wearing a mask when necessary (move- Wearing of FFP2 by HCWs N = 693 ment for technical exams or during care) was adequate Justified 99.0% among 81.5%. Physical distancing in common spaces was Hand hygiene respected in 99% of observations. A screen was deployed Respect of indications N = 449; 60.6% in 76.2% of double occupancy rooms. Long enough friction N = 277; 15.5% Technique respected N = 248; 13.7% Discussion Disinfection of shared equipment N = 98; 78.6% In this study carried out during the COVID-19 lockdown Physical distancing respected for HCW (break N = 119; 54.6% rooms…) period in France, 5% of nosocomial cases were reported Wearing of mask for patients when needed N = 260 among all patients hospitalised for COVID-19 in our institution. Considering a range of incubation time up to Adequate 81.5% 14  days, acquisition was questionable for 4 nosocomial Inadequate* 3.5% cases with an onset of symptoms between 5 and 14 days. Not wearing mask 15.0% However, only 1 case occurred before 7  days of hospi - Screen in double occupancy rooms N = 151 talisation, therefore the number of nosocomial cases is Correctly used (deployed) 76.2% probably not be excessively overestimated. Most of the Physical distance respected between patients in com‑ N = 73; 99.0% mon spaces (rehabilitation spaces, corridors…) nosocomial cases had risk factors for severe COVID-19 and 4 died from COVID-19. Survey of hygiene measures Meaning having the mask under the nose or the mouth Number of COVID+ cases Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 6 of 8 highlighted good compliance with mask wearing a but a HCWs was not possible, a factor that may have led to an lack of correct hand hygiene. During the first wave, the increased number of nosocomial cases. positive test rate in the Grenoble department (Isère) was As regards hand hygiene we observed moderate com- lower than the mean of France, the the highest peak at pliance (60.6%) and, above all, poor technique (13.7%) the hospital being reached at week 13 with a positive rate and insufficient friction time (15.5%). A lack of time or of 18.17%. a lack of knowledge could explain these results. What- Several studies have analysed the relative proportions ever the reason, education on the importance of hand of nosocomial COVID-19 cases. A meta-analysis con- hygiene is essential to promote these gestures. Moreover, ducted in Wuhan on nosocomial infection of COVID-19, the disinfection of shared equipment could be improved SARS and MERS, showed a proportion of nosocomial (78.6%). The survivability of Coronaviruses on inanimate COVID-19 at 44% [11]. Comparing our nosocomial rate surfaces has been shown to range from hours to days [25]. to the literature is complex, due to the different defini - Even though the proportion of transmission from con- tions used in various studies. One study used the same taminated surfaces remains unknown, hand hygiene and definition of nosocomial cases in Japan and reported disinfection of shared equipment are essential to avoid- rate of nosocomial cases at 18.5% [12]. Another hospital ance of cross-transmission [26]. The Screen deployment in Spain, using an interval of 6  days, presented a noso- in double occupancy rooms is another hygiene measure comial rate of 2.5% [13]. Percentages of nosocomial cases needing to be improved in our hospital. Indeed, in the reported in 2 urology departments in Spain [14], a diges- first cluster, all the nosocomial cases were acquired in tive surgery department in Paris [15], an orthopeadic sur- double occupancy rooms. Transmission from one patient gery department in Spain [16] and a university Hospital to another sharing the same room, especially in SARS- in London [17] were 2.1%, 4.9%, 6.5% and 11.3% respec- CoV-2 with droplet transmission, is hard to control. This tively. A study conducted in a large US Academic medical constitutes a huge challenge for our institution insofar as center found 2 nosocomial cases among 697 COVID- 65% of the rooms are double occupancy. Hygiene audits 19 positive patients [18]. Finally, a study in three acute have shown a patient compliance rate of 81.5% for wear- hospitals in Scotland found 19 (11%) nosocomial cases ing a surgical mask when they moved or during care. among 173 COVID-19 positive patients [19]. In compari- In France, citizens are not used to wearing masks when son with influenza nosocomial cases, a meta-analysis [20] they present respiratory symptoms or when they are in showed that the proportion of nosocomial cases among closed and crowded spaces; use of masks is generally lim- the total number of patients with influenza ranged from ited to healthcare settings. In the second cluster, patient 15 to 59%. We can suggest two hypotheses to explain behavior may have influenced transmission. In the Mood these differences and the low rate of COVID-19 nosoco - Disorder unit, many manual activities shared between mial cases. First, the COVID-19 incidence rate in Greno- patients and HCWs such as card games or manual artis- ble during the first wave was rather low. However, other tic activities are part of the treatment. Moreover, patients factors may also explain these results, including hygiene admitted in the 2 units with clusters are mainly psychi- measures. During the COVID-19 outbreak, HCWs atric patients or patients with social difficulties. These and patients systematically wore masks, which was not units are at risk for cross-transmission because of major the case in the influenza epidemic. According to these patient turnover, patients with difficulties complying with results, universal wearing of a surgical mask by HCWs instructions, shared spaces and wandering patients. In could be a way to control nosocomial transmission of res- our hospital, though there was no hand hygiene program piratory viruses [21]. Another hypothesis concerns the targeting patients, but information on barrier measures lockdown and the ban on visits, which was never imple- was provided on screens in halls and patient rooms. Con- mented during an influenza epidemic. Some studies have cerning the cluster where 7 HCWs were tested, 4 were evaluated the effect of non-pharmaceutical interventions infected. All patients and HCW were tested at the same including the lockdown and proved their efficiency [22, time, so we cannot draw conclusions on the chronol- 23]. In our study, all nosocomial cases were grouped ogy of transmission [27]. Furthermore, physical proxim- within the first 3  weeks of lockdown. As fourteen days ity between HCWs during breaks could also be a way of is the longest incubation time reported in the literature transmission. A phylogenetic study based on sequencing [24], we can suppose that the lockdown was efficient and could clarify these epidemiological links and confirm or helped to control nosocomial cases. It is important to not the existence of a single strain [28]. Of note, no clus- note that given the high proportion of double occupancy ter was identified in surgery units, probably due to the rooms in our hospital for patients and a HCW staff short - drastic reduction in their activity following the ban on age, quarantine of all exposed asymptomatic patients and elective surgery [29, 30]. Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 7 of 8 Acknowledgements The strengths of our study are based on prospective We thank Alexis Baveux for his help in translating into English and Jeffrey data collection. The same data have been collected from Arsham for editing this manuscript. We are also indebted to all members of electronic medical records in our institution to follow the virology laboratory and infection control unit. nosocomial influenza cases, and we know this is a reliable Authors’ contributions and effective system [31]. Moreover, we were in touch AL, FC, MG, CG, MRM and CL conceptualized and designed the study. SL, BN with occupational health teams, infectious disease spe- and PM validated the analysis of SARS‑ CoV‑2. MLM, PP and OE validated the diagnosis of COVID‑19. AL, FC, MG and CL contributed to the bibliography. AL, cialists and biologists in case of diagnosis uncertainty. FC, MG and CL prepared the documents for the Ethics Committees. AL, FC, All of these factors should help to reinforce knowledge of MG, SL, BN, MLM, MRM and CL analysed and interpreted the data. AL, FC, MG this emerging disease, especially concerning nosocomial and CL drafted the manuscript. All authors have approved the final version of the manuscript. cases, which are poorly described in the literature. However this study has some limitations. First, our Funding definition of nosocomial cases was based on 5-day incu - None. bation, whereas the incubation time described by the Availability of data and materials WHO is 1 to 14  days [24], meaning that we may have The datasets used and/or analysed during the current study are available from defined patients as nosocomial cases whereas they were the corresponding author on reasonable request. not, or conversely. Given this wide range of incubation time, there is no optimum definition. We have chosen Declarations median incubation as a means of achieving early detec- Ethics approval and consent to participate tion of potential nosocomial clusters in view of prevent- Study ethics approval was obtained on 30 September 2020 (CECIC Rhône‑ ing further transmission, the objective being to avoid Alpes‑Auvergne, Clermont ‑Ferrand, IRB 5891). classifying a nosocomial case as community-acquired. Consent for publication Second, asymptomatic cases were not tested and system- Not applicable. atic screening 14 days after discharge was not performed, Competing interests certainly causing missed SARS-CoV-2 infections. Third, All authors report no conflicts of interest relevant to this article. An abstract our institution was relatively spared and did not have as containing partial data was presented at the ESCMID Conference on Coronavi‑ many cases of COVID-19 as other hospitals elsewhere. rus Disease (ECCVID), 2020, online conference. Finally, hygiene audits were performed after the lock- Author details down period and did not adequately reflect the reality of Infection Control Unit, Grenoble Alpes University Hospital, Grenoble, France. lockdown period. Grenoble Alpes University/CNRS, Grenoble INP, MESP TIM‑ C UMR 5525, Grenoble, France. Virology Laboratory, Grenoble Alpes University Hospital, Grenoble, France. Grenoble Alpes University/CNRS/CEA, Institut de Biologie Structurale (IBS), HIV and persistent viral infections, Grenoble, France. I nfec‑ Conclusions tious Diseases Department, Grenoble Alpes University Hospital, Grenoble, France. Hospital Hygiene Department, Pavilion E ‑ Grenoble Alpes University In healthcare facilities, nosocomial transmission of res- Hospital, CS 10217, 38043 Grenoble Cedex 9, France. piratory viruses is a major issue and SARS-CoV-2 is not exempt from nosocomial transmission [32]. Hygiene Received: 23 November 2020 Accepted: 20 July 2021 measures, especially mask wearing and hand hygiene, are fundamental to control cross-transmission, and training of HCWs is an obviously necessary means of achieving References good compliance. However, nosocomial transmission 1. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A novel corona‑ also depends on patient characteristics and their abil- virus from patients with pneumonia in China, 2019. N Engl J Med. ity to comply with prevention measures. A specific and 2020;382(8):727–33. 2. World Health Organisation. Coronavirus disease 2019 (COVID‑19) Situ‑ targeted policy should probably be established in units ation Report –51 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ admitting patients who have difficulties observing these coron aviru se/ situa tion‑ repor ts/ 20200 311‑ sitrep‑ 51‑ covid‑ 19. pdf measures (psychiatry, social medicine or even geriatrics), 3. Zheng Z, Peng F, Xu B, Zhao J, Liu H, Peng J, et al. Risk factors of critical & mortal COVID‑19 cases: a systematic literature review and meta‑analysis. J the objective being to effectively prevent nosocomial Infect. 2020;81(2):e16‑25. transmission. 4. World Health Organisation. Coronavirus disease (COVID‑19) Situation Report–132 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ coron aviru se/ situa tion‑ repor ts/ 20200 531‑ covid‑ 19‑ sitrep‑ 132. pdf? sfvrsn= Abbreviations d9c2e aef_2 CHU‑ GA: Grenoble Alpes University Hospital; COVID‑19: Coronavirus disease 5. World Health Organisation. Modes of transmission of virus causing 19; CT‑scan: Computed tomographic scan; HCW: Healthcare workers; ICU: COVID‑19: implications for IPC precaution recommendations. Scientific Intensive care units; IQR: Interquartile range; ORION: Outbreak Reports and brief. 2020 [Internet]. https:// www. who. int/ news‑ room/ comme ntari es/ Intervention studies of Nosocomial infection; RT‑PCR: Reverse transcription detail/ modes‑ of‑ trans missi on‑ of virus‑‑ causi ng‑ covid‑ 19‑ impli catio ns‑ for‑ polymerase chain reaction; SARS‑ CoV‑2: Severe Acute Respiratory Syndrome ipc‑ preca ution‑ recom menda tions coronavirus 2; WHO: World Health Organization. Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 8 of 8 6. World Health Organisation. Clinical management of severe acute respira‑ 20. Voirin N, Barret B, Metzger M‑H, Vanhems P. Hospital‑acquired influenza: tory infection when novel coronavirus (2019‑nCoV ) infection is suspected a synthesis using the Outbreak Reports and Intervention Studies of [Internet]. https:// apps. who. int/ iris/ bitst ream/ handle/ 10665/ 330893/ Nosocomial Infection (ORION) statement. J Hosp Infect. 2009;71(1):1–14. WHO‑ nCoV‑ Clini cal‑ 2020.3‑ eng. pdf? seque nce= 1& isAll owed=y 21. Ambrosch A, Rockmann F, Klawonn F, Lampl B. Eec ff t of a strict hygiene 7. Haut Conseil de la Santé Publique. Avis relatif à la rationalisation de bundle for the prevention of nosocomial transmission of SARS‑ CoV‑2 in l’utilisation des masques chirurgicaux anti‑projections et des masques the hospital: a practical approach from the field. J Infect Public Health. filtrant de type FFP2 pour les professionnels de santé en établissements 2020;13(12):1862–7. de santé, en établissements médico‑sociaux et en ville en période épi‑ 22. Hsiang S, Allen D, Annan‑Phan S, Bell K, Bolliger I, Chong T, et al. The effect démique de stade 3: 10 of large‑scale anti‑ contagion policies on the COVID‑19 pandemic. Nature. 8. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of 2020;584(7820):262–7. patients infected with 2019 novel coronavirus in Wuhan. China Lancet 23. Flaxman S, Mishra S, Gandy A, Unwin HJT, Mellan TA, Coupland H, et al. Lond Engl. 2020;395(10223):497–506. Estimating the effects of non‑pharmaceutical interventions on COVID ‑19 9. Lauer SA, Grantz KH, Bi Q, Jones FK, Zheng Q, Meredith HR, et al. The in Europe. Nature. 2020;584(7820):257–61. incubation period of coronavirus disease 2019 (COVID‑19) from publicly 24. World Health Organisation. Coronavirus disease 2019 (COVID‑19) Situ‑ reported confirmed cases: estimation and application. Ann Intern Med. ation Report –73 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ 2020;172(9):577–82.coron aviru se/ situa tion‑ repor ts/ 20200 402‑ sitrep‑ 73‑ Covid‑ 19. pdf 10. Stone SP, Cooper BS, Kibbler CC, Cookson BD, Roberts JA, Medley GF, et al. 25. Akram MZ. Inanimate surfaces as potential source of 2019‑nCoV spread The ORION statement: guidelines for transparent reporting of outbreak and their disinfection with biocidal agents. Virusdisease. 2020;31(2):94–6. reports and intervention studies of nosocomial infection. Lancet Infect 26. Seto WH, Tsang D, Yung RWH, Ching TY, Ng TK, Ho M, et al. Eec ff tiveness Dis. 2007;7(4):282–8. of precautions against droplets and contact in prevention of nosocomial 11. Zhou Q, Gao Y, Wang X, Liu R, Du P, Wang X, et al. Nosocomial infections transmission of severe acute respiratory syndrome (SARS). Lancet Lond among patients with COVID‑19, SARS and MERS: a rapid review and Engl. 2003;361(9368):1519–20. meta‑analysis. Ann Transl Med. 2020;8(10):629. 27. Huttunen R, Syrjänen J. Healthcare workers as vectors of infectious 12. Harada S, Uno S, Ando T, Iida M, Takano Y, Ishibashi Y, et al. Control of a diseases. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. nosocomial outbreak of COVID‑19 in a University Hospital. Open Forum 2014;33(9):1477–88. Infect Dis. 2020;7(12):512. 28. Meredith LW, Hamilton WL, Warne B, Houldcroft CJ, Hosmillo M, Jahun 13. Gras‑ Valentí P, Mora‑Muriel JG, Chico ‑Sánchez P, Algado ‑Sellés N, Soler ‑ AS, et al. Rapid implementation of SARS‑ CoV‑2 sequencing to investigate Molina VM, Hernández‑Maldonado M, et al. Eec ff tivity of a program for cases of health‑ care associated COVID‑19: a prospective genomic surveil‑ the control and prevention of covid‑19 Healthcare ‑Associated Infections lance study. Lancet Infect Dis. 2020;20(11):1263–71. in a Spanish Academic Hospital. J Patient Saf. 2021;17(4):323–30. 29. Laux CJ, Bauer DE, Kohler A, Uçkay I, Farshad M. Disproportionate Case 14. Sánchez MD, Sánchez M, De La Morena JM, Ogaya‑Pinies G, Mateo E, reduction after ban of elective surgeries during the SARS‑ CoV‑2 pan‑ Moscatiello P, et al. Nosocomial SARS‑ CoV‑2 infection in urology depart ‑ demic. Clin Spine Surg. 2020;33(6):244–6. ments: results of a prospective multicentric study. Int J Urol Off J Jpn Urol 30. Burkhard J, Lacher S, Holy D, Schenk P, Schäfer C, Kahr P, et al. No Assoc. 2021;28(1):62–7. nosocomial transmission of SARS‑ CoV‑2 between Healthcare Workers in 15. Luong‑Nguyen M, Hermand H, Abdalla S, Cabrit N, Hobeika C, Brouquet Surgical Departments unexposed to Covid‑19 patients. Ann Case Rep. A, et al. Nosocomial infection with SARS‑ Cov‑2 within Departments of 2020;5(6):533. Digestive Surgery. J Visc Surg. 2020;157(3S1):S13–8. 31. Bocquet A, Wintenberger C, Lupo J, Morand P, Pavese P, Gallouche M, 16. Lakhani K, Minguell J, Guerra‑Farfán E, Lara Y, Jambrina U, Pijoan J, et al. et al. Description of an influenza outbreak in a French university hospital Nosocomial infection with SARS‑ CoV‑2 and main outcomes after surgery and risk factors of nosocomial influenza. Eur J Clin Microbiol Infect Dis. within an orthopaedic surgery department in a tertiary trauma centre in 2021;40(4):879–84. Spain. Int Orthop. 2020;44(12):2505–13. 32. Hui DS, Azhar EI, Kim Y‑ J, Memish ZA, Oh M‑D, Zumla A. Middle East 17. Taylor J, Rangaiah J, Narasimhan S, Clark J, Alexander Z, Manuel R, et al. respiratory syndrome coronavirus: risk factors and determinants of Nosocomial COVID‑19: experience from a large acute NHS Trust in South‑ primary, household, and nosocomial transmission. Lancet Infect Dis. West London. J Hosp Infect. 2020;106(3):621–5. 2018;18(8):e217–27. 18. Rhee C, Baker M, Vaidya V, Tucker R, Resnick A, Morris CA, et al. Incidence of nosocomial COVID‑19 in patients hospitalized at a large US Academic Publisher’s Note Medical Center. JAMA Netw Open. 2020;3(9):e2020498. Springer Nature remains neutral with regard to jurisdictional claims in pub‑ 19. Khan KS, Reed‑Embleton H, Lewis J, Saldanha J, Mahmud S. Does noso ‑ lished maps and institutional affiliations. comial COVID‑19 result in increased 30‑ day mortality? A multi‑ centre observational study to identify risk factors for worse outcomes in patients with COVID‑19. J Hosp Infect. 2021;107:91–4. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance & Infection Control Springer Journals

SARS-CoV-2 nosocomial infection acquired in a French university hospital during the 1st wave of the Covid-19 pandemic, a prospective study

Loading next page...
 
/lp/springer-journals/sars-cov-2-nosocomial-infection-acquired-in-a-french-university-R7FP7nB0Xs
Publisher
Springer Journals
Copyright
Copyright © The Author(s) 2021
eISSN
2047-2994
DOI
10.1186/s13756-021-00984-x
Publisher site
See Article on Publisher Site

Abstract

Background: In healthcare facilities, nosocomial transmissions of respiratory viruses are a major issue. SARS‑ CoV‑2 is not exempt from nosocomial transmission. Our goals were to describe COVID‑19 nosocomial cases during the first pandemic wave among patients in a French university hospital and compliance with hygiene measures. Methods: We conducted a prospective observational study in Grenoble Alpes University Hospital from 01/03/2020 to 11/05/2020. We included all hospitalised patients with a documented SARS‑ CoV‑2 diagnosis. Nosocomial case was defined by a delay of 5 days between hospitalisation and first symptoms. Hygiene measures were evaluated between 11/05/2020 and 22/05/2020. Lockdown measures were effective in France on 17/03/2020 and ended on 11/05/2020. Systematic wearing of mask was mandatory for all healthcare workers (HCW ) and visits were prohibited in our institu‑ tion from 13/03/2021 and for the duration of the lockdown period. Results: Among 259 patients included, 14 (5.4%) were considered as nosocomial COVID‑19. Median time before symptom onset was 25 days (interquartile range: 12–42). Eleven patients (79%) had risk factors for severe COVID‑19. Five died (36%) including 4 deaths attributable to COVID‑19. Two clusters were identified. The first cluster had 5 cases including 3 nosocomial acquisitions and no tested HCWs were positive. The second cluster had 3 cases including 2 nosocomial cases and 4 HCWs were positive. Surgical mask wearing and hand hygiene compliance were adequate for 95% and 61% of HCWs, respectively. Conclusions: The number of nosocomial COVID‑19 cases in our hospital was low. Compliance regarding mask wear ‑ ing, hand hygiene and lockdown measures drastically reduced transmission of the virus. Monitoring of nosocomial COVID‑19 cases during the first wave enabled us to determine to what extent the hygiene measures taken were effec‑ tive and patients protected. Trial registration Study ethics approval was obtained retrospectively on 30 September 2020 (CECIC Rhône‑Alpes‑ Auvergne, Clermont‑Ferrand, IRB 5891). Keywords: SARS‑ CoV‑2, COVID ‑19, Outbreak, Healthcare ‑associated infection, Mask, Hand hygiene Background *Correspondence: caroline.landelle@gmail.com Severe Acute Respiratory Syndrome coronavirus 2 Hospital Hygiene Department, Pavilion E ‑ Grenoble Alpes University (SARS-CoV-2), responsible for Coronavirus disease 19 Hospital, CS 10217, 38043 Grenoble Cedex 9, France (COVID-19), rapidly spread all around the world and Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 2 of 8 was declared a pandemic on 11/03/2020 by the World contact precautions (surgical mask, gloves, gown) were Health Organization (WHO) [1, 2]. Given that the elderly required. FFP2 masks were also used, during aerosol- or persons with comorbidities are more likely to develop generating procedures and in accordance with national serious disease [3], preventing the acquisition of SARS- French recommendations [7]. Visits in our institution CoV-2 within healthcare facilities rapidly became a major were prohibited from 13/03/2021 and for the duration challenge. of the lockdown period. A maximum of 157 beds were During the first wave, the French government chose available in ICU and 186 in other COVID-19 dedicated to apply strict containment measures and massive lock- units. When a case of COVID-19 was suspected in a non- down from 17/03/2020 to 11/05/2020. Isolation and COVID area, the patient was tested and transferred to a social distancing measures were established such as the COVID area in case of positivity. CHU-GA hospitalised closing of schools and public spaces and the prohibition only seriously ill patients or those with comorbidities. All of travel, and different barrier measures (washing hands others remained home and followed up by regular phone regularly, coughing inside the elbow, etc.) were strongly calls in accordance with a special and dedicated protocol. recommended. Despite these measures, by 31/05/2020 The testing criteria were not only clinical symptoms com - in France, SARS-CoV-2 had resulted in almost 150,000 monly suggestive of COVID-19 such as fever, dry cough cases, more than 28,000 deaths and about 17,000 hos- and tiredness, but also a suspicious computed tomog- pitalisations [4]. While SARS-CoV-2 is spread primarily raphy scan (CT-scan) [8]. All HCWs with suspected through droplets, transmission by contact with contami- COVID-19 were tested as well. The first-line approach nated objects and surfaces or aerosols can also occur [5]. for testing was nasopharyngeal swab. In case of doubt or A number of measures were taken to prevent nosoco- negative result with strong clinical suspicion, clinicians mial transmission, including: strict ban on hospital visits, used imagery or clinical evidence to confirm or refute strengthened hand hygiene, and systematic wearing of a the assumption, which was possibly corroborated by a surgical mask by healthcare workers (HCWs) [6]. deeper sample such as tracheal or bronchoalveolar-lav- In this study, we sought to describe nosocomial cases age fluid. Samples were analysed in the virology labora - and clusters of COVID-19 cases acquired in a French tory by real-time reverse transcription polymerase chain university hospital during the first wave of the COVID- reaction (RT-PCR) assay for SARS-CoV-2. Contact cases 19 epidemic. A secondary aim was to assess compliance were defined as HCWs or patients with close contact with hygiene measures implemented during the epidemic (< 1  m, ≥ 15  min) to clinical cases without mask (room- period. mates, shared activities etc.). Contact cases were moni- tored closely but tested only if symptomatic. Methods Generalities The patients included We conducted a prospective observational study dur- All hospitalised patients with positive RT-PCR results ing the first wave of the COVID-19 epidemic period in for SARS-CoV-2 or CT-scan signs suggestive or typical Grenoble Alpes University Hospital (CHU-GA), from of COVID-19 (levels 4 and 5 of CO-RADS score) were 01/03/2020 to 11/05/2020. CHU-GA is the largest hos- included. Non-hospitalised patients (i.e. emergency stay, pital of Grenoble city (France) with more than 9500 consultation, etc.), even those with a positive result (posi- employees, over 2100 beds in 149 units (86 medical units, tive RT-PCR or radiologic evidence), were excluded. A 47 surgery units and 16 intensive care units (ICU)/pos- COVID-19 case was considered as nosocomial if onset tICU) with 65% of double rooms; approximately 2400 of symptoms occurred more than 5  days after hospi- patients are admitted every day. talisation, considering that 5  days is the median incuba- tion time for COVID-19 [9]. Cases attributable to other General measures at Grenoble Alpes University Hospital healthcare facilities were not considered in our study as During the epidemic period CHU-GA was designated as nosocomial cases. At that time there was no consensual the COVID-19 reference hospital for the department of nationwide definition for nosocomial clusters. We used Isère. Overall organisation was modified so as to reduce the following definition: ≥ 2 nosocomial cases among normal hospital activity, including a ban on elective sur- patients and HCWs with fewer than 7  days between gery for the duration of the lockdown period, the objec- cases. tive being to cope with a massive influx of COVID-19 patients. Surgical mask wearing within the hospital Data collection was mandatory for HCWs and for patients when mov- Patient data were collected from their electronic medi- ing outside of their room or during care. Units reserved cal records by residents of the hospital hygiene unit. for COVID-19 patients were set up, where droplets and They included age, sex, hospitalisation unit, onset of Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 3 of 8 symptoms, co-infection, risk factors for severe COVID- Table 1 Nosocomial COVID‑19 case characteristics 19 (overweight, obesity with Body Mass Index > 30, Characteristics Nosocomial hypertension, diabetes, pulmonary disease, cardiac dis- COVID-19 cases (n = 14) ease, neuromuscular disease, kidney disease, immunode- ficiency), ICU stay, clinical evolution, origins of infection Gender, n (%) (community-acquired or nosocomial). For nosocomial Male 8 (57) cases, investigations were extensive, collecting informa- Median age in years (IQR) 63.7 (45.8–83.3) tion concerning the acquisition unit and patient room Median time between hospitalization and symp‑ 24.5 (11.5–42.0) setting (double or single room) and all nosocomial con- tom onset in days (IQR) tact generated (patients and HCWs). The study complied Patient 1 23 with the Outbreak Reports and Intervention studies Of Patient 2 21 Nosocomial infection (ORION) reporting guidelines Patient 3 41 [10]. Patient 4 10 Between 11/05/2020 and 22/05/2020, audits were car- Patient 5 13 ried out in all non-COVID acute care units (88 units) to Patient 6 18 assess compliance with hygiene measures. Observations Patient 7 26 were carried out by nurses from the hygiene unit and Patient 8 33 pertained to the following items: correct mask wearing Patient 9 49 by HCWs and patients when needed, hand hygiene, phys- Patient 10 77 ical distancing, screen deployment in double occupancy Patient 11 6 rooms and disinfection of shared equipment. Patient 12 43 Patient 13 32 Analyses and ethical aspects Patient 14 9 Qualitative variables were expressed in absolute number Risk factors, n (%)* 11 (78.6) and in percentage. Quantitative variables were expressed Overweight (25 < BMI** < 30) 2 (14.3) as median and interquartile range (IQR). Groups were Obesity (BMI** > 30) 0 (0.0) compared by means of Fisher’s exact test. Ethics approval Hypertension 6 (42.9) was obtained on 30 September 2020 (CECIC Rhône- Diabetes 4 (28.6) Alpes-Auvergne, Clermont-Ferrand, IRB 5891). Pulmonary disease 7 (50.0) Cardiac Disease 5 (35.7) Results Neuromuscular disease 1 (7.1) From 01/03/2020 to 11/05/2020, 4811 samples from Kidney Disease 2 (14.3) suspected patients and HCWs were analysed in the Immunodeficiency 1 (7.1) virology laboratory in search of SARS-CoV-2, and 259 Co infection, n (%) 0 (0.0) hospitalised patients with COVID-19 were identified. Intensive Care Unit stay, n (%) 1 (7.1) Among them, 62 (23.9%) were transferred to the ICU; Vital status, n (%) 215 (83.0%) were discharged and 37 (14.3%) died. All in Dead 5 (35.7) all, 245 (94.6%) cases were community-acquired and 14 * Other than age > 65 years; ** BMI: Body Mass Index (5.4%) were considered as nosocomial COVID-19 cases. Concerning nosocomial COVID-19 patients, 8 (57.0%) were male; median age was 63.7  years (IQR: 45.8–83.3) was higher (13.1% vs 35.7%; p < 0.005); in 4 out of the 5 (Table  1). Median time between hospitalisation and (80%) cases, it was attributable to COVID-19. As regards symptom onset was 24.5  days (IQR: 11.5–42), four the 14 nosocomial cases, they were found in 9 units: 7 patients had symptoms between 5 and 14 days after hos- with isolated cases, and 2 where clusters were identified pitalization. Eleven (78.6%) had risk factors other than (Table  2). All nosocomial cases of COVID-19 involving age exceeding 65  years. In this population, 2 (14.3%) the patient and caregivers had cycle threshold (Ct) values patients were overweight, but neither was clinically below 33 and 27 respectively, which confirmed conta - obese. However, half of them had a past history of pul- gious status and recent acquisition. In the forensic medi- monary disease such as asthma or chronic obstructive cine unit (social medicine, suicidology), the first case pulmonary disease, 6 (42.9%) had hypertension, 5 (35.7%) was community-acquired and identified on 16/03/2020. had cardiovascular disease and 4 (28.6%) presented with Starting with this case, 2 nosocomial cases were identi- diabetes. Five of them (35.7%) died. In comparison with fied. The 3 patients had shared a room for about 2  days community cases, mortality among nosocomial cases Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 4 of 8 Table 2 Distribution of nosocomial cases among units and number of healthcare workers (HCWs) tested Unit Nosocomial COVID-19 cases out of N of positive HCW out Patient or HCW Ct** Acquisition total COVID-19 cases in each unit of total HCW sample* Neurology 1/1 0/3 Patient 33.48 HA Geriatric 2/2 1/5 Patient 20.08 HA Patient Missing data HA HCW 27.5 – Forensic Medicine 3/5 0/3 Patient 29.13 CA (cluster 1) Patient Negative CA Patient Start of curve HA Patient 25.85 HA Patient 31.65 HA Pediatric surgery 1/1 2/5 Patient 33.49 HA HCW 18.97 – HCW 25.78 – Thoracic oncology 2/2 0/1 Patient 12.52 HA Patient 15.66 HA Endocrine Vascular Thoracic Surgery 1/1 1/4 Patient 20.46 HA HCW 23.63 – Hepatology and Gastroenterology 1/3 0 Patient 18.15 HA Patient 29.45 CA Patient Missing data CA Nephrology 1/1 0/3 Patient 16.65 HA Mood disorder unit (cluster 2) 2/5 4/7 Patient 18.53 CA Patient 20.22 HA Patient 17.73 HA Patient 22.24 CA Patient Negative CA HCW 17.99 – HCW 23.52 – HCW 17.36 – HCW 20.47 – HCWs healthcare workers, Ct cycle threshold. HA Hospital-acquired, CA Community-acquired *Sampled between 5 and 15 days after the first symptoms of the first case **The lowest Ct value between the 2 targets was chosen during each of their hospitalisations. The first noso - the Mood Disorder unit, the first case was considered comial case appeared 3  days after the index case. After as community-acquired insofar as he was hospitalised 6  days of hospitalization, fever was ascertained on on 27/03/2020 and his first symptoms were declared on 19/03/2020 and a nasopharyngeal swab on 20/03/2020 29/03/2020. This case was linked to 2 nosocomial cases, was positive for SARS-CoV-2. The second nosocomial the first of which had been hospitalised since 14/02/2020, case was hospitalised for 10  days, with the first symp - while the first symptoms were declared on 03/04/2020. toms appearing on 23/03/2020. A nasopharyngeal swab The second nosocomial case presented symptoms on the was sampled on 24/03/2020. On 02/04/2020, the unit same day and had been hospitalised for about 3 months. received another patient, whose first symptoms were Seven HCWs from this unit were tested for SARS-CoV-2, declared on 06/04/2020, and the case was considered as a 4 of whom tested positive (57.1%). community-acquired. The virus had probably been trans - Figure  1 represents the distribution of nosocomial and mitted a roommate who was admitted on 25/03/2020 community-acquired cases and underscores the fact that and presented a positive sample on 10/04/2020. All in all the nosocomial cases were grouped in time and suc- all, 3 out of the 5 COVID-19 cases were nosocomial and cessive; they occurred in weeks 12, 13 and 14, the first none of the HCWs tested positive for SARS-CoV-2. In 3 weeks of the lockdown. Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 5 of 8 Lockdown period -visits forbidden -wearing of amasksystematic 100 -limited journeys 5 13 12 12 9 8 89 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 Week number Number of COVID+ communitycases Number of COVID+ nosocomial cases Fig. 1 Time distribution of nosocomial‑acquired cases among community‑acquired cases of COVID ‑19 As regards observation of hygiene measures (Table  3), the mask (FFP2 or surgical) was correctly worn by 94.7% Table 3 Hygiene measures observed during audit in 88 units of of HCWs. FFP2 mask use was justified for 99.0% of Grenoble Alpes University Hospital HCWs. Concerning hand hygiene, 60.6% of HCWs car- ried it out when necessary, 15.5% achieved sufficiently Hygiene measures observed Compliance (%) long friction and 13.7% performed it correctly. Disinfec- Wearing of mask (FFP2 or surgical) by HCWs N = 693 tion of shared equipment took place in 78.6% of obser- Adequate 94.7% vations. In 45.5% of observations, HCWs were too close Inadequate* 3.0% to each other during breaks. Concerning hygiene meas- Not wearing mask 2.3% ures for patients, wearing a mask when necessary (move- Wearing of FFP2 by HCWs N = 693 ment for technical exams or during care) was adequate Justified 99.0% among 81.5%. Physical distancing in common spaces was Hand hygiene respected in 99% of observations. A screen was deployed Respect of indications N = 449; 60.6% in 76.2% of double occupancy rooms. Long enough friction N = 277; 15.5% Technique respected N = 248; 13.7% Discussion Disinfection of shared equipment N = 98; 78.6% In this study carried out during the COVID-19 lockdown Physical distancing respected for HCW (break N = 119; 54.6% rooms…) period in France, 5% of nosocomial cases were reported Wearing of mask for patients when needed N = 260 among all patients hospitalised for COVID-19 in our institution. Considering a range of incubation time up to Adequate 81.5% 14  days, acquisition was questionable for 4 nosocomial Inadequate* 3.5% cases with an onset of symptoms between 5 and 14 days. Not wearing mask 15.0% However, only 1 case occurred before 7  days of hospi - Screen in double occupancy rooms N = 151 talisation, therefore the number of nosocomial cases is Correctly used (deployed) 76.2% probably not be excessively overestimated. Most of the Physical distance respected between patients in com‑ N = 73; 99.0% mon spaces (rehabilitation spaces, corridors…) nosocomial cases had risk factors for severe COVID-19 and 4 died from COVID-19. Survey of hygiene measures Meaning having the mask under the nose or the mouth Number of COVID+ cases Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 6 of 8 highlighted good compliance with mask wearing a but a HCWs was not possible, a factor that may have led to an lack of correct hand hygiene. During the first wave, the increased number of nosocomial cases. positive test rate in the Grenoble department (Isère) was As regards hand hygiene we observed moderate com- lower than the mean of France, the the highest peak at pliance (60.6%) and, above all, poor technique (13.7%) the hospital being reached at week 13 with a positive rate and insufficient friction time (15.5%). A lack of time or of 18.17%. a lack of knowledge could explain these results. What- Several studies have analysed the relative proportions ever the reason, education on the importance of hand of nosocomial COVID-19 cases. A meta-analysis con- hygiene is essential to promote these gestures. Moreover, ducted in Wuhan on nosocomial infection of COVID-19, the disinfection of shared equipment could be improved SARS and MERS, showed a proportion of nosocomial (78.6%). The survivability of Coronaviruses on inanimate COVID-19 at 44% [11]. Comparing our nosocomial rate surfaces has been shown to range from hours to days [25]. to the literature is complex, due to the different defini - Even though the proportion of transmission from con- tions used in various studies. One study used the same taminated surfaces remains unknown, hand hygiene and definition of nosocomial cases in Japan and reported disinfection of shared equipment are essential to avoid- rate of nosocomial cases at 18.5% [12]. Another hospital ance of cross-transmission [26]. The Screen deployment in Spain, using an interval of 6  days, presented a noso- in double occupancy rooms is another hygiene measure comial rate of 2.5% [13]. Percentages of nosocomial cases needing to be improved in our hospital. Indeed, in the reported in 2 urology departments in Spain [14], a diges- first cluster, all the nosocomial cases were acquired in tive surgery department in Paris [15], an orthopeadic sur- double occupancy rooms. Transmission from one patient gery department in Spain [16] and a university Hospital to another sharing the same room, especially in SARS- in London [17] were 2.1%, 4.9%, 6.5% and 11.3% respec- CoV-2 with droplet transmission, is hard to control. This tively. A study conducted in a large US Academic medical constitutes a huge challenge for our institution insofar as center found 2 nosocomial cases among 697 COVID- 65% of the rooms are double occupancy. Hygiene audits 19 positive patients [18]. Finally, a study in three acute have shown a patient compliance rate of 81.5% for wear- hospitals in Scotland found 19 (11%) nosocomial cases ing a surgical mask when they moved or during care. among 173 COVID-19 positive patients [19]. In compari- In France, citizens are not used to wearing masks when son with influenza nosocomial cases, a meta-analysis [20] they present respiratory symptoms or when they are in showed that the proportion of nosocomial cases among closed and crowded spaces; use of masks is generally lim- the total number of patients with influenza ranged from ited to healthcare settings. In the second cluster, patient 15 to 59%. We can suggest two hypotheses to explain behavior may have influenced transmission. In the Mood these differences and the low rate of COVID-19 nosoco - Disorder unit, many manual activities shared between mial cases. First, the COVID-19 incidence rate in Greno- patients and HCWs such as card games or manual artis- ble during the first wave was rather low. However, other tic activities are part of the treatment. Moreover, patients factors may also explain these results, including hygiene admitted in the 2 units with clusters are mainly psychi- measures. During the COVID-19 outbreak, HCWs atric patients or patients with social difficulties. These and patients systematically wore masks, which was not units are at risk for cross-transmission because of major the case in the influenza epidemic. According to these patient turnover, patients with difficulties complying with results, universal wearing of a surgical mask by HCWs instructions, shared spaces and wandering patients. In could be a way to control nosocomial transmission of res- our hospital, though there was no hand hygiene program piratory viruses [21]. Another hypothesis concerns the targeting patients, but information on barrier measures lockdown and the ban on visits, which was never imple- was provided on screens in halls and patient rooms. Con- mented during an influenza epidemic. Some studies have cerning the cluster where 7 HCWs were tested, 4 were evaluated the effect of non-pharmaceutical interventions infected. All patients and HCW were tested at the same including the lockdown and proved their efficiency [22, time, so we cannot draw conclusions on the chronol- 23]. In our study, all nosocomial cases were grouped ogy of transmission [27]. Furthermore, physical proxim- within the first 3  weeks of lockdown. As fourteen days ity between HCWs during breaks could also be a way of is the longest incubation time reported in the literature transmission. A phylogenetic study based on sequencing [24], we can suppose that the lockdown was efficient and could clarify these epidemiological links and confirm or helped to control nosocomial cases. It is important to not the existence of a single strain [28]. Of note, no clus- note that given the high proportion of double occupancy ter was identified in surgery units, probably due to the rooms in our hospital for patients and a HCW staff short - drastic reduction in their activity following the ban on age, quarantine of all exposed asymptomatic patients and elective surgery [29, 30]. Landoas  et al. Antimicrob Resist Infect Control (2021) 10:114 Page 7 of 8 Acknowledgements The strengths of our study are based on prospective We thank Alexis Baveux for his help in translating into English and Jeffrey data collection. The same data have been collected from Arsham for editing this manuscript. We are also indebted to all members of electronic medical records in our institution to follow the virology laboratory and infection control unit. nosocomial influenza cases, and we know this is a reliable Authors’ contributions and effective system [31]. Moreover, we were in touch AL, FC, MG, CG, MRM and CL conceptualized and designed the study. SL, BN with occupational health teams, infectious disease spe- and PM validated the analysis of SARS‑ CoV‑2. MLM, PP and OE validated the diagnosis of COVID‑19. AL, FC, MG and CL contributed to the bibliography. AL, cialists and biologists in case of diagnosis uncertainty. FC, MG and CL prepared the documents for the Ethics Committees. AL, FC, All of these factors should help to reinforce knowledge of MG, SL, BN, MLM, MRM and CL analysed and interpreted the data. AL, FC, MG this emerging disease, especially concerning nosocomial and CL drafted the manuscript. All authors have approved the final version of the manuscript. cases, which are poorly described in the literature. However this study has some limitations. First, our Funding definition of nosocomial cases was based on 5-day incu - None. bation, whereas the incubation time described by the Availability of data and materials WHO is 1 to 14  days [24], meaning that we may have The datasets used and/or analysed during the current study are available from defined patients as nosocomial cases whereas they were the corresponding author on reasonable request. not, or conversely. Given this wide range of incubation time, there is no optimum definition. We have chosen Declarations median incubation as a means of achieving early detec- Ethics approval and consent to participate tion of potential nosocomial clusters in view of prevent- Study ethics approval was obtained on 30 September 2020 (CECIC Rhône‑ ing further transmission, the objective being to avoid Alpes‑Auvergne, Clermont ‑Ferrand, IRB 5891). classifying a nosocomial case as community-acquired. Consent for publication Second, asymptomatic cases were not tested and system- Not applicable. atic screening 14 days after discharge was not performed, Competing interests certainly causing missed SARS-CoV-2 infections. Third, All authors report no conflicts of interest relevant to this article. An abstract our institution was relatively spared and did not have as containing partial data was presented at the ESCMID Conference on Coronavi‑ many cases of COVID-19 as other hospitals elsewhere. rus Disease (ECCVID), 2020, online conference. Finally, hygiene audits were performed after the lock- Author details down period and did not adequately reflect the reality of Infection Control Unit, Grenoble Alpes University Hospital, Grenoble, France. lockdown period. Grenoble Alpes University/CNRS, Grenoble INP, MESP TIM‑ C UMR 5525, Grenoble, France. Virology Laboratory, Grenoble Alpes University Hospital, Grenoble, France. Grenoble Alpes University/CNRS/CEA, Institut de Biologie Structurale (IBS), HIV and persistent viral infections, Grenoble, France. I nfec‑ Conclusions tious Diseases Department, Grenoble Alpes University Hospital, Grenoble, France. Hospital Hygiene Department, Pavilion E ‑ Grenoble Alpes University In healthcare facilities, nosocomial transmission of res- Hospital, CS 10217, 38043 Grenoble Cedex 9, France. piratory viruses is a major issue and SARS-CoV-2 is not exempt from nosocomial transmission [32]. Hygiene Received: 23 November 2020 Accepted: 20 July 2021 measures, especially mask wearing and hand hygiene, are fundamental to control cross-transmission, and training of HCWs is an obviously necessary means of achieving References good compliance. However, nosocomial transmission 1. Zhu N, Zhang D, Wang W, Li X, Yang B, Song J, et al. A novel corona‑ also depends on patient characteristics and their abil- virus from patients with pneumonia in China, 2019. N Engl J Med. ity to comply with prevention measures. A specific and 2020;382(8):727–33. 2. World Health Organisation. Coronavirus disease 2019 (COVID‑19) Situ‑ targeted policy should probably be established in units ation Report –51 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ admitting patients who have difficulties observing these coron aviru se/ situa tion‑ repor ts/ 20200 311‑ sitrep‑ 51‑ covid‑ 19. pdf measures (psychiatry, social medicine or even geriatrics), 3. Zheng Z, Peng F, Xu B, Zhao J, Liu H, Peng J, et al. Risk factors of critical & mortal COVID‑19 cases: a systematic literature review and meta‑analysis. J the objective being to effectively prevent nosocomial Infect. 2020;81(2):e16‑25. transmission. 4. World Health Organisation. Coronavirus disease (COVID‑19) Situation Report–132 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ coron aviru se/ situa tion‑ repor ts/ 20200 531‑ covid‑ 19‑ sitrep‑ 132. pdf? sfvrsn= Abbreviations d9c2e aef_2 CHU‑ GA: Grenoble Alpes University Hospital; COVID‑19: Coronavirus disease 5. World Health Organisation. Modes of transmission of virus causing 19; CT‑scan: Computed tomographic scan; HCW: Healthcare workers; ICU: COVID‑19: implications for IPC precaution recommendations. Scientific Intensive care units; IQR: Interquartile range; ORION: Outbreak Reports and brief. 2020 [Internet]. https:// www. who. int/ news‑ room/ comme ntari es/ Intervention studies of Nosocomial infection; RT‑PCR: Reverse transcription detail/ modes‑ of‑ trans missi on‑ of virus‑‑ causi ng‑ covid‑ 19‑ impli catio ns‑ for‑ polymerase chain reaction; SARS‑ CoV‑2: Severe Acute Respiratory Syndrome ipc‑ preca ution‑ recom menda tions coronavirus 2; WHO: World Health Organization. Landoas et al. Antimicrob Resist Infect Control (2021) 10:114 Page 8 of 8 6. World Health Organisation. Clinical management of severe acute respira‑ 20. Voirin N, Barret B, Metzger M‑H, Vanhems P. Hospital‑acquired influenza: tory infection when novel coronavirus (2019‑nCoV ) infection is suspected a synthesis using the Outbreak Reports and Intervention Studies of [Internet]. https:// apps. who. int/ iris/ bitst ream/ handle/ 10665/ 330893/ Nosocomial Infection (ORION) statement. J Hosp Infect. 2009;71(1):1–14. WHO‑ nCoV‑ Clini cal‑ 2020.3‑ eng. pdf? seque nce= 1& isAll owed=y 21. Ambrosch A, Rockmann F, Klawonn F, Lampl B. Eec ff t of a strict hygiene 7. Haut Conseil de la Santé Publique. Avis relatif à la rationalisation de bundle for the prevention of nosocomial transmission of SARS‑ CoV‑2 in l’utilisation des masques chirurgicaux anti‑projections et des masques the hospital: a practical approach from the field. J Infect Public Health. filtrant de type FFP2 pour les professionnels de santé en établissements 2020;13(12):1862–7. de santé, en établissements médico‑sociaux et en ville en période épi‑ 22. Hsiang S, Allen D, Annan‑Phan S, Bell K, Bolliger I, Chong T, et al. The effect démique de stade 3: 10 of large‑scale anti‑ contagion policies on the COVID‑19 pandemic. Nature. 8. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features of 2020;584(7820):262–7. patients infected with 2019 novel coronavirus in Wuhan. China Lancet 23. Flaxman S, Mishra S, Gandy A, Unwin HJT, Mellan TA, Coupland H, et al. Lond Engl. 2020;395(10223):497–506. Estimating the effects of non‑pharmaceutical interventions on COVID ‑19 9. Lauer SA, Grantz KH, Bi Q, Jones FK, Zheng Q, Meredith HR, et al. The in Europe. Nature. 2020;584(7820):257–61. incubation period of coronavirus disease 2019 (COVID‑19) from publicly 24. World Health Organisation. Coronavirus disease 2019 (COVID‑19) Situ‑ reported confirmed cases: estimation and application. Ann Intern Med. ation Report –73 [Internet]. https:// www. who. int/ docs/ defau lt‑ source/ 2020;172(9):577–82.coron aviru se/ situa tion‑ repor ts/ 20200 402‑ sitrep‑ 73‑ Covid‑ 19. pdf 10. Stone SP, Cooper BS, Kibbler CC, Cookson BD, Roberts JA, Medley GF, et al. 25. Akram MZ. Inanimate surfaces as potential source of 2019‑nCoV spread The ORION statement: guidelines for transparent reporting of outbreak and their disinfection with biocidal agents. Virusdisease. 2020;31(2):94–6. reports and intervention studies of nosocomial infection. Lancet Infect 26. Seto WH, Tsang D, Yung RWH, Ching TY, Ng TK, Ho M, et al. Eec ff tiveness Dis. 2007;7(4):282–8. of precautions against droplets and contact in prevention of nosocomial 11. Zhou Q, Gao Y, Wang X, Liu R, Du P, Wang X, et al. Nosocomial infections transmission of severe acute respiratory syndrome (SARS). Lancet Lond among patients with COVID‑19, SARS and MERS: a rapid review and Engl. 2003;361(9368):1519–20. meta‑analysis. Ann Transl Med. 2020;8(10):629. 27. Huttunen R, Syrjänen J. Healthcare workers as vectors of infectious 12. Harada S, Uno S, Ando T, Iida M, Takano Y, Ishibashi Y, et al. Control of a diseases. Eur J Clin Microbiol Infect Dis Off Publ Eur Soc Clin Microbiol. nosocomial outbreak of COVID‑19 in a University Hospital. Open Forum 2014;33(9):1477–88. Infect Dis. 2020;7(12):512. 28. Meredith LW, Hamilton WL, Warne B, Houldcroft CJ, Hosmillo M, Jahun 13. Gras‑ Valentí P, Mora‑Muriel JG, Chico ‑Sánchez P, Algado ‑Sellés N, Soler ‑ AS, et al. Rapid implementation of SARS‑ CoV‑2 sequencing to investigate Molina VM, Hernández‑Maldonado M, et al. Eec ff tivity of a program for cases of health‑ care associated COVID‑19: a prospective genomic surveil‑ the control and prevention of covid‑19 Healthcare ‑Associated Infections lance study. Lancet Infect Dis. 2020;20(11):1263–71. in a Spanish Academic Hospital. J Patient Saf. 2021;17(4):323–30. 29. Laux CJ, Bauer DE, Kohler A, Uçkay I, Farshad M. Disproportionate Case 14. Sánchez MD, Sánchez M, De La Morena JM, Ogaya‑Pinies G, Mateo E, reduction after ban of elective surgeries during the SARS‑ CoV‑2 pan‑ Moscatiello P, et al. Nosocomial SARS‑ CoV‑2 infection in urology depart ‑ demic. Clin Spine Surg. 2020;33(6):244–6. ments: results of a prospective multicentric study. Int J Urol Off J Jpn Urol 30. Burkhard J, Lacher S, Holy D, Schenk P, Schäfer C, Kahr P, et al. No Assoc. 2021;28(1):62–7. nosocomial transmission of SARS‑ CoV‑2 between Healthcare Workers in 15. Luong‑Nguyen M, Hermand H, Abdalla S, Cabrit N, Hobeika C, Brouquet Surgical Departments unexposed to Covid‑19 patients. Ann Case Rep. A, et al. Nosocomial infection with SARS‑ Cov‑2 within Departments of 2020;5(6):533. Digestive Surgery. J Visc Surg. 2020;157(3S1):S13–8. 31. Bocquet A, Wintenberger C, Lupo J, Morand P, Pavese P, Gallouche M, 16. Lakhani K, Minguell J, Guerra‑Farfán E, Lara Y, Jambrina U, Pijoan J, et al. et al. Description of an influenza outbreak in a French university hospital Nosocomial infection with SARS‑ CoV‑2 and main outcomes after surgery and risk factors of nosocomial influenza. Eur J Clin Microbiol Infect Dis. within an orthopaedic surgery department in a tertiary trauma centre in 2021;40(4):879–84. Spain. Int Orthop. 2020;44(12):2505–13. 32. Hui DS, Azhar EI, Kim Y‑ J, Memish ZA, Oh M‑D, Zumla A. Middle East 17. Taylor J, Rangaiah J, Narasimhan S, Clark J, Alexander Z, Manuel R, et al. respiratory syndrome coronavirus: risk factors and determinants of Nosocomial COVID‑19: experience from a large acute NHS Trust in South‑ primary, household, and nosocomial transmission. Lancet Infect Dis. West London. J Hosp Infect. 2020;106(3):621–5. 2018;18(8):e217–27. 18. Rhee C, Baker M, Vaidya V, Tucker R, Resnick A, Morris CA, et al. Incidence of nosocomial COVID‑19 in patients hospitalized at a large US Academic Publisher’s Note Medical Center. JAMA Netw Open. 2020;3(9):e2020498. Springer Nature remains neutral with regard to jurisdictional claims in pub‑ 19. Khan KS, Reed‑Embleton H, Lewis J, Saldanha J, Mahmud S. Does noso ‑ lished maps and institutional affiliations. comial COVID‑19 result in increased 30‑ day mortality? A multi‑ centre observational study to identify risk factors for worse outcomes in patients with COVID‑19. J Hosp Infect. 2021;107:91–4. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : fast, convenient online submission thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

Journal

Antimicrobial Resistance & Infection ControlSpringer Journals

Published: Aug 5, 2021

Keywords: SARS-CoV-2; COVID-19; Outbreak; Healthcare-associated infection; Mask; Hand hygiene

References