The establishment of the SO-ZI/AMR in 2012 has resulted in a monthly transparent overview of nosocomial outbreaks in the Netherlands. Our results suggest that outbreaks with HRMO and other pathogens occurred regularly in Dutch healthcare settings in the past ten years, but that they mostly remained limited in size and were usually quickly controlled. The most frequently reported causative microorganisms were MRSA, VRE (in hospitals) and highly resistant Enterobacterales.

In the Netherlands, a combination of restrictive antibiotic use, high standards of hospital infection prevention and control, nationwide surveillance and an active MRSA search-and-destroy policy has proven to be able to limit MRSA prevalence and spread, as compared to other countries [13]. Accordingly, hospital MRSA outbreaks in our study were small and remained in phase 1/2. Carbapenemase-producing Enterobacterales, P. aeruginosa and Acinetobacter baumannii are considered as most feared HRMO since they can cause severe infections for which limited therapeutic options are available. Although the prevalence of CPE slowly increases in the Netherlands [6], the number of CPE outbreaks remains limited. The Dutch national bacterial pathogen surveillance showed that the CPE population is dynamic and diverse, suggesting that it is based on multiple introductions in the Netherlands rather than largescale within-country transmission [14]. In our data, outbreaks of carbapenemase-producing K. pneumoniae were more frequently reported than of carbapenemase-producing E. coli, which is in line with their increased ability of transmission [15]. In 2018, we noticed an increase in outbreaks caused by highly resistant Enterobacterales, and for the first time, an outbreak (NDM-producing C. freundii) was classified as phase 4. This outbreak was carefully monitored and the reporting hospital was offered support.

We compared our data with those from other countries. Norway, a country with similar resistance rates as the Netherlands [13], has implemented a web-based outbreak notification system, which is based on mandatory notification using criteria that differ from the SO-ZI/AMR, and is not limited to nosocomial outbreaks. They reported 157 nosocomial outbreaks in 2019, of which 17 (11%) were caused by highly resistant bacterial pathogens [16]. Although comparison with our data is not straightforward because of the differing notification criteria, this is considerably lower than the number of HRMO outbreaks we found in the same year (n = 52). However, taking into account the difference in the number of hospital and LTCF beds between Norway and the Netherlands (54,825 vs. 230,364, respectively, data from hospitals in 2019 and LTCF from 2012 [17,18,19]), the HRMO outbreak incidence is comparable with our data (31 vs. 23 per 100,000 beds in the respective countries). Germany reported 54 nosocomial outbreaks with HRMO bacteria between 1 November 2011 and 31 October 2012 [20]. However, the authors expect that many outbreaks were not reported during this pilot phase of the system, due to a narrow outbreak definition or lack of awareness on the hospital side. In our data, outbreaks of CPE, P. aeruginosa, and Acinetobacter species were rare and included few patients. In contrast, large outbreaks with these HRMO were reported in other countries in both Europe and the rest of the world, as confirmed in literature and in the Worldwide Outbreak Database, a database claiming to include all outbreak reports from medical literature in a standardised manner [21]. The moderate outbreak frequency in the Netherlands is probably associated with the low prevalence of these HRMO in the Netherlands and high standards of infection prevention which include the screening of high-risk patients upon hospital admittance (i.e. recent hospitalisation abroad). This allows healthcare facilities to take targeted control measures – e.g. isolation of all colonised or infected patients and exchange of information upon transfer between hospitals.

Since the establishment of the SO-ZI/AMR, valuable insights have been gained in the characteristics of outbreaks of (highly resistant) pathogens in Dutch healthcare settings, such as the severity, duration and causative agents. Furthermore, the SO-ZI/AMR contributes to an open communication which is essential in minimizing the public health threat of nosocomial outbreaks. Although the reporting to and monitoring by the SO-ZI/AMR may have contributed to increased awareness and thereby to controlling the outbreak in terms of limiting the duration or size of outbreaks, the true impact of the structure cannot be quantified with the available data. In 2017, an external qualitative evaluation of the SO-ZI/AMR was performed. As there were no outbreaks classified as phase 4/5 until 2017, the role of the SO-ZI/AMR in providing support and facilitating communication between healthcare facilities could not be evaluated and evaluation was focussed mainly on the signalling role of the SO-ZI/AMR. The central assessment of the severity of outbreaks by the SO-ZI/AMR as an authoritative body was perceived as one of the strengths of the structure. The fact that outbreaks in phase 1–3 are not followed by sanctions imposed by healthcare authorities, helps to normalise the fact that outbreaks in healthcare occur, which contributes to transparency and willingness to report and share information. The signalling function of the SO-ZI/AMR was also relevant when multiple outbreaks with NDM-producing K. pneumoniae and VIM-producing P. aeruginosa were noticed [22, 23]. The SO-ZI/AMR suggested the hospitals with an active outbreak of NDM-producing K. pneumoniae to share typing data and experience, including effectiveness of control measures, in order to help each other in further controlling the outbreaks. When multiple VIM-producing P. aeruginosa outbreaks occurred in one region of the country during a specific period, a meeting between the affected hospitals was initiated to investigate possible causes and infection control measures. The SO-ZI/AMR reported on the outcome of this meeting in their monthly bulletin, in order to inform other healthcare professionals. In these outbreaks, VIM-producing P. aeruginosa was suggested to be associated with previous use of antibiotics and persistence in environmental hospital sources [24,25,26]. Nationwide efforts are now undertaken to better understand these environmental sources and to contain these [27,28,29,30].

Our results also have limitations. First, our data may have suboptimal representativeness. Due to the voluntary nature of the SO-ZI/AMR and the narrow notification criteria, smaller outbreaks - that were quickly controlled and did not lead to potential ward closure – may not have been reported. One might argue that the likelihood of reporting depends on resource availability, IPC expertise, scientific interest, etc. During the period of the study, the overall median number of reported outbreaks reported per institute was 11 (range 3–23) for university hospitals, 3 (range 1–16) for non-university hospitals and 1 (range (1–3) for LTCF. However, these differences in numbers of reported outbreaks may also reflect actual differences in outbreak occurrence in these settings. There was no evidence of large HRMO outbreaks that were not reported to the SO-ZI/AMR and the perception is that the overview of reported HRMO outbreaks is fairly complete. Suboptimal representativeness was more likely for LTCF than for hospitals. The reason for adding LTCF in 2015 was to gain more insight in HRMO prevalence and control in LTCF. In 2016, a point prevalence study was undertaken on ESBL carriage in LTCF residents [31]. This increased the active detection and reporting of ESBL outbreaks. Still, outbreak detection, contact tracing and reporting of outbreaks remained limited in LTCF. However, once in 2018 a financial reimbursement rule was installed for outbreaks of HRMO in LTCF for which notification of the outbreak to the SO-ZI/AMR was required [32], reporting increased. Thus, especially in the earlier years, we have missed outbreaks in LTCF. Data reported during the COVID-19 pandemic (2020–2021) are also prone to suboptimal representativeness., as the number of outbreaks reported in 2020 and 2021 was lower compared to the years before. Underreporting (since hospitals faced overwhelming patient influx during the various COVID-19 waves) in these years could have contributed to this observation. For instance, the number of SARS-CoV-2 outbreaks in hospitals and particularly LTCF was likely much higher than reported to the SO-ZI/AMR, considering the number of LTCF locations with at least 1 positive test over time [33]. Still, also lower transmission rates due to increased infection prevention measures and reduced travel-related HRMO carriers, might be an explanation for the lower numbers of reported HRMO outbreaks during the COVID-19 pandemic. With regard to our results on non-HRMO pathogens (including viruses), it is important to note that these outbreaks generally do not meet the notification criteria. Some of them were reported anyway, and the SO-ZI/AMR did not discard these. Therefore our data do not provide a complete overview of outbreaks for all pathogens presented in this paper. A second limitation that should be accounted for when interpreting our results is the lack of accurate data on the start and end date of the outbreaks. We therefore defined outbreak duration as the duration between the date of reporting and the date of the SO-ZI/AMR monthly meeting in which the outbreak was assigned Phase 0. As notification of outbreaks to the SO-ZI/AMR was only indicated when continuity of care was jeopardised or transmission was ongoing despite control measures, it is likely that outbreaks were reported some time after they had started. Also, some outbreaks were only reported after they had been controlled. It is therefore likely that the duration of outbreaks in our results is an underestimation. As a third and final limitation that should be mentioned, the severity phase classification by the SO-ZI/AMR was a collective decision based on the expert panel’s professional judgement and strict criteria were not in place. Assigned classifications were not externally validated.

In 2022, procedural updates to the SO-ZI/AMR were implemented. Notification criteria were updated to also include an outbreak definition, the number of severity phases was reduced from five to three and include objective definitions, and outbreaks are now reported through a dedicated secured web-based platform using a personal account.