Abstract
Background
Vancomycin-resistant Enterococcus (VRE) and carbapenemase-producing Enterobacterales (CPE) cause outbreaks in hospitals and the community. There is limited literature on the clearance time of VRE and CPE colonization. We reported the natural clearance time of VRE and CPE among residents of the Residential Care Home for the Elderly (RCHE) and the factors associated with prolonged colonization.
Methods
This retrospective study reviewed cases of VRE and CPE colonization reported to the Centre for Health Protection, Department of Health, Hong Kong Special Administrative Region from 1 January, 2012 to 31 December, 2024. We reviewed the demographic characteristics and outcomes of the VRE and CPE cases when they were cleared of the bacteria or died during the follow-up period, up to 31 December 2024. Clearance of VRE and CPE was defined as negative culture results for at least two and three consecutive specimens collected at least 48 h apart at the RCHE respectively. We compared the clearance time of VRE and CPE using the Kaplan–Meier method and determined the factors influencing the duration of clearance by univariate and multiple Cox regression.
Results
A total of 3626 VRE cases and 4434 CPE cases were followed up. CPE cases tended to be older and had a higher proportion of females compared to VRE cases. There was no statistical difference in the types of homes between the two groups. The mortality rate of VRE (25.7%) was similar to that of CPE (25.1%). It was found that the carriage duration of CPE was significantly longer than that of VRE, as tested by the log-rank test (p < 0.01). Half of the VRE and CPE cases will clear the bacteria by 85 days and 131 days, respectively. The carriage duration for the majority (90%) of VRE and CPE cases was 400 and 818 days, respectively. After adjusting for all associated factors, a longer length of stay for readmission to hospitals and lower occupancy rates in RCHEs were significantly associated with prolonged carriage status.
Conclusions
The natural clearance duration of VRE and CPE provides useful information to improve guidelines of screening of previously colonized patients, and duration of contact precautions to prevent transmission of these resistant organisms among the vulnerable groups.
Keywords: Antimicrobial resistance, Vancomycin-resistant Enterococcus, Carbapenemase-producing Enterobacterales, Epidemiology, Colonization, Infection control
Background
Vancomycin-resistant Enterococcus (VRE) and carbapenem-resistant Enterobacterales, most commonly due to carbapenemase-producing Enterobacterales (CPE), are emerging pathogens causing significant healthcare burden and have been listed as priority pathogens in the WHO bacterial priority pathogen list in 2024 [1]. Although Enterococci are normally found in the human intestines, female genital tract and the environment, VRE may result in severe opportunistic infections, such as bacteremia, endocarditis, and urinary tract infections, particularly in elderly and immunocompromised individuals. The surge in vancomycin-resistant Enterococcus faecium, attributed to the emergence of the clonal cluster 17 (CC17) genogroup, has led to hospital outbreaks worldwide, including in Hong Kong [2–7]. On the other hand, an increasing prevalence of CPE has been reported in Hong Kong with the predominance of blaNDM and blaIMP [8]. Similar to VRE, colonization of CPE may lead to serious clinical outcomes, including sepsis, pneumonia, meningitis, wound infections, and urinary tract infections. Elderly people staying in long-term care facilities are at higher risk of infections by multidrug-resistant organisms (MDRO), including VRE and CPE. In a systematic review involving 134 studies, old age, male sex, dementia, diabetes, cancer, chronic wounds, dependence, medical devices, previous antibiotic use, previous hospitalization, and previous MDRO colonization have been identified as risk factors for colonization by MDROs in long-term care facilities [9]. Outbreaks of VRE and CPE have been reported not only in hospitals but also in residential care homes for the elderly (RCHE) in Hong Kong [10–12]. RCHE are institutions that provide varying levels of care for aged people among whom about one-third of the residents were ambulatory and about one tenth were bed-ridden [13]. Over half of the residents have been reported to have more than one underlying co-morbidity such as hypertension, stroke, dementia and diabetes mellitus [13]. Stringent infection control by contact precautions is crucial to prevent the transmission of these MDROs among vulnerable groups in these settings.
For every case of VRE and CPE diagnosed at public hospitals in Hong Kong, the hospital infection control team notifies the Infection Control Branch (ICB) of the Centre for Health Protection, Department of Health, prior to the patient’s discharge to the RCHE, for preparation of the RCHE to take care of the residents who are VRE and CPE carriers. ICB has been providing training and education, published guidelines on handling these carriers in the RCHE for contact precautions including practice of proper hand hygiene, placement in a single room or cohorted in the same room or partitioned area; adoption of contact precautions for caring procedures; cleaning and disinfection of the environment with 1000 ppm sodium hypochlorite at least twice daily; use of dedicated equipment like blood pressure cuff and wheelchair; use of dedicated facilities such as own toilet and bathing facilities. If shared facilities are used, they must be thoroughly cleaned and disinfected after each use. On the other hand, a hospital infection control team is required to flag up newly diagnosed MDRO cases in the electronic Clinical Management System. This serves to alert frontline staff of the need for enhanced infection control precautions in case they are readmitted to the hospitals. The end of MDRO carriage is documented in the electronic system once the patient is cleared.
Currently, there is no effective decolonization therapy for VRE and CPE, and the prevention of these transmissions in RCHE mainly relies on strict infection control measures using barrier precautions, apart from standard precaution [14]. Therefore, the duration of colonization determines the length of time required to implement infection control measures in these settings. Extended colonization durations pose pressure on the workload of RCHE staff in Hong Kong. Unlike methicillin-resistant Staphylococcus aureus, for which natural clearance has been well documented, there is scanty literature on the clearance time of VRE and CPE colonization [15]. Previous studies have explored on the natural history and risk factors for VRE among hospitalized patients [16–18]. However, the duration of colonization and factors influencing the clearance (which represent getting below detection) of VRE and CPE in RCHEs have not been well established [19]. Therefore, we aimed to report the natural clearance time of VRE and CPE and to examine the associated factors for prolonged colonization among the RCHE residents.
Methods
Study design and epidemiological investigations
This retrospective study reviewed cases of VRE and CPE colonialization reported to the Centre for Health Protection, Department of Health, Hong Kong Special Administrative Region, from 1 January 2012 to 31 December 2024. We captured all cases reported by the hospital infection control teams of public hospitals under the Hospital Authority. Information on the characteristics of the RCHE where the carriers stayed, including the type, geographic location, capacity and occupancy was obtained from the Social Welfare Department. We followed up the colonization status for VRE and CPE monthly after the residents returned to the RCHE. Specimens were collected by the Community Geriatric Assessment Teams or Community Nursing Service under the Hospital Authority in the RCHE, and were sent to hospitals for laboratory testing. We reviewed the outcomes of the cases when they were cleared of VRE and CPE or when they died during the follow-up period, which extended to 31 December 2024 (Fig. 1). Data on the length of stay during subsequent hospital readmissions (readmission LOS) were obtained from the Clinical Data Analysis and Reporting System of the Hospital Authority, a comprehensive electronic database used for clinical data retrieval across public hospitals in Hong Kong. Our study was performed in accordance with the ethical standards of the Helsinki Declaration, which was accepted by the World Health Community in 1975 (revised in 2013).
Fig. 1.
Schematic diagram for follow up of vancomycin-resistant Enterococcus and carbapenemase-producing Enterobacterales cases
Laboratory methods for testing of VRE and CPE
For both VRE and CPE, stool specimens or rectal swabs were collected from residents monthly after their discharge to the RCHE. Additional specimens for screening may include urine from catheterized patients, swabs from open wounds and aspirates from drains. If antibiotics were administered, screening should be performed no sooner than 48 h after the completion of treatment. The specimens were cultured for VRE and CPE using selective media. For VRE, D-coccosel containing 4–6 mg/L vancomycin, chromogenic agar plates were used. For CPE, all Enterobacterales isolates were tested for carbapenem susceptibility. Isolates with reduced susceptibility were screened for carbapenemase with preliminary phenotypic confirmation, such as the modified carbapenem inactivation method or the Carba NP test. All suspected CPE isolates underwent carbapenemase detection by Polymerase Chain Reaction for carbapenemase gene and antigen detection using GeneXpert or Carba-5. Clearance of VRE and CPE was defined as negative culture results for at least two and three consecutive specimens collected at least 48 h apart at the RCHE respectively, including all previously positive body sites.
Statistical analysis
We compared the demographics of the cases reported between 2012 and 2024 and the characteristics of RCHE where the carriers resided, including type, geographic location, capacity and occupancy. Chi-square test was employed for comparing categorical data and Mann–Whitney U test was used for numeric data related to the characteristics of the cases and RCHEs. We also estimated the clearance probabilities of VRE and CPE carriers during the follow-up time using the Kaplan–Meier method. Patients who died during the follow-up were treated as censored events. All remaining patients were censored at the end of the study period (31 December 2024). The clearance duration was defined as the time from the date of the first positive specimen obtained in the hospital to the date of the third consecutive specimen negative for VRE or CPE. We compared the difference in clearance time between VRE and CPE cases using the log-rank test. In addition, Cox regression analysis was performed to examine factors that might affect clearance probability, including age, sex, MDRO type (VRE or CPE), RCHE region, RCHE type (private homes or non-private homes), RCHE size, RCHE occupancy and readmission LOS. Hazard ratios and corresponding 95% confidence intervals were transformed and expressed as percentage changes in clearance probability ([exp(coefficient) − 1]× 100%). Proportional hazards assumption for each factor was tested using the Schoenfeld residuals test. Factors not fulfilling the assumption in the univariate analysis were adjusted in the multivariate Cox regression model by stratification. For all analyses, a type I error rate of 0.05 was used. Statistical analyses were performed using R software (version 4.2.2) and the “survival” package (version 3.4–0).
Results
Figure 2 shows the number of cases reported annually from 2012 to 2024. There was an epidemic of VRE from 2013 to 2014, which subsequently subsided before rebounding in 2021. For CPE, there was a rising trend, especially since 2020 when the COVID-19 pandemic commenced, with a peak in the latter half of 2024. The characteristics of the VRE (n = 3626) and CPE cases (n = 4434) and their respective RCHE are presented in Table 1. CPE cases were older and included a higher proportion of females, while VRE cases tended to have a longer readmission LOS. The Kowloon region accounted for the highest proportion of CPE and VRE cases (VRE:63.2%; CPE:54.2%). The Hong Kong region had a higher proportion of CPE cases (30.7%) and a lower proportion of VRE (7.9%) compared to the New Territories (VRE:29.0%; CPE: 15.0%). There was no statistical difference in the types of homes between the two groups. Private homes accounted for over 70% (VRE: 76.4%; CPE: 75.6%). While no statistical difference was found in the capacity of RCHEs between the two groups, a higher proportion of RCHE had an occupancy > 80% among the CPE cases. During the follow-up period, 69.8% of VRE cases and 61.7% of CPE cases were cleared of bacteria. The mortality rates were similar for VRE (25.7%, 932/3626) and CPE (25.1%, 1115/4434).
Fig. 2.
Number of vancomycin-resistant Enterococcus and carbapenemase-producing Enterobacterales cases reported to Centre for Health Protection, 2012–2024
Table 1.
Descriptive analysis of MDRO cases (Jan 2012–Dec 2024)
| Predictors | MDRO (n (Column %)) | p value | ||
|---|---|---|---|---|
| VRE (n = 3626) | CPE (n = 4434) | |||
| Age group | < 65 | 295 (8.1%) | 376 (8.5%) | < 0.01 |
| 65–84 | 1721 (47.5%) | 1893 (42.7%) | ||
| ≥ 85 | 1610 (44.4%) | 2165 (48.8%) | ||
| Sex | Female | 1070 (29.5%) | 2039 (46.0%) | < 0.01 |
| Male | 2556 (70.5%) | 2395 (54.0%) | ||
| Readmission LOS | 0 day | 317 (8.7%) | 524 (11.8%) | < 0.01 |
| 1–45 days | 1551 (42.8%) | 2071 (46.7%) | ||
| > 45 days | 1758 (48.5%) | 1839 (41.5%) | ||
| Region | Hong Kong | 285 (7.9%) | 1362 (30.7%) | < 0.01 |
| Kowloon | 2290 (63.2%) | 2405 (54.2%) | ||
| New Territories | 1051 (29.0%) | 667 (15.0%) | ||
| RCHE type | Non-private | 855 (23.6%) | 1084 (24.4%) | 0.38 |
| Private | 2771 (76.4%) | 3350 (75.6%) | ||
| RCHE capacity (number of RCHE residents) | < 85 | 1051 (29.0%) | 1441 (32.5%) | 0.12 |
| 85–150 | 1393 (38.4%) | 1682 (37.9%) | ||
| > 150 | 1182 (32.6%) | 1311 (29.6%) | ||
| RCHE occupancy | < 60% | 907 (25.0%) | 1134 (25.6%) | < 0.01 |
| 60–80% | 1135 (31.3%) | 1294 (29.2%) | ||
| > 80% | 1584 (43.7%) | 2006 (45.2%) | ||
| Outcome | Clear | 2530 (69.8%) | 2737 (61.7%) | < 0.01 |
| Censored (death) | 932 (25.7%) | 1115 (25.1%) | ||
| Censored | 164 (4.5%) | 582 (13.1%) | ||
Among the 3626 VRE cases followed up, 3575 cases were identified during hospitalisation, the median number of specimen collected was 5, with IQR being 3–8. For the remaining 51 VRE cases, the relevant specimen records were not available. Among the 4434 CPE cases followed up, 4319 cases were identified during hospitalisation, median number of specimen collected was 5, with IQR being 4–8. For the remaining CPE 115 cases, the relevant specimen records were not available. There are 57.4% (2051/3575 VRE cases) and 48.7% (2104/4319 CPE cases) of VRE and CPE cases respectively that had samples collected every month during the study period. The median (IQR) time between sample collection are 8 days (4–25 days) for VRE cases and 12 days (5–30 days) for CPE cases. There was no significant change in the clearance time of VRE and CPE between 2012 and 2024 (Fig. 3). Figure 4 shows the Kaplan–Meier curve for clearance time of the two bacteria. It was found that the carriage duration of CPE was significantly longer than that of VRE, as indicated by the log-rank test (p < 0.01). Half of the VRE and CPE cases will clear the bacteria by 85 and 131 days, respectively. The carriage duration for 90% of VRE and CPE cases was 400 and 818 days, respectively. In the univariate analysis, apart from the MDRO type, readmission LOS, RCHE region and occupancy were significantly associated with the clearance time (Table 2). In the multivariate regression model, after adjusting for all associated factors, readmission LOS and RCHE occupancy were found to be significantly associated with the duration of clearance (Table 2). Longer readmission LOS and lower RCHE occupancy were associated with longer carriage duration.
Fig. 3.
Time of natural clearance of vancomycin-resistant Enterococcus and carbapenemase-producing Enterobacterales cases by year, 2012–2024
Fig. 4.
Kaplan–Meier estimate of the clearance time for vancomycin resistant Enterococcus and carbapenemase-producing Enterobacterales
Table 2.
Univariate and multivariate Cox regression analysis of factors influencing the clearance time of MDRO
| Predictors | Univariate analysis | Multivariate analysis | |||||
|---|---|---|---|---|---|---|---|
| Change in clearance % | p value | PH assumption* | Change in clearance % | p value | PH assumption* | ||
| Sex | Female | (Reference) | – | 0.60 | (Reference) | – | 0.96 |
| Male | 2.31% (− 3.21–8.15%) | 0.42 | − 4.37% (− 9.83–1.41%) | 0.14 | |||
| Age group† | < 65 | (Reference) | – | < 0.01 | – | – | – |
| 65–84 | 12.42% (1.89–24.04%) | 0.02 | – | – | |||
| ≥ 85 | 10.01% (− 0.33–21.44%) | 0.06 | – | – | |||
| MDRO type† | VRE | (Reference) | – | < 0.01 | – | – | – |
| CPE | − 36.73% (− 40.08–− 33.19%) | < 0.01 | – | – | |||
| Readmission LOS | 0 days | (Reference) | – | 0.24 | (Reference) | – | 0.08 |
| 1–45 days | − 6.48% (− 15.05–2.94%) | 0.17 | − 5.50% (− 14.24–4.13%) | 0.25 | |||
| > 45 days | − 23.05% (− 30.01– − 15.39%) | < 0.01 | − 27.14% (− 33.81– − 19.80%) | < 0.01 | |||
| RCHE region† | Hong Kong | (Reference) | – | < 0.01 | – | – | – |
| Kowloon | 40.79% (31.17–51.12%) | < 0.01 | – | – | |||
| New Territories | 17.41% (7.72–27.98%) | < 0.01 | – | – | |||
| RCHE type† | Non-Private | (Reference) | – | < 0.01 | – | – | – |
| Private | − 0.85% (− 6.95–5.64%) | 0.79 | – | – | |||
| RCHE capacity | < 85 | (Reference) | – | 0.02 | (Reference) | – | 0.54 |
| 85–150 | − 2.62% (− 9.45–4.71%) | 0.47 | 1.56% (− 6.22–9.98%) | 0.70 | |||
| > 150 | 0.40% (− 6.11–7.36%) | 0.91 | 4.74% (− 2.97–13.07%) | 0.24 | |||
| RCHE occupancy | < 60% | (Reference) | – | 0.04 | (Reference) | – | 0.68 |
| 60–80% | 9.13% (2.19–16.55%) | 0.01 | 8.26% (1.06–15.97%) | 0.02 | |||
| > 80% | 14.42% (6.80–22.59%) | < 0.01 | 17.74% (7.55–28.90%) | < 0.01 | |||
*P value < 0.05 suggests violation of proportional hazard (PH) assumption
†Predictors violated the PH assumption are addressed in the multivariate model by stratification
Discussion
To the best of our knowledge, this is the largest study to report the duration of natural clearance for VRE and CPE involving over 8000 residents in long-term care settings. We estimated that half of the VRE and CPE cases would be cleared by 85 and 131 days, respectively. It takes over 2 years for the majority (90%) of CPE cases and over 1 year for the majority of VRE cases to clear the bacteria. The longer the duration of natural clearance of VRE and CPE, the longer the residents must remain under contact precaution. This has important manpower and resource implications in the RCHE, which are usually less favorable when compared with hospital settings, and hence pose a higher risk of transmission of resistant bacteria among these vulnerable groups.
Most previous studies on VRE colonization were conducted in hospital settings. A systematic review pooling data from 13 studies identified a wide range of VRE clearance times from 1 to 43 weeks [20]. Using a logistic regression model, the review estimated that 50% of the subjects cleared colonization at 25 weeks after the initial positive stool test [20]. This apparent longer colonization period (compared with about 12 weeks in the current study) could be attributed to selective pressure during hospitalization where antimicrobials were often administered to select out the resistant organisms, resulting in persistent colonization. However, the lack of a consistent definition of clearance, uncertainties regarding the timing of initial colonization, variations in the sampling frequency for monitoring the clearance status, variation in the laboratory methods used and follow-up duration have limited the external validity of these studies. In a community study involving 127 patients discharged from hospitals, the median time to clearance after hospital discharge was 62 days, which is similar to the current study findings [19]. Other studies have reported persistent colonization for up to 2–3 years [17, 21]. On the contrary, there is scanty literature reporting the clearance time of CPE. In a study involving 142 known CPE-colonized patients, carriers underwent follow-up perirectal cultures no sooner than 8 weeks after the initial positive culture, at an outpatient clinic visit or upon readmission to the hospital. Results showed that only 17 patients had 3 consecutive negative follow-up perirectal cultures with re-positive cases found at 7–8 months without clear documentation of the clearance time [22]. In another hospital study that censored patients at discharge, only 12 out of 147 patients met the definition of CPE clearance and the median time from identification to clearance was 27.5 days [23]. Figure 3 illustrates the time to natural clearance of VRE and CPE cases from 2012 to 2024, excluding censored cases, i.e. patients who died before clearance or remained positive at study end. In contrast, Fig. 4 presents the Kaplan–Meier estimate of clearance time for VRE and CPE including all censored cases. Because Fig. 3 excludes censored cases, it presents a shortened estimate of the median clearance time compared to Fig. 4 since the cases might still be positive should they have not died or followed up for a longer period.
In the multivariate Cox regression model, we demonstrated that length of stay in readmission was significantly associated with a longer duration of carriage. It has been shown that prolonged hospitalization is an associated factor for MDRO colonization [16]. Other studies have shown that factors influencing the duration of VRE colonization in hospitals, including immunosuppressed patients [19, 24–26]. and antibiotic use in particular vancomycin and fluoroquinolone [19, 27, 28]. Non-clearance of CPE was shown to be significantly associated with KPC CPE in previous studies [23, 29]. The frequent and co-occurrence of major risk factors makes residents of long-term care facilities more vulnerable to colonization and infections by multi-drug resistant bacteria, in particular, the previous antibiotics usage such as fluoroquinolones and extended-spectrum cephalosporins, presence of invasive medical devices, old age and the degree of dependence on nursing care [30]. Besides, facility risk factors including crowded condition as reflected by high number of residents per bedroom, inadequate staffing, high staff turnover, limited hand washing facilities have been reported to contribute to colonization and transmission of the resistant bacteria [30, 31]. Yet, the paradoxical finding of longer colonization associated with lower RCHE occupancy could not be fully explained in our study.
The time of clearance may vary if the definition of clearance differs in terms of the number and interval for sample taking. In this study, we defined the time to clearance as at least three consecutive negative cultures collected monthly. Other studies required three negative cultures, which should be tested at least 1 week apart [16, 17, 19, 32, 33] while it was defined as two consecutive negative cultures in one study [32]. Hence, the clearance time might have been slightly overestimated in this study when compared with other studies that had a shorter time interval of sample taking.
Members of the order Enterobacterales and the genus Enterococcus usually constitute a small proportion of the healthy gut microbiota in human [34]. The symbiotic relationships with other members of the microbiota limit the growth of multi-drug resistant bacterial strains such as VRE and CPE via direct or indirect inhibition, known as colonization resistance [35]. However, if the alpha diversity of gut microbiota (summarizing the mean species diversity) is altered, overgrowth of resistant strains of Enterobacterales and Enterococci may occur [36, 37]. Risk factors for VRE and CPE colonization include conditions that disrupt the normal microbial flora, such as antibiotic use, hospitalization, discharge to a long-term care facility, or dialysis [19, 27, 38, 39]. Despite both VRE and CPE being colonized in the gut, we documented the different trajectory of clearance as reflected in the Kaplan–Meier curves. It is worth further exploring the underlying microbiological mechanisms that may help unveil the potential for decolonization therapy.
Apart from the large sample size involving over 8000 residents, another strength of the present study was the longest follow-up duration of 13 years from 2012 to 2024. Unlike the hospital studies that censored patients when discharged, we monitored the colonization status of the residents until they fulfilled the definition of clearance or died. Compared with other studies that counted the date of colonization from hospital discharge, our present study counted the reporting date by the 1st positive specimen which were usually earlier than the hospital discharge date and hence the closer to the real acquisition time of the VRE and CPE. Besides, we included all cases reported by all public hospitals in Hong Kong, meaning that selection bias should be minimal. Yet, there are a couple of limitations of this research. Firstly, this was a retrospective study and information such as the exact time of acquisition of colonization, co-morbidity of residents and antibiotic intake was not available for analysis. Secondly, the following up samples were collected at monthly intervals. If more frequent tests had been performed, a more precise clearance time would have been detected. Nevertheless, more frequent tests would require significant resources and frequent disturbances to the residents.
Conclusions
In this large retrospective study among RCHE residents, we found that CPE had a longer average carriage time of 131 days than VRE of 85 days, while the 90% of the cases could be cleared naturally by 818 days and 400 days, respectively. Length of stay for readmission to hospitals and RCHE occupancy were associated factors for prolonged carriage of these resistant bacteria. The natural duration of clearance would provide useful information to improve guidelines of screening of previously colonized patients, and duration of contact precautions to prevent transmission of these resistant organisms among the vulnerable groups.
Acknowledgements
We would like to thank you the community geriatric assessment team to take the specimens and laboratory staff in the hospitals for conducting the laboratory tests.
Author contributions
EM conceptualized the study design. RL and VC were responsible for coordinating the specimens taking by the hospital outreaching teams and laboratory testing in the hospitals. BS and LL coordinate the monitoring of clearance status of RCHE residents. EH and EK performed the data analysis. EM wrote the manuscript with inputs from all authors. All authors read and approved the final manuscript.
Funding
None reported.
Data availability
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Declarations
Ethics approval and consent to participate
As a public health and quality improvement initiative, this surveillance program was exempt from human participant research oversight by the Centre for Health Protection, Department of Health of the HKSAR. The study was performed in accordance with the ethical standards of the Helsinki Declaration, which was accepted by the World Health Community in 1975 (revised in 2013).
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.