Original article
Lyme borreliosis incidence in Lombardy, Italy (2000–2015): Spatiotemporal analysis and environmental risk factors

https://doi.org/10.1016/j.ttbdis.2019.07.001Get rights and content

Abstract

Lyme borreliosis cases have been reported from Lombardy in northern Italy, where Ixodes ricinus is the main vector of Borrelia burgdorferi sensu lato. However, spatial and temporal variation in the incidence of Lyme borreliosis is not well understood. In the present study, based on new notified cases of Lyme borreliosis from 2000 to 2015, an average of 1.24 new cases per million residents per year was documented. New cases, georeferenced at the municipal level, were analyzed by retrospective space-time analysis (using SaTScan v. 9.3.1); and land cover, extrapolated from a Corine Land Cover dataset (using QGIS 2.8.1), was used to implement an environmental risk factor analysis. Firstly, a temporal high-risk cluster was detected in Lombardy: the relative risk of Lyme borreliosis was 3.73 times higher during 2008–2015 compared with the entire study period. Moreover, in a spatiotemporal high-risk cluster with a circular base, land cover consisting of wildland-urban interface, meadow, forest and meadow-forest transition were significantly higher compared to low-risk areas. Results of the present study demonstrate that the incidence of Lyme borreliosis is increasing in Lombardy and that environmental conditions are suitable for I. ricinus ticks infected with B. burgdorferi s.l.: citizens and health systems should be aware of Lyme borreliosis to reduce tick bites with personal protective behaviors and to avoid misdiagnosis, particularly within the area including the observed high-risk cluster. Economic resources should be invested to inform about methods to prevent tick bites, how to check people and pets after frequenting risk areas, and ways of removing the biting ticks when they are found.

Introduction

The Borrelia burgdorferi sensu lato (s.l.) complex includes several causative agents of Lyme borreliosis in Western Europe, where the hard tick Ixodes ricinus is the main vector. The incidence of tick-borne diseases is increasing worldwide, and this trend has been widely documented for Lyme borreliosis (Rizzoli et al., 2011; Kugeler et al., 2015). Lyme borreliosis eco-epidemiology is complex as it depends on: tick development and survival; abundance of vertebrates serving as spirochete reservoirs; hosts that contribute to the spread of the tick; and human exposure to tick-bites (Kilpatrick et al., 2017). All these factors are linked to environmental features, and geospatial analysis tools have proved to be helpful in the understanding of tick-borne disease epidemiology (Svec et al., 2013).

In Italy, the first case of Lyme borreliosis was recorded in northern Italy in 1983 (Crovato et al., 1985) and since then most new cases have been observed in the Liguria, Friuli-Venezia Giulia, and Trentino-Alto Adige regions (Cimmino et al., 1992; Pavan et al., 2000; Nazzi et al., 2010). At present, these northern regions have higher incidence of Lyme borreliosis compared to central and southern Italy, where Lyme borreliosis appears to be hypoendemic (Santino et al., 1995, 1996; Fazii and Riario Sforza, 1999). Some regions of northern Italy, such as Piedmont and Lombardy, also have low incidence or report only sporadic cases (Orani and Sala, 1994; Casabianca et al., 1996). Following the increase of diagnosed cases since 1983, the Ministry of Health included Lyme borreliosis in the list of notifiable diseases in 1992. In Lombardy, the most populous region of Italy, I. ricinus has long been known to be present and B. burgdorferi s.l. spirochetes have been detected in this tick (Scali et al., 2001; Pistone et al., 2010; Olivieri et al., 2017). Despite this, the epidemiology and spatial distribution of Lyme borreliosis cases are poorly understood, and the regional trend of disease incidence has not been described. To fill these knowledge gaps, the present study aimed to evaluate i) the incidence of Lyme borreliosis in the resident population of Lombardy from 2000 to 2015; ii) the distribution of new cases with a retrospective spatiotemporal analysis; and iii) the existence of environmental predictors for disease incidence. To address these research questions, new cases of Lyme borreliosis, georeferenced at the municipal level, were analyzed by space-time scan statistic (Kulldorff, 1997) followed by an environmental risk factors analysis based on a Corine Land Cover dataset.

Section snippets

Study area and data sources

Lombardy is a region of northern Italy (Latitude: 45°40′ N; Longitude: 9°30′ E), covering 23,863.7 km2 and divided into 12 provinces (Fig. 1). It is the most populous region of Italy, with a population density of 419.7 inhabitants per km2. The health care system is regionally managed in Italy, and notifiable diseases are recorded at the regional level. For the study, new notified cases of Lyme borreliosis in the resident population from 2000 (January the 1 st) to 2015 (December the 31 st) were

Results

In the 16 years from 2000 to 2015, 189 new cases of Lyme borreliosis were recorded in the resident population of the Lombardy Region (11.8 new cases/year). The resident population amounted to 9,523,648 people: an average of 1.24 new cases per million of residents per year was observed. The spatial distribution of municipalities in which these cases were recorded is shown in Fig. 2. The annual incidence across the study period varied from 0.3 (minimum, observed in 2005) to 2.6 (maximum, observed

Discussion

According to Sykes and Makiello (2017), the incidence of Lyme borreliosis in Italy during 2001–2015 was 0.01 new cases per million of resident population/year, but the disease is probably underdiagnosed and underreported. During our study period (2000–2015), 1.24 new cases per million residents/year were observed in Lombardy. Noticeable differences were documented both between years and between provinces (Fig. 3): the annual incidence for 2014 was 2.61, more than twice the average for

Conclusions

In conclusion, the results presented in this study showed that the incidence of Lyme borreliosis in Lombardy is higher than the estimates previously proposed for Italy (Sykes and Makiello, 2017). Increasing incidence of Lyme borreliosis must be taken into account by healthcare practitioners, who should always consider a differential diagnosis with Lyme borreliosis in patients with compatible clinical symptoms. Further, medical staff should always be encouraged to report cases of the disease,

Acknowledgments

The authors are grateful to Marco Farioli and Alessandra Piatti (Regione Lombardia). The opinions expressed herein are those of the authors; endorsement by Regione Lombardia is not intended nor should be inferred. The authors are grateful to prof. Giusto Trevisan (Ospedale Maggiore di Trieste) for his support.

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