Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany

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Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany R. Sassnau a,∗ , A. Daugschies b , M. Lendner b , C. Genchi c a b c

Hasenheide 65, D-10967 Berlin, Germany Institute of Parasitology, University of Leipzig, An den Tierkliniken 35 D-04103 Leipzig, Germany Department of Veterinary Sciences and Public Health, University of Milan, Via Celoria 10, 20133 Milano, Italy

a r t i c l e

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Article history: Received 10 April 2014 Received in revised form 23 June 2014 Accepted 27 June 2014 Keywords: Dirofilariosis Heartworm Dirofilaria immitis Dirofilaria repens Climate change Prevention Germany

a b s t r a c t Recently concerns are increasing that dirofilarial nematodes may spread from endemic areas in southern, eastern and central Europe to countries in northern regions of Europe. The increasing number of autochthonous cases of canine Dirofilaria repens infections in Germany indicates that worms of this genus may invade new areas, and climate change may be a key factor in this scenario. Thus analysis of long term development of regional temperature is a pivotal factor in risk analysis related to transmission of these worms. Such information is important for suggestions of counteracting strategies, such as definition of periods of increased transmission risk and, consequently, time slots most suited for preventative measures. In this study, mean daily temperature data from 34 geographical clustered weather stations representing all parts of Germany were analyzed. It is concluded that the increasing trend for average daily temperatures observed in the period from 1984 to 2013 has led to climatic conditions that allow the completion of dirofilarial life cycles in large parts of Germany between May and October. Autochthonous infection with D. repens is already established in some regions and targeted diagnosis and medical prophylaxis is advisable for dogs assumedly exposed during risk of transmission periods. It appears likely that global warming will support further spread of D. repens. Furthermore for the population of dogs the spread of the more pathogenic species D. immitis in hitherto non-endemic Germany is a potential risk if mean temperatures rise to a level suitable for parasite development in the abundant vector mosquitoes during the warmer seasons. © 2014 Elsevier B.V. All rights reserved.

1. Introduction “Heat adapted” parasites like Dirofilaria immitis and D. repens have their natural habitats in regions of higher average temperatures, e.g. southern European countries (Rossi

∗ Corresponding author. Tel.: +49 030 6936111. E-mail addresses: [email protected] (R. Sassnau), [email protected] (A. Daugschies), [email protected] (M. Lendner), [email protected] (C. Genchi).

et al., 1996). Dogs imported from such a regions or visiting endemic areas may carry these worms into non-endemic countries and D. repens has recently become endemic in large parts of central and eastern Europe with increasing cases in dogs and humans (Ermakova et al., 2014; ´ Osinska et al., 2014; Salamatin et al., 2013). Further, an increasing number of canine dirofilariosis as a “travel” disease aquired in southern and central Europe is reported for Germany (Hirsch and Pantchev, 2008; Pantchev et al., 2011) and it appears quite likely that many infection in dogs, particularly subclinical cases, remain undiagnosed

http://dx.doi.org/10.1016/j.vetpar.2014.06.034 0304-4017/© 2014 Elsevier B.V. All rights reserved.

Please cite this article in press as: Sassnau, R., et al., Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany. Vet. Parasitol. (2014), http://dx.doi.org/10.1016/j.vetpar.2014.06.034

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and thus untreated. These dogs may remain microfilaraemic for years (McCall et al., 2008) serving as potential reservoirs for transmission of the parasite to the competent mosquito vectors. The completion of the parasite life cycle and the transmission to dogs depends on larval development to the infective third stage (L3) in the vector. For this part of the life cycle, suitable environmental temperature is a critical factor (Genchi et al., 2009, 2011a; Brown et al., 2012). Due to global warming, average temperatures may reach a level suitable for completion of larval development of D. immitis and D. repens in the vector even in countries located in temperate zones such as Germany (Genchi et al., 2011b; Sassnau and Genchi, 2013). The presence of microfilaraemic dogs combined with suitable temperatures and general abundance of vectors are the basis for the spread of Dirofilaria spp. into previously non infected regions. Recently, 26 autochthonous cases of D. repens infection in dogs were reported from Southwest and Northeast Germany (Hermosilla et al., 2006; Pantchev et al., 2009; Sassnau et al., 2009, 2013; Kershaw et al., 2008; von Samson Himmelstjerna, 2013). The first autochthonous human infection in northern Germany was diagnosed in the spring of 2014 (Tappe et al., 2014). Moreover DNA of D. repens and D. immitis were lately detected in mosquitoes

trapped in Germany in 2011, 2012 and 2013 (Czajka et al., 2014; Kronefeld et al., 2014; Becker et al., 2014). These findings and the detection of DNA of D. repens in mosquitoes in Austria and Slovakia (Bocková et al., 2013; Silbermayr et al., 2014) underlines the assumption that dirofilarial infections are currently spreading to northern Europe. The aim of this study was to examine temperature data records in Germany collected over almost 30 years (1984–2013) to assess whether average temperature conditions have allowed the development of L3 in the arthropod vector and, if this is the case, to identify the regions where it is possible. Based on this analysis, the most suitable periods for a rational preventative strategy against heartworm disease and canine subcutaneous dirofilariosis are recommended.

2. Materials and methods Daily mean temperatures during the period of highest mosquito abundance (May 1st to October 15th) recorded by 34 stations of the German Weather Service (DWD) in the years 1984 to 2013 were used for the evaluation (Table 1). The weather stations were stratified into 6 geographic clus-

Table 1 Geographic origin of the Weather stations (DWD). Cluster

Name of the station

Longitude

Latitude

N N N N N N

Emden Bremen Hamburg-Fuhlsbuettel Hannover Schleswig Schwerin

7.23 8.8 9.99 9.68 9.55 11.39

53.39 53.05 53.64 52.47 54.53 53.64

0 4 11 55 43 59

NE NE NE NE NE

Berlin-Tempelhof Angermuende Potsdam Neuruppin Berge

13.4 13.99 13.06 12.81

52.47 53.03 52.38 52.91

48 54 81 38

E E E E E E

Cottbus Dresden-Klotzsche Goerlitz Leipzig-Schkeuditz Leipzig/Halle Erfurt-Weimar Magdeburg

14.32 13.77 14.95 12.22 12.24 10.96 11.58

51.78 51.13 51.16 51.42 51.44 50.98 52.1

69 222 238 133 131 316 76

SE SE SE SE SE SE

Nuernberg Munich-Airport Regensburg Weiden Wuerzburg Fuerstenzell

11.06 11.81 12.1 12.19 9.96

49.5 48.35 49.04 49.67 49.77

314 445.5 365.4 439.6 268

SW SW SW SW SW

Karlsruhe Rheinstetten Konstanz Mannheim Saarbruecken-Ensheim Trier-Petrisberg

8.37 8.33 9.19 8.56 7.11 6.66

49.04 48.97 47.68 49.51 49.21 49.75

111.6 116.1 442.5 96.1 320 265

W W W W W W

Duesseldorf Gießen/Wettenberg Kassel Cologne-Bonn Frankfurt/Main Muenster/Osnabrueck

6.77 8.65 9.44 7.16 8.6 7.7

51.3 50.6 51.3 50.87 50.05 52.14

36.6 202.7 231 92 112 47.8

Elevation(m)

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◦ days (DDU/30 defined as the sum of average daily  C valDDU, for ues exceeding 14 ◦ C over 30 successive days [ i = (i1 , i2 , . . . i30 ) hereafter referred to as ‘130 DDU/30  ]). We denominated this period of 30 suitable days for extrinsic development of one generation of L3 as “1P30 ”. The number of P30 was plotted in a line with scatter plot for each cluster in the period 1984 to 2013. For the observation period 2004 to 2013 minimum, maximum, median and quartiles of P30 numbers were calculated for each station and year. The results were plotted as box plots stratified for the geographic clusters. For the same time span, temperature data were used to determine the period when infection of the vector and transmission to the host is theoretically most likely. The prepatency period of 34 weeks (Webber and Hawking, 1955; Anderson, 2000) was considered in this estimation. Modified stacked bar-horizontal plot was used to assess the first and last day suitable for transmission per year. The descriptive statistical analysis was performed using Microsoft Excel® for Windows (Microsoft Corp., Redmont, USA).

3. Results

Fig. 1. Map of Germany showing the geographic origin of the utilized weather stations. The background of the map demonstrates the mean daily temperature of each July in the time frame 1961–1990, generated by the DWD.

ters (Fig. 1): North (N), Northeast (NE), East (E), Southeast (SE), Southwest (SW) and West (W). In accordance with the heartworm development unit (HDU) introduced for D. immitis by Fortin and Slocombe (1981), DDU (Dirofilaria development units) were calculated because both D. immitis and D. repens were found to have a similar climate-dependent development and transmission pattern (Genchi et al., 2011a,b). The DDU are calculated as the daily sum of degrees centigrade above a 14 ◦ C threshold (for Tmean ≥ 15, DDU = Tmean − 14). At least 130 DDU are necessary for extrinsic development of one generation of microfilariae (L1) to infective larvae (L3) (Fortin and Slocombe, 1981; Genchi et al., 2009, 2011a,b). Maximum life expectancy of vector mosquitoes is 30 days and no extrinsic development of larvae will occur at a temperature of 14 ◦ C or lower (Slocombe et al., 1989), although development will be completed even when temperature fluctuations below the 14 ◦ C threshold occur providing, however, 130 DDU accumulation within 30 subsequent

The comparison of the number of P30 between regional clusters as well as within clusters showed local differences within the same period (Fig. 2). An oscillating pattern during the observation period was obvious for the single weather stations, however, over the years all clusters displayed a general trend towards increasing number of P30 and this was substantiated by linear regression for two stations per cluster representing those with either the minimum or maximum trends. Except for cluster N all clusters presented more than 30 P30 in most years of the observation period [86%] (Fig. 2). Notably even the site with the lowest initial value (mostly cluster E and SE) increased above a number of 30 P30 by the end of the observation period in these clusters (Fig. 2) but not in cluster N, where only 30% of years were in the range of at least 30 P30 and the lowest linear trend line did not reach the level of 30 P30 (Fig. 2). 3.1. Observations in the decade 2004–2013 In clusters NE, E, SE, SW and W the extrinsic development was possible in each year of the observation period in all areas where weather data were recorded (Fig. 3). Median values over the observation period above 30 P30 were evident in 89% of the areas in these clusters. In the cluster SW the median was in fact greater than 60 P30 at three out of five locations. At two sites maximum values exceeded 90 P30 , and even the minimum values were higher than 60 P30 at these two weather stations. In contrast, in the cluster N the median was below 30 P30 at each of six locations. Climatic conditions were generally not suited here for extrinsic development to the L3 stage in 23% of the locations where less than 1 P30 were recorded (Fig. 3). The seasonal pattern of periods theoretically allowing extrinsic development and thus transmission to the host were similar in clusters NE, E, SE, SW and W and data for SW are plotted in Fig. 4a as a representative example.

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Cluster N

Cluster NE

90 number of P30

60

30

60

30

0

Bremen Emden Hamburg Hannover - linear regression

12

19 84 19 86 19 88 19 90 19 92 19 94 19 96 19 98 20 00 20 02 20 04 20 06 20 08 20 10 20 12

20

08

10 20

20

06

04 20

Hannover

20

00

02 20

20

96

94

98 19

19

19

90

92 19

19

86

88 19

19

19

84

0

Berlin Angermuende Berlin - linear regression

Schleswig Schwerin Schleswig - linear regression

Cluster W

Leipzig

12

10

20

20

06

08 20

04

20

20

02

00

Cottbus Dresden Goerlitz Cottbus - linear regression

Frankfurt/Main Muenster Kassel - linear regression

20

98 19

20

96

94 19

19

90

92

19

19

86

88

19

19

19

number of P30

84

12 20

10

08 20

20

06

04

Cologne

20

20

02

00 20

20

98 19

94

96 19

19

92 19

19

19

19

19

90

0 88

0 86

30

84

Erfurt Magdeburg Erfurt - linear regression

Cluster SE

Cluster SW 90

Mannheim

Saarbruecken Trier Saarbruecken - linear regression

Nuernberg

Munich

Weiden

Wuerzburg

0

2 20 1

20 1

8 20 0

6

4 20 0

20 0

2 20 0

0

8 19 9

Regensburg

Wuerzburg - linear regression

20 0

4

6 19 9

19 9

19 8

12 20

08

10 20

20

06

04 20

20

02

00

20

20

98 19

94

96 19

19

90

92 19

19

86

88 19

19

84

Karlsruhe Konstanz Karlsruhe - linear regression

2

0 19 9

0

19 9

30

4

30

0

60

8

60

6

number of P30

90

19 8

number of P30

60

30

Duesseldorf Gießen Kassel Frankfurt/Main - linear regression

number of P30

Neuruppin Berge Angermuende - linear regression

90

60

19

Potsdam

Cluster E

90

19 8

number of P30

90

Fuerstenzell

Weiden - linear regression

Fig. 2. Number periods per year with at least 130 P30 . Local distribution in the considered clusters from 1984 to 2013. Linear regression was calculated for two stations per cluster representing the curves of the minimum and maximum.

Altogether, the key days (first/last possible day of infection of the vector/host) were similar in these clusters. Time slots theoretically suitable for transmission were particularly short in cluster N (Fig. 4b). In contrast to the clusters NE, E, SE, SW and W the seasonal climatic pattern did not allow larval development in the vector in cluster N in 2012. From our data it appeared that in case of an assumed autochthonous infection microfilaraemia and availability of the next generation of mosquitoes do not overlap in most regions. The range of periods between onset of prepatency and the first day of patency that may allow successful infection of mosquitoes is related to the mean temperatures of two successive years. In five cases (year/station) allocated to clusters NE, E, SE, and SW the theoretical period of prepatency and of temperature conditions allowing transmission of microfilaria was overlapping. In general it appears that autochthonous infection of dogs with Dirofilaria spp. is theoretically possible from the beginning of June to October (Fig. 5). Climate conditions appear periodically suitable for microfilarial

transmission to the vector and subsequent development of L3 in mosquitoes from the beginning of May to early September in many but not all regions in Germany. 4. Discussion Climate-based forecast models employing the concept of growing degree day have been developed for different vectorborne diseases of parasitological importance (Malone, 2005). For Dirofilaria infections, climate-based models that determine the effect of temperature on the extrinsic incubation of larval stages in mosquitoes are based on the study of Fortin and Slocombe (1981), which demonstrated that at 30 ◦ C, development of D. immitis microfilariae to infective L3 larvae was completed in 8–9 days in Aedes vexans, Ae.triseriatus, and Anopheles quadrimaculatus. This increased to 10–14 days at 26 ◦ C, 17 days at 22 ◦ C, and 29 days at 18 ◦ C. For D. repens, the development times of microfilariae at the different temperatures are quite similar: 8–13 days at 28–30 ◦ C, 10–11 days at 26 ◦ C,

Please cite this article in press as: Sassnau, R., et al., Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany. Vet. Parasitol. (2014), http://dx.doi.org/10.1016/j.vetpar.2014.06.034

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Cluster E

Cluster NE

Cluster SE

5

Cluster SW

Cluster W

mumber of P30

90

60

30

2. quartil

Muenster

Frankfurt/Main

Kassel

Cologne

Gießen

Trier

Duesseldorf

Saarbruecken

Konstanz

Mannheim

Karlsruhe

Fuerstenzell

Weiden

Wuerzburg

Munich

Regensburg

Nuernberg

Erfurt

Magdeburg

Leipzig

Goerlitz

Dresden

Berge

Cottbus

Potsdam

Neuruppin

Berlin

Angermuende

Schwerin

Schleswig

Hamburg

Hannover

Emden

Bremen

0

3. quartil

Fig. 3. Box plot showing the periods of at least 130 P30 for all used weather stations in the years 2004–2013 (minimum, maximum, median and quartiles).

Fig. 4. Summary of the time frames of suitable conditions for the extrinsic and intrinsic development of D. immitis/D. repens in the years 2004–2013 in the considered clusters. In the display the period of prepatency is launched at the last day where infections were possible.

Oct. 01

Sept. 15

Oct. 04

Sept. 04 Sept. 01

Aug. 15

Aug. 01

July 15

July 01

June 15

May 03

June 02 June 01

Time frame where infections of mosquitoes were possible Time frame where infections of dogs were possible Time period of prepatency Period between the last day of prepatency and the first day where infections of mosquitoes were possible First / last day of possible infection of the vector First / last day of possible infection of the host

Cluster N NE E SE SW W

May 15

Legend:

recently, Kuzmin et al. (2005) found infective larvae of D. repens in salivary glands and proboscis of experimental infected mosquitoes (An. maculipennis, Cx. pipiens and Ae. aegypti) after 14–16 days at 18–29 ◦ C. Furthermore, there is a general and reasonable assumption in models developed from these observations that infected mosquitoes in the wild are unlikely to survive for more than 30 days (Knight and Lok, 1995). Based on these data, climate-based models have been used in order to predict the occurrence and seasonality of D. repens and D. immitis in Europe (Genchi et al., 2011a). While D. repens has a low pathogenic potential in dogs, D. immitis may cause severe and even lethal cardiovascular disease in dogs and cats. Both D. repens and D. immitis are zoonotic and able to trigger a variety of clinical syndromes in humans. Due to the lack of reliable diagnostic tools and a low awareness of zoonotic dirofilariosis, human infection is often not correctly diagnosed (Genchi et al., 2011b; Simón et al., 2012). While 116 cases of human

May 01

Oct. 04 Oct. 01

Sept. 07 Sept. 01

Sept. 15

Oct. 01

Sept. 15

Aug. 15

Aug. 01

Sept. 01

Aug. 15

Aug. 01 Aug. 08

July 15 July 15

July 04 July 01

June 15

May 15

May01

Year 2013 2011 2009 2007 2005

July 01

June 15

June 01

June 02

Cluster N

June 01

June 04

May 15

May 01

Year 2013 2011 2009 2007 2005

May 03

Cluster SW

Sept. 04

16–20 days at 22 ◦ C in Ae. aegypti, Ae. caspius, Ae. detritus, Ae. vexans, An. claviger, An. maculipennis, Culex pipiens (Webber and Hawking, 1955; Bain, 1978; Cancrini et al., 1988). In Ae. albopictus the development from microfilaria stage to infective larvae takes 14–18 days at 26 ◦ C for D. immitis and 16–18 days for D. repens (Cancrini et al., 1995). More

Legend:

Time frame where infections of mosquitoes were possible Time frame where infections of dogs were possible First / last day of possible infection of the vector First / last day of possible infection of the host Fig. 5. Maximal range of the time frames of suitable conditions for the extrinsic development of D. immitis/D. repens and the period of transmission of L3 in the years 2004–2013 of all clusters.

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infections with D. immitis were published up to 2012 in the USA (Simón et al., 2012) only three cases are recently reported from Europe and identified by molecular analysis (Avellis et al., 2011; Foissac et al., 2013; Pozgain et al., 2013). In contrast human infections with D. repens largely predominates in Europe (Genchi et al., 2011b; Simón et al., 2012; Salamatin et al., 2013; Ermakova et al., 2014). This study shows that the observed increase of the mean daily temperature in the past years would theoretically allow extrinsic incubation of D. immitis and D. repens in several but not all regions of Germany. Following the provisional data of the DWD related to climate change (DWD, 2013) the current trend allows the prediction that the risk of spread of dirofilarial worms will further increase in parts of Germany. Bearing in mind that both Dirofilaria species are zoonotic and there is an increasing concern about human infections (Genchi et al., 2011a; Cielecka et al., 2012; Simón et al., 2012), some consideration on prevention and control in dogs, that are the most important reservoir, is necessary (EASAC, 2010). Prevention in dogs to avoid spreading and endemisation of dirofilarioses is possible and safe treatment options are available (McCall et al., 2008; Traversa et al., 2013; Genchi et al., 2013). Preventative strategies for dogs under risk should consider three points: • Primary diagnostic screening. • Prevention of the infection of the vector. • Prevention of the infection in the vertebrate host. In the diagnostic screening for the presence of D. immitis in the dog an ELISA, based on the detection of soluble heartworm antigen, is suitable at the earliest five to six months post infection. In dogs with very low worm burdens antigen may never or only sporadically be detected (American Heartworm Society, 2014). All other diagnostic tools (microscopy for microfilaria and molecular tests) for D. immitis and D. repens are applicable in patency only. To note that the period between the last day of prepatency and the first day where infections of mosquitoes are possible can be short or overlap with the following transmission cycle (Fig. 4). In this case, diagnosis of dirofilariosis, acquired in the previous year, can deliver false negative results before the start of the period suitable for transmission from dogs to mosquitoes. The dog is the most important reservoir of both heartworm and subcutaneous (D. repens) infections. Both infections can be effectively prevented by treating dogs with macrocyclic lactone compounds (McCall (2005); McCall et al., 2008; Fok et al., 2010; Genchi et al., 2013). The prevention is based on the property of these compounds to kill the third and fourth larval stages of Dirofilaria worms. Thus, although the terms ‘prophylaxis’ or ‘prevention’ are currently used, the administration of these drugs actually interrupts the development of larvae transmitted by mosquitoes to the animal during the previous 30–60 days. All the available preventative drugs against Dirofilaria spp. have a wide range of efficacy and are well tolerated which allows them to be administered every 30 days throughout the period of increased risk. The first treatment should be

applied within a month after the beginning of exposure to transmission and the final dose within one month after the end of mosquito activity. Macrocyclic lactones have a retroactive or “reach-back” activity preventing patent infection and microfilaraemia when administered within the prepatent period, i.e. 3–4 months after transmission of L3 (McCall, 2005). Preventive treatment is currently not recommended to protect dogs from dirofilarial infection in Germany, however, from our data (Fig. 5) two treatments at an interval of 4 months (1st: late May/early June and 2nd: mid September/late October) would be suitable to protect dogs exposed to infection. Of course, dogs originating from risk areas or traveling dogs not subjected to adequate prevention should always be examined for dirofilarial infection and in case treated to avoid disease and import of the parasite. 5. Conclusion and clinical relevance The increasing number of reported autochthonous canine Dirofilaria infections, the finding of D. immitis and D. repens in mosquitoes, traveling and import of potentially infected dogs highlights the need to define a time frame suitable for prevention in dogs living at risk in Germany. The extrinsic development of dirofilarial larvae is dependent on the environmental temperature and it is fundamental to consider this for efficient prevention. Regional peculiarities and individual life style should also be regarded. The climatic conditions in Germany during the years 2004–2013 would have allowed transmission of Dirofilaria spp. from late April to mid-October. The increasing trend of average daily temperature as demonstrated for the observed period is related to a risk of emergence of parasites from warmer climates to areas that are non-endemic, so far. Thus, appropriate prevention may be of particular importance in the future. Conflict of interest statement No conflict of interest is declared. Acknowledgements The authors thank the German Weather Service (DWD), which provided us with the weather data. References American Heartworm Society, 2014. http://www.heartwormsociety. org/veterinary-resources/canine-guidelines.html (accessed June 16, 2014). Anderson, R.C., 2000. Nematode Parasites of Vertebrates. Their Development and Transmission, 2nd ed. CABI Publishing, Wallingford, Oxon. Avellis, F.O., Kramer, L.H., Mora, P., Bartolino, A., Benedetti, P., Rivasi, F., 2011. A case of human conjunctival dirofilariosis by Dirofilaria immitis in Italy. Vector Borne Zoonot. Dis. 11, 401–452. http:// dx.doi.org/10.1089/vbz.2010.007 Bain, O., 1978. Développement en Camargue de la filaire du chien, Dirofilaria repens Railliet et Henry, 1911, chez les Aedes halophile. Bull. Muséum National Hist. Naturelle 351, 19–27. Becker, N., Krüger, A., Kuhn, C., Plenge-Bönig, A., Thomas, S.M., SchmidtChanasit, J., Tannich, E., 2014. Mosquitoes as vectors for exotic pathogens in Germany. [Article in German] Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 57 (May (5)), 531–540. http://dx.doi.org/10.1007/s00103-013-1918-8

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Please cite this article in press as: Sassnau, R., et al., Climate suitability for the transmission of Dirofilaria immitis and D. repens in Germany. Vet. Parasitol. (2014), http://dx.doi.org/10.1016/j.vetpar.2014.06.034