Dirofilaria immitis and D. repens in Europe: a systematic literature review on vectors, host range, and the spatial distribution in the 20th and 21st century

Dirofilaria immitis and D. repens in Europe: a systematic literature review on vectors, host range, and the spatial distribution in the 20th and 21st century | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results Dirofilaria immitis and D. repens in Europe: a systematic literature review on vectors, host range, and the spatial distribution in the 20th and 21st century Carolin Hattendorf , View ORCID Profile Renke Lühken doi: https://doi.org/10.1101/2025.02.17.638693 Carolin Hattendorf 1 Bernhard Nocht Institute for Tropical Medicine , Hamburg, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site Renke Lühken 1 Bernhard Nocht Institute for Tropical Medicine , Hamburg, Germany Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Renke Lühken For correspondence: luehken{at}bnitm.de Abstract Full Text Info/History Metrics Data/Code Preview PDF Abstract Background Dirofilaria immitis and D. repens are mosquito-borne nematodes with dogs as primary hosts, but other mammalian species including humans can be also infected. In the last century, circulation of both pathogens was predominantly restricted to Southern Europe. However, different studies indicated a potential establishment in Central, Eastern and Western parts of Europe as an increasing threat to animal and human health. Methods We conducted a systematic literature review of publications reporting D. immitis and D. repens screening in mosquitoes and mammalian vertebrates in Europe. These data were used to analyse the range of vectors and hosts and for a comparison of the spatial distribution between the 20 th and 21 st century. Results Both nematodes appear to have a high overlap of Aedes , Anopheles and Culex vector species, which are abundant in Europe. Most D. immitis infections were reported in dogs, while D. repens predominated in humans. Dirofilaria immitis infections were detected in a wider range of wild and zoo animals. Compared to the last century, many more countries especially in Central Europe were affected by Dirofilaria spp. circulation, illustrating a significant spread over the last 20 years. Conclusion Our findings suggest that D. immitis and D. repens are a growing health concern for animals and humans in Europe. Continuous globalisation and climate warming will probably lead to a further spread and increased circulation in the future. All data are made available open access, which will enable further analysis in the future. Introduction Two Dirofilaria species are present in Europe: D. immitis and D. repens ( 1 ). Both circulate in an enzootic cycle between mosquitoes and domestic dogs, although other carnivores like Red Foxes and Grey Wolves can also be infected (e.g. ( 2 – 5 )). Mosquitoes are infected with microfilaria during blood-feeding on an infected host, which then develop to infective larvae in susceptible vectors ( 6 ). Dirofilaria can be transmitted to other mammals, such as humans and rodents, although these are generally ‘dead-end’ hosts ( 6 ), i.e. no development of microfilaria occurs. Dirofilaria immitis localise in the pulmonary arteries of dogs, where they sexually reproduce and release microfilariae into the bloodstream ( 1 , 7 ). Infections can lead to severe disease in dogs and cats with symptoms ranging from chronic cough to heart failure ( 8 , 9 ). In humans, D. immitis mostly forms pulmonary nodes, which are generally asymptomatic, but frequently mistaken with lung cancer in radiography ( 6 ). However, some humans develop severe symptoms including fever, chest pain, coughing, haemoptysis, wheezing arthralgia or malaise ( 10 ). Dirofilaria repens infections generally localises subcutaneously ( 1 , 6 ). Approximately 35 % of human D. repens infections occur in the ocular region, which can lead to impaired or a complete loss of vision ( 11 ). Around 10 % of affected patients suffer permanent complications like retinal detachment or glaucoma ( 12 ). Notably, there have been a few reported cases where viable D. repens microfilariae have been found in the blood stream of infected humans ( 13 – 17 ), but these seem to be rare exceptions. The majority of human Dirofilaria infections in Europe are caused by D. repens ( 18 ), while the majority of reported Dirofilaria cases in dogs are D. immitis ( 1 ). However, it has to be noted that D. immitis is easier to diagnose in dogs because it more often leads to severe symptoms in dogs and respective tests are available ( 19 ). First cases of human dirofilariosis presumably were diagnosed in 1566 in a Portuguese girl ( 20 ) and 1626 in an Italian dog ( 21 ) for D. repens and D. immitis , respectively. In the 20th century, autochthonous circulation of these parasites was predominantly reported from the Southern parts of Europe, but currently there are increasing reports of a spread towards Central, West and East Europe ( 22 ). Many previously Dirofilaria -free countries are now considered endemic ( 23 ). Climate warming is thought to be the main reason, allowing the successful development of the nematodes in the mosquito ( 24 – 26 ). Another important factor is the movement of dogs in Europe, which was made considerably easier with European regulations for traveling with pets ( 27 ). To gain a better picture of the vector range and spatial expansion of D. immitis and D. repens in Europe over the last two centuries, we conducted a systematic literature review of Dirofilaria data in mosquitoes and vertebrate hosts, including the collection of different metadata (e.g. sampling time and site). Methods All published articles matching the keyword ‘dirofilaria’ in any search field recorded in PubMed ( 28 ) were extracted on 24.01.2022. Papers were selected using the following inclusion criteria: 1) article language English or German, 2) a host was diagnosed with an acute infection of Dirofilaria spp., i.e. excluding studies only screening antibodies, and 3) the sampling was conducted in Europe. The following information was extracted from each publication: country, date of diagnosis/sampling, sampling location, host species, travel history, screening method, number of tested and number of positive specimens per Dirofilaria species. In addition, for mosquito studies the mosquito trap and pooling information (pool size, body part, etc.) were noted. If the date of diagnosis was not specified, the date of publication was used and if only a sampling period was given, the total number of cases was split evenly across the sampling years. The accuracy of the sampling locations was classified to decide which level of the Nomenclature of Territorial Units for Statistics (NUTS) classification of the European Union ( 29 ) was used for visualisation of parasite distribution in humans, dogs and other vertebrate hosts: ‘very high’ (coordinates or address, NUTS-3 level), ‘high’ (town or specific area, NUTS-2 level), ‘medium’ (hospital or greater area (e.g. county), NUTS-1 level), and ‘low’ (country, NUTS-0 level). For the spatial analysis of the Dirofilaria distribution, we only included reports with unremarkable travel history. However, many studies did not include any information on the travel history. Therefore, we also conducted the spatial visualisation with all unremarkable and unknown travel history for the supplement. Reports with a known travel history were excluded from analysis. Furthermore, we compiled visual summaries of country-specific Dirofilaria screening results from mosquitoes and less common vertebrate hosts, excluding humans and dogs. All computational analysis was performed in R (Version: 4.2.2) using the R-Studio IDE (Version:2022.12.0) ( 30 ). Additionally, functions from the following packages were used for data preparation, visualization and analysis: terra ( 31 ), tidyterra ( 32 ), geodata ( 33 ) readxl ( 34 ), ggpubr ( 35 ), plyr ( 36 ), dplyr ( 37 ), and ggplot2 ( 38 ). Results A total of 3,847 publications were extracted from PubMed. Of these, 473 (12.3 %) matched our inclusion criteria. We observed an increase in publications reporting Dirofilaria from the beginning of the 1990s and another increase in the mid-2000s ( Fig. 1 ). Download figure Open in new tab Fig. 1: Number of studies reporting Dirofilaria immitis and D. repens in Europe 38 publications (8.0 %) included screenings of mosquitoes for Dirofilaria with a total of 1,658,041 specimens tested over 62 mosquito taxa collected in 14 different European countries ( Fig. 2 ). Dirofilaria immitis was detected in 17 different mosquito taxa from 12 countries, most frequently in Culex pipiens s.l. (11 countries) and Aedes caspius (7 countries). Dirofilaria repens infections were reported for 31 different mosquito species from 13 countries with Aedes vexans (8 countries), Cx. pipiens s.l. (6 countries) and Anopheles maculipennis s.l. (6 countries) most frequently found positive. A total of 15 mosquito taxa were found positive for both Dirofilaria species. Dirofilaria immitis was exclusively detected in Ae. behningi , while D. repens was exclusively found in 16 different taxa of the Aedes , Anopheles , Culiseta and the Uranotaenia genus, e.g. Ae. cantans , An. claviger , Cs. annulata or Ur. unguiculata . Most studies on Dirofilaria prevalence in mosquitoes focused on Southern and Eastern Europe, but some studies also confirmed autochthonous circulation in Central Europe, e.g. Austria or Germany. Download figure Open in new tab Fig. 2: Dirofilaria immitis and D. repens reports in mosquitoes for different European countries 198 publications (41.9 % of included publications) reported dog infections with a total of 11,713 cases. Of these, 7,757 (66.2 %) were identified as D. immitis , 3,948 (33.7 %) as D. repens , and eight (0.1 %) were not further differentiated Dirofilaria species. In 199 publications (42.1 %), human Dirofilaria spp. infections were described, summing up to 2,555 reported human cases, of which the majority of 2,438 (95.4 %) was D. repens , followed by 95 (3.7 %) not further specified Dirofilaria spp. and 22 (0.9 %) D. immitis . Only 33 publications (7.0 %) reported Dirofilaria infections in cats (278 cases): 252 (90.1 %) D. immitis , 24 (8.6 %) D. repens and two (0.7 %) not further specified Dirofilaria species. In addition, 59 publications (12.5 %) described Dirofilaria infection in other mammals, the majority of which were caused by D. immitis ( Fig. 3 ). These studies predominantly focused on domestic cats (34 publications, 7.2 %) and Red Foxes (15 publications, 3.2 %). In addition, Dirofilaria were detected in a wide variety of wild carnivores (e.g. Golden Jackal, Grey Wolf or Eurasian Otter) and zoo animals (e.g. Lion or California Sea Lion). A wider variety of vertebrate hosts was studied in Slovakia, Serbia and Romania, while studies in other countries focused on few potentially infected species like Red Foxes or only reported single cases. Download figure Open in new tab Fig. 3: Dirofilaria immitis and D. repens reports in vertebrates except humans and dogs for different European countries Download figure Open in new tab Fig. 4: Dirofilaria immitis cases in humans, dogs and other mammals with unremarkable travel history in Europe until and since 2001 at different geographical levels Download figure Open in new tab Fig. 5: Dirofilaria repens cases in humans, dogs and other mammals with unremarkable travel history in Europe until and since 2001 at different geographical levels Only focusing on the studies with unremarkable travel history, the majority of the few D. immitis cases in dogs and other mammals until 2001 were recorded in Southern Europe, particularly in Spain, Italy and Portugal ( Fig. 2 ; see supplementary file 1 and supplementary file 2 for visualisation of all cases with unremarkable and unknown travel history). No human cases were reported before 2001. In the 21 st century, D. immitis infections were found in most countries of South and Central Europe and even in Central Europe, such as Poland and France. A wide distribution in particular was confirmed in dogs and other mammals for wide parts of Eastern Europe and Italy. Dirofilaria repens infections, especially looking into human cases, were reported much more widespread than D. immitis already during the 20 th century in particular for various regions in Italy and France, while dogs were only tested positive in Italy and Spain ( Fig. 3 ). We observed a strong increase of affected countries for both, humans and dogs, including countries in Eastern and Southern Europe (e.g. Ukraine, Slovakia, Greece), but also Central Europe including the Netherlands, Germany or Poland. The most Northern infection was reported in humans from Finland. Download figure Open in new tab Supplementary file 1: Dirofilaria immitis cases in humans, dogs and other mammals with unremarkable and unknown travel history in Europe until and since 2001 at different geographical levels Download figure Open in new tab Supplementary file 2: Dirofilaria repens cases in humans, dogs and other mammals with with unremarkable and unknown travel history in Europe until and since 2001 at different geographical levels Discussion The number of publications reporting Dirofilaria spp. infections have increased in the last two decades compared to the previous century ( 18 , 22 ). This is most likely driven by both, increased research and awareness, but also the spread of the parasites ( 25 , 39 ). Dirofilaria immitis and D. repens have to be considered endemic in countries that were considered to be Dirofilaria -free in the 20 th century, e.g. Czech Republic ( 40 , 41 ). The spread of competent vector species probably does not play a major role here. There is a huge overlap between the vector species for D. immitis and D. repens , which are widespread in Europe and show host-feeding patterns with a substantial proportion of mammals, e.g. Cx. pipiens s.l. or An. maculipennis s.l. ( 42 – 44 ). Interestingly, the exotic Ae. albopictus was much more often reported to be infected with D. immitis than D. repens . This mosquito species has been implicated as an important driver of the spread of Dirofilaria ( 22 , 26 , 45 ). Most infections were reported from dogs as the primary host of Dirofilaria ( 1 ). The majority of these cases were caused by D. immitis , which is well known to cause a more severe disease in dogs compared to D. repens , leading to a higher probability of diagnosis ( 7 ). Additionally, rapid tests are only available for D. immitis and not D. repens. Therefore, D. repens might be underreported and its actual prevalence among dogs is probably higher ( 11 ). In contrast, the overwhelming majority of cases in humans were caused by D. repens , confirming previous observations that most human Dirofilaria infections in Europe are caused by this species ( 46 , 47 ). The reason for this remains unclear, given that human infections with D. immitis are regularly reported, particularly in North America ( 48 ). One hypothesis suggested that European D. immitis might be genetically distinct from D. immitis found in other regions, making it less capable of surviving within humans ( 11 ). However, this hypothesis has later been disproven ( 49 , 50 ). Another explanation could be that D. repens influences the circulation of D. immitis , e.g. it has been shown for Southern Italy that D. repens impedes the spread of D. immitis in dogs ( 51 ). If this plays a general epidemiological role and if this is also true for humans requires further research. Furthermore, it has been proposed that D. repens is more difficult to control, because, as mentioned above, rapid tests are only available for D. immitis and current preventative and curative treatments are designed for D. immitis and are not as effective against D. repens ( 18 ). Additionally, D. repens infections are often asymptomatic in dogs which might lead to a longer time period where a dog is infective, and a mosquito can ingest and transmit the parasite to further hosts ( 6 , 52 ). Besides dogs and humans, there were also several reports of infections in cats, although it is assumed that cats do not play an important role for Dirofilaria transmission ( 53 ). Similarly, several other mammalian species diagnosed with an infection were held in zoos or as pets, allowing diagnosis ( 54 – 57 ). Furthermore, there are some wild animals in which Dirofilaria infections were identified, predominantly in canids like Red Foxes ( 4 , 5 , 58 – 69 ), Golden Jackals ( 59 – 62 , 70 , 71 ), and Grey Wolves ( 2 , 3 , 58 , 59 , 62 , 72 , 73 ). Zoo and wild animals were almost always infected by D. immitis , which again might be because D. immitis in comparison to D. repen s infections more often leads to severe symptoms, corresponding test kits are available or because D. immitis has a broader host range. It is undeniable that both, D. immitis and D. repens , are spreading in Europe and more humans and animals are at risk of infection. In part this might be also a diagnostic artefact, i.e. imported and travelling dogs are more routinely tested, which leads to more detection ( 39 ). Transport of pets has significantly increased during the 21 st century as a consequence of the Pet Travel Scheme, which was introduced by the EU in 2000 and made travel of companion animals significantly easier and led to an increase in imported cases ( 27 ). Another reason is the continuously high number of stray dogs in some countries, which are not subject to regular treatment and act as reservoirs for the parasites, e.g. countries with many stray dogs, such as Romania or Bulgaria continue to regularly report Dirofilaria spp. cases ( 74 – 76 ). However, probably one of the most important factors for the spread of Dirofilaria is climate warming. Higher temperatures lead to faster development of Dirofilaria larvae inside the mosquito vector ( 77 , 78 ). Prolonged warm periods extend the transmission season ( 26 ). There is a significant increase in areas at risk, especially in more Northern countries. This spread has been predicted since the early 2000s ( 25 , 52 ) and with continuous climate warming will further increase in the future. Finally, increasing temperatures in Europe also allowed the widespread establishment of exotic mosquito species such as Ae. albopictus ( 79 – 81 ), which is an important vector for D. immitis and D. repens and the establishment of the vector species in numerous European regions has been linked to increased Dirofilaria circulation ( 22 ). Conclusion Dirofilaria immitis and D. repens are an increasing threat to veterinary and public health in Europe. Both parasites have dramatically expanded their circulation area and are now endemic in areas that were considered Dirofilaria- free only one or two decades ago ( 23 ). The warming climate and the abundant presence of competent vectors allows the establishment of the parasites in Central Europe, e.g. Germany and Poland. Due to their rising relevance in animal and human health, a Europe-wide unified surveillance system similar to the system in the United States ( 82 ) should be implemented in order to better understand the change of circulation patterns and to plan and execute preventative strategies, e.g. dog treatment. All data and code are provided as open access, allowing for future analyses. Ethics approval and consent to participate Not applicable. Consent for publication Not applicable. Availability of data and materials The datasets supporting the conclusions of this article and all codes used for data analysis are available at https://github.com/luehkenecology/dirofilaria_review_europe Competing interests The authors declare that they have no competing interests. Funding This project is funded through the Federal Ministry of Education and Research of Germany, with the grant number 01Kl2022. Author contributions Conceptualization: RL; data collection: CH; data analysis: CH, RL; writing: CH, RL; all authors read and approved the final manuscript. Acknowledgements Not applicable. Footnotes https://github.com/luehkenecology/dirofilaria_review_europe References 1. ↵ McCall JW , Genchi C , Kramer LH , Guerrero J , Venco L . Heartworm disease in animals and humans . Adv Parasitol . 2008 ; 66 : 193 – 285 . OpenUrl CrossRef PubMed Web of Science 2. ↵ Moroni B , Rossi L , Meneguz PG , Orusa R , Zoppi S , Robetto S , et al. Dirofilaria immitis in wolves recolonizing northern Italy: are wolves competent hosts? Parasit Vectors . 2020 Sep 22 ; 13 ( 1 ). 3. ↵ Segovia JM , Torres J , Miquel J , Llaneza L , Feliu C . Helminths in the wolf, Canis lupus, from north-western Spain . J Helminthol . 2001 Jun ; 75 ( 2 ): 183 – 92 . OpenUrl CrossRef PubMed Web of Science 4. ↵ Medkour H , Laidoudi Y , Marié J Lou , Fenollar F , Davoust B , Mediannikov O . 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