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Microorganisms associated with hedgehog arthropods

Parasites & Vectors volume 16, Article number: 211 (2023) Cite this article

Abstract

Hedgehogs are small synanthropic mammals that live in rural areas as well as in urban and suburban areas. They can be reservoirs of several microorganisms, including certain pathogenic agents that cause human and animal public health issues. Hedgehogs are often parasitized by blood-sucking arthropods, mainly hard ticks and fleas, which in turn can also carry various vector-born microorganisms of zoonotic importance. Many biotic factors, such as urbanization and agricultural mechanization, have resulted in the destruction of the hedgehog’s natural habitats, leading these animals to take refuge near human dwellings, seeking food and shelter in parks and gardens and exposing humans to zoonotic agents that can be transmitted either directly by them or indirectly by their ectoparasites. In this review, we focus on the microorganisms detected in arthropods sampled from hedgehogs worldwide. Several microorganisms have been reported in ticks collected from these animals, including various Borrelia spp., Anaplasma spp., Ehrlichia spp., and Rickettsia spp. species as well as Coxiella burnetii and Leptospira spp. As for fleas, C. burnetii, Rickettsia spp., Wolbachia spp., Mycobacterium spp. and various Bartonella species have been reported. The detection of these microorganisms in arthropods does not necessarily mean that they can be transmitted to humans and animals. While the vector capacity and competence of fleas and ticks for some of these microorganisms has been proven, in other cases the microorganisms may have simply been ingested with blood taken from an infected host. Further investigations are needed to clarify this issue. As hedgehogs are protected animals, handling them is highly regulated, making it difficult to conduct epidemiological studies on them. Their ectoparasites represent a very interesting source of information on microorganisms circulating in populations of these animals, especially vector-born ones.

Graphical abstract

Background

Hedgehogs are small synanthropic nocturnal omnivorous mammals whose dorsal part of the skin is wholly covered with spines [1, 2]. They are hibernating animals, dig their own burrows, and live in rural areas as well as in urban and suburban areas [1]. Hedgehogs belong to the Erinaceidae family, and include up to 17 known species divided into five genera (Erinaceus, Atelerix, Hemiechinus, Paraechinus and Mesechinus) distributed worldwide [3, 4]. Hedgehogs are found in Europe, Africa and Asia and were introduced by importation into New Zealand and the Americas [1, 4, 5]. Hedgehog populations have been continuously decreasing, leading the authorities of several countries to provide protection by classifying them in their lists of species threatened with extinction. It is therefore prohibited to kill them or to retain them in captivity [3].

Interest in these animals has increased over the years. The first studies, dating from the late nineteenth century, were mainly focused on the histology, physiology and anatomy of hedgehogs [6]. Researchers have been very interested in their hibernation process, mainly in the physiological changes allowing them to go from an homeothermic animal status to a poikilothermic animal status and vice versa [7].

In the 1940s, laboratory-reared populations of Erinaceus europaeus hedgehogs were established as a means to meet research needs [8]. However, it was only in the 1950s that researchers began to show greater interest in their role as reservoirs for pathogens involved in human and animal public health issues and possibly responsible for zoonoses [5, 9, 10]. Laboratory-reared hedgehog specimens were used in experimental models which aimed to determine their sensitivity to different microorganisms, including Borrelia strains (B. duttoni, B. crocidurae, B. hispanica and B. persica) [9]. The experimental infection of a hedgehog by Trypanosoma gambiense showed that this parasite caused a chronic infection in the animal leading to its death [11]. Different microorganisms have already been reported in hedgehogs, including bacteria (Yersinia pseudotuberculosis, Coxiella burnetii, Mycobacterium spp., Corynebacterium spp., methicillin-resistant Staphylococcus aureus, Salmonella spp., Leptospira spp., Chlamydia psittaci and Streptococcus spp.), protozoa (Cryptosporidium spp., Toxoplasma gondii), fungus (Candida albicans, Microsporum spp., Trichophyton erinacei) and viruses (Coronaviruses, Herpesvirus, rabies virus, Paramyxovirus) [2, 3]. Similarly, several vector-borne microorganisms have also been detected, including Tick-borne encephalitis virus (TBEV), Crimean-Congo hemorrhagic fever orthonairovirus (CCHFV), Severe Fever with Thrombocytopenia Syndrome Virus (SFTSV), Bhanja bandavirus, Yersinia pestis, Rickettsia spp., Bartonella spp., Babesia spp., Candidatus Neoehrlichia mikurensis and Leishmania spp. [2, 3, 12,13,14,15]. In addition, several studies have reported hedgehog infection by Borrelia burgdorferi sensu stricto (B. burgdorferi s.s.), the agent of Lyme disease [3, 16], and Anaplasma phagocytophilum, the agent of granulocytic anaplasmosis [3, 12].

Hedgehogs are often parasitized by mites and blood-sucking arthropods (Fig. 1), mainly hard ticks and fleas (Fig. 2) [12, 13]. Ixodes hexagonus and Ixodes ricinus are the most frequently collected ticks from hedgehogs [3, 13, 17, 18], but other tick species have also been reported, including Rhipicephalus sanguineus sensu lato (Rh. sanguineus s.l.) (Fig. 2), Rhipicephalus (Boophilus) annulatus, Rhipicephalus camicasi, Haemaphysalis erinacei (Fig. 2), Haemaphysalis flava, Haemaphysalis longicornis, Haemaphysalis colesbergensis, Haemaphysalis norvali, Amblyomma marmoreum, Dermacentor nuttalli, Hyalomma aegyptium, Hyalomma excavatum, Hyalomma asiaticum, Hyalomma dromedarii, Hyalomma schulzei, Ixodes acuminatus, Rhipicentor nuttalli and the soft tick Ornithodoros [4, 13, 16,17,18,19,20,21,22,23,24,25,26,27,28,29,30]. All developmental stages (larva, nymph and male/female adults) have been found feeding on these animals [27, 31]. Moreover, one study has shown that odors related to animal health status seems to have an impact on the tick infestation rate [4]. The most common species of flea collected from hedgehogs is Archaeopsylla erinacei (Fig. 2) [4, 16, 18, 21, 32]. Other flea species have also been reported (Leptopsylla segnis, Ctenocephalides canis and Ctencephalides felis) [17, 18, 33, 34].

Fig. 1
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Hedgehogs parasitized by ticks

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Fig. 2
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Photographs of arthropods sampled from Atelerix algirus hedgehogs taken with a Zeiss Axio Zoom V16 stereomicroscope (Carl Zeiss Meditec France S.A.S., Marly le Roi, France) and a VHX-7000 digital microscope (Keyence Corp., Osaka, Japan). a–c Haemaphysalis erinacei capitulum, dorsal and ventral views, d, e Rhipicephalus sanguineus sensu lato male dorsal and ventral views, f, g Rhipicephalus sanguineus sensu lato female dorsal and ventral views, h, i Archaeopsylla erinacei female flea

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Fleas and ticks are also known to be vectors of different pathogens, thereby presenting a risk to human and animal health, causing such diseases as bartonellosis, flea-borne spotted fever rickettsiosis, plague, murine typhus for fleas and borreliosis, anaplasmosis, tick-borne spotted fever rickettsiosis, ehrlichiosis and several arboviruses for ticks [13, 16, 21, 35, 36]. Some of these flea and tick species have a weak host specificity and can bite different hosts, including wild, domestic and peri-domestic animals as well as humans; as such, they can thus participate in the exchange of microorganisms between their different hosts. [16, 18, 27, 37]. In addition, some tick species feed on a different host at each developmental stage and can thus actively participate in the spread of pathogens that could be responsible for zoonoses [38].

Many biotic factors, such as urbanization, land consolidation and large-scale mechanized agriculture, have resulted in the destruction of the hedgehog’s natural habitats, leading them to take refuge near human dwellings where they seek food and shelters in gardens and parks [2, 3]. In some countries and populations, hedgehogs can be used in traditional medicine and also eaten [3, 4]. In addition, the European hedgehog E. europaeus and the African pygmy hedgehog Atelerix albiventris are frequently taken as pets and are often transported with their parasites and pathogens from one region to another, exposing humans to several zoonotic agents, including those carried by their ectoparasites [2, 13, 18].

Two interesting reviews on hedgehog zoonoses have been published. However, the authors of these reviews mainly focused on the microorganisms detected in the hedgehogs themselves, and only partially addressed those detected in the ectoparasites collected from them by mentioning some of the pathogens associated with ticks but not those associated with fleas [2, 3].

The aim of the present review is to collate and list the information available in the literature on the microorganisms depicting a zoonotic threat that have been detected in arthropods sampled from different hedgehog species worldwide. We do not detail here the microorganisms detected in the hedgehogs themselves because this topic has been adequately covered in the two previous reviews [2, 3].

Microorganisms detected in ticks collected from hedgehogs

Coxiella burnetii

Coxiella burnetii is a Gram-negative obligate, intracellular bacterium [39] that is the causative agent of Q fever [20, 39]. This bacterium is widely distributed in the environment and affects different domestic and wild animal species as well as humans and arthropods [20, 27, 39], but livestock are considered to be the principal reservoir for this zoonotic disease [3, 20]. This bacterium can be transmitted to humans and animals through direct contact with infected animals or indirectly via aerosols, infected urine, feces, birth products, milk and other dairy products [3, 20, 28].

Coxiella burnetii has been reported in over 40 tick species collected from several animals, including hedgehogs [27]. It has been detected in Hyalomma excavatum collected from Hemiechinus auritus (the long-eared hedgehog) in Egypt (Alexandria) [28], in 3.2% (4/125) of Ha. flava ticks collected from Erinaceus amurensis (the Amur hedgehogs) captured in forests near the cesspools in Xianning City, Hubei Province, in Central China [20] and in Ha. erinacei sampled from Atelerix algirus (North African hedgehog) collected dead in Bouira Province of northern Algeria [21]. Previous studies reported C. burnetii in hedgehog tissues, suggesting that these animals as well as their associated ectoparasites could be considered as reservoir hosts for this pathogen [3, 20, 21]. Ticks have been suspected of playing a role in the epidemiology and transmission of C. burnetii. However, to our knowledge, only one experimental study has demonstrated the vectorial capacity of Hyalomma aegyptium ticks for C. burnetii [27, 40]. Moreover, ticks have been shown to transmit C. burnetii horizontally through their saliva and feces and also vertically through transstadial and transovarial routes [27].

Borrelia spp.

Borrelia burgdorferi sensu lato (B. burgdorferi s.l.) is a spirochete bacteria and the causative agent of Lyme borreliosis, the most common vector-borne disease in Europe and USA, infecting various vertebrate reservoir hosts [3, 41,42,43]. Ticks, mainly the endophilic I. hexagonus and those of the exophilic I. ricinus complex, are the recognized vectors, and transmission occurs during blood meals through their infected saliva [18, 41,42,43,44]. Humans are considered as dead-end hosts and do not play a role in the epidemiology of B. burgdorferi s.l. [43]. The B. burgdorferi s.l. group contains three Candidatus genospecies and at least 20 validated species, including B. burgdorferi s.s., B. afzelii, B. garinii, B. bavariensis and B. spielmanii [41, 42, 45].

Preliminary results of a study conducted by Skuballa et al. showed that an I. hexagonus nymph and an I. ricinus female tick sampled from European hedgehogs from Karlsruhe (Germany) were infected with B. afzelii and B. spielmanii [41]. Another study conducted in Germany on I. hexagonus ticks collected from hedgehogs showed that two specimens were infected with B. afzelii, one was infected with B. spielmanii and one was co-infected with B. garinii and B. afzelii [42]. Furthermore, the DNA of B. miyamotoi, the spirochete bacterium belonging to the relapsing fever group, causing human non-specific febrile illness, and B. bavariensis, have been detected in both I. hexagonus and I. ricinus collected from hedgehogs [3]. These Borrelia species, which are either confirmed or suspected pathogens for humans, have also been previously detected in hedgehog tissue, suggesting that they may be reservoir hosts. However, further investigation is needed in order to determine the precise role that hedgehogs play in the epidemiology of these bacteria [3, 18, 41].

Anaplasma phagocytophilum

Anaplasma phagocytophilum is an obligate intracellular Gram-negative bacterium [31, 46]. It is an emerging tick-born zoonotic pathogen responsible for granulocytic anaplasmosis, an acute febrile disease of public health importance that affects humans, domestic and wild animals distributed worldwide [3, 12, 46]. Ixodes ticks, mainly I. ricinus in Europe, I. scapularis and I. pacificus in the Americas and I. persulcatus in Asia, have been reported to be the main vectors of A. phagocytophilum, and wild rodents are considered as natural reservoir hosts. Infection of humans is accidental, and humans are considered to be dead-end hosts [3, 12, 31, 46].

Anaplasma phagocytophilum was detected in 15/38 (39.47%) engorged I. hexagonus female ticks collected from 7/14 (50%) E. europaeus hedgehogs from Germany [12], in 74/277 (27%) I. hexagonus and 6/25 (24%) I. ricinus ticks sampled from hedgehogs captured alive in the Netherlands, in 413/563 (73.36%) I. ricinus and 90/338 (26.63%) I. hexagonus sampled from a captive hedgehog population in Baden-Württemberg (Germany) [31] and in the same two tick species from hedgehogs in a study conducted in Belgium [3]. In addition, 4/13 (30.8%) pools of Dermacentor nuttalli ticks collected from hedgehogs in Hebei Province (China) were positive for A. phagocytophilum. Dermacentor ticks are unusual hosts, and their vectorial capacity should therefore be investigated [46].

Hedgehogs are often parasitized by ticks and thus can be involved in the circulation of this bacterium [3]. Indeed, A. phagocytophilum has also been detected in E. europaeus and Erinaceus roumanicus hedgehog blood and tissue [3, 12, 31]. The sequences obtained by Skuballa et al. from hedgehog tissue were almost identical to those they obtained from the ticks collected from the hedgehogs in a study they conducted in Germany, indicating that transmission can probably occur from one of these hosts to the other [12]. Only some of the different A. phagocytophilum strains have been confirmed to be human pathogens, and the reservoirs of the pathogenic strains involved in human disease remain unknown [12, 46]. Sequencing has revealed that the most frequent variant (variant ‘A’) found in the study conducted by Silaghi et al. [31] was similar to that reported previously in human, canine and equine granulocytic anaplasmosis [31]. The role of the strains found in hedgehogs and their ticks in terms of public health issues remains unclear, but the findings provided by Silaghi et al. [31] suggest they may have some involvement. Further studies are necessary to clarify this.

Anaplasma marginale

Anaplasma marginale is a tick-borne pathogen causing a hemolytic disease that can sometimes be severe [26]. About 20 tick species have been reported as potential vectors in which the bacteria multiply in the midgut and salivary glands. Nevertheless, Dermacentor spp., Rhipicephalus annulatus and Rhipicephalus bursa are considered to be the main vectors [26, 47]. Transmission can occur between some tick species through the transovarian, transstadial and intra-stadial routes, and it has been previously proven that transmission to another host is possible [26].

Using PCR and sequencing, A. marginale has been detected in three Rhipicephalus turanicus tick pools and in the blood of 2/53 (3.8%) live long-eared hedgehogs (H. auritus) from which the ticks were sampled. These hedgehogs were captured in urban and suburban areas around Zabol in south-eastern Iran [26]. In addition, 40 I. hexagonus sampled from E. europaeus hedgehogs in the Netherlands tested positive for this bacterium [26]. The infection in hedgehogs seems to be subject to cyclical variations, raising questions as to whether the infection is persistent, making this animal a suitable reservoir, or whether it is rapidly eliminated by the immune system [26]. Further investigations are needed to clarify the involvement of hedgehogs in the epidemiological cycle of this bacterium.

Anaplasma bovis

Anaplasma bovis is an Anaplasmataceae agent of bovine anaplasmosis, a tick-borne infectious disease, which parasitizes monocytes and macrophages. It causes animal body weight loss, abortions and decreased milk production, and frequently leads to death of the infected animal [48, 49]. Anaplasma bovis has been detected in 4% (5/125) of Ha. flava ticks sampled from E. amurensis hedgehogs captured in forests near the cesspools in Xianning City, Hubei Province, in central China [20].

Ehrlichia spp.

The DNA of two potential new uncultivated Ehrlichia species has been reported in ticks collected from hedgehogs. The first was phylogenetically close to Ehrlichia ewingii and was detected in 9.6%, (12/125) of Ha. flava ticks sampled from E. amurensis hedgehogs captured in forests near the cesspools in Xianning City, Hubei Province, in central China [20]. The second was detected in Rh. sanguineus s.l. and Ha. erinacei ticks sampled from A. algirus hedgehogs in Bouira Province in north-central Algeria [21]. Phylogenetic analysis revealed that the detected Ehrlichia spp. clustered together with another uncultured Ehrlichia in a clade separate from other known species [21]. These two Ehrlichia spp. have not been cultivated to allow formal description of the species. Their potential pathogenicity for animals and humans also remains unknown and requires investigation.

Rickettsia

Rickettsia are obligate intracellular bacteria causing emerging and re-emerging diseases worldwide [50]. The principal vectors are hematophagous arthropods, and they are mainly associated with ticks, fleas and lice [50].

Rickettsia massiliae

Several studies conducted in Algeria reported detecting R. massiliae in hedgehog ticks. Indeed, this bacterium has been detected in Rh. sanguineus s.l. ticks sampled from hedgehogs in Algiers [51], in north-east Algeria [4] and in 40/59 (67,80%) Rh. sanguineus s.l. ticks sampled from dead A. algirus hedgehogs in the Bouira province [21]. The DNA of R. massiliae has also been found in 22/212 (10.38%) Rh. sanguineus s.l. collected from five European hedgehogs (E. europaeus) captured in seven districts in the north and center of Portugal [13] and in 11/12 (91.7%) Rh. sanguineus s.l. ticks collected from a female E. europaeus hedgehog that was captured in the city center of Marseille, France [16]. Rhipicephalus sanguineus s.l. ticks represent the main vectors of R. massiliae, and this bacterium has been detected in their saliva [51]. Transovarial and transstadial transmission has also been reported among the tick population, suggesting that these ticks might be potentially reservoirs [16, 52]. Cases of human infection by R. massiliae have been reported in the literature [13].

Rickettsia conorii

Rickettsia conorii is the etiological agent of Mediterranean spotted fever (MSF) rickettsiosis, an endemic zoonosis in the Mediterranean basin transmitted mainly by the brown dog tick Rh. sanguineus s.l. [50]. Rickettsia conorii conorii strain Malish has been detected in a Rh. sanguineus s.l. specimen collected from a hedgehog in Algiers [51].

Other Rickettsia species

Other Rickettsia species, including R. japonica and R. raoultii, have been detected in 4/125 (3.2%) and 3/125 (2.4%) Ha. flava ticks, respectively, collected from E. amurensis hedgehogs captured in forests near the cesspools in Xianning City, Hubei Province in central China [20]. Rickettsia heilongjiangensis (R. heilongjiangensis XY-1) was reported for the first time in 79/110 (71.8%) Ha. flava ticks and in 7/45 (15.6%) E. amurensis hedgehogs from which the positive ticks were collected in Xuyi County, southeast China [25]. Rickettsia helvetica has been reported in I. hexagonus and I. ricinus ticks sampled from hedgehogs in Belgium [3, 13]. The agent of Siberian tick typhus, Rickettsia sibirica sibirica, has been detected in ticks from hedgehogs collected in a suburb of Beijing, China, and this bacterium has been also isolated from the same hedgehog which provided the positive tick sample [4].

In the same study conducted in Xuyi County, southeast China mentioned above, a potential new species, Candidatus Rickettsia xuyiensis XY-2 was detected in 8/110 (7,3%) Ha. flava ticks collected from E. amurensis hedgehogs [25]. The hedgehog from which the positive ticks were collected tested also positive [25].

A potential new uncultivated Rickettsia species of the spotted fever group has been reported in 11.25% of Rh. sanguineus s.l. and in 77% of Ha. erinacei ticks sampled from A. algirus and Paraechinus aethiopicus hedgehogs in north-east Algeria [4], and another potential new uncultivated Rickettsia species close to the previous one has been detected in two Ha. erinacei ticks collected from A. algirus hedgehogs in the Bouira province in Algeria [21].

Rickettsia species have already been detected in hedgehogs, which suggests that they are suitable reservoir hosts. However, their precise role in the epidemiological cycle of these rickettsial agents remain poorly known [4, 13].

Leptospira spp.

Leptospira spp. are obligate aerobe spirochete bacteria belonging to the Leptospiraceae family and are the agent of leptospirosis, a widespread zoonotic disease. Humans can become infected after direct contact with infected urine or indirectly through a contaminated environment [3, 53].

Leptospira spp. was detected in two Rh. sanguineus s.l. ticks collected from A. algirus hedgehogs for the first time in Algeria. However, sequencing did not allow the identification of the species [21].

Several studies have reported Leptospira species in hedgehog kidneys worldwide [3]. Leptospira interrogans and L. borgpetersenii have been reported in wild hedgehogs in France, L. interrogans has been reported in wild E. amurensis (Amur hedgehogs) from China and in A. algirus hedgehogs from the Bouira Province, Algeria [3, 21] and L. ballum has also been isolated from hedgehogs [3]. These animals are strongly suspected to play a role in the epidemiology of this zoonotic disease and its transmission to humans [3]. The involvement of ticks in the cycle should be further investigated to find out whether the specimens in the study by Aouadi et al. mentioned above were positive simply because they had ingested blood from an infected host or whether they have real vectorial capacity and competence for Leptospira species.

All of the microorganisms reported in the different tick species sampled from hedgehogs are summarized in Fig. 3 and in Table 1.

Fig. 3
figure 3

Microorganisms detected in different tick species sampled from hedgehogs worldwide

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Table 1 Summary table of microorganisms detected in ticks and fleas collected from different hedgehog species worldwide
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Microorganisms detected in fleas collected from hedgehogs

Rickettsia

Rickettsia felis

Rickettsia felis, the agent of flea-borne spotted fever rickettsiosis, is an emerging Gram-negative obligate intracellular bacterium reported worldwide which affects humans [54]. Although fleas, mainly cat fleas Ctenocephalides felis, are the recognized vectors, this bacterium has been also reported in other flea and arthropod species, such as booklice [36, 54, 55]. In addition, mosquitos have been reported to be a competent vector under experimental conditions [56] (Fig. 4)

Fig. 4
figure 4

Microorganisms detected in different flea species sampled from hedgehogs worldwide

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Rickettsia felis have been detected in A. erinacei fleas collected from different hedgehog species, including A. algirus hedgehogs in a western region of Algeria (the Oran district) and in a north-central region of Algeria (the Bouira province) [21, 57]; in 33.3% of the fleas sampled from E. europaeus hedgehogs from Spain [32]; and with a high infection rate (99.2% and 95.5%) in A. erinacei fleas collected, respectively, from E. europaeus hedgehogs captured in the city center of Marseille in France, and in A. algirus and P. aethiopicus hedgehogs in Algeria [4, 16]. Furthermore, R. felis has been detected in A. erinacei maura collected from E. europaeus in Mértola, a southern region of mainland Portugal [35] and in A. erinacei and C. felis fleas collected from A. algirus hedgehogs in Cheabat El Balout (Ouled Driss, Souk Ahras) in Algeria [17]. Rickettsia felis transovarial transmission has been reported in fleas, suggesting that they might be potentially reservoirs. Nevertheless, the role of hedgehogs in the epidemiological cycle remains unclear, and further investigations are necessary [57].

Rickettsia felis-like organisms

A very high infection rate of a R. felis-like organism has been detected in A. erinacei fleas collected from hedgehogs in Bavaria (Germany). The authors concluded that this may be a strain variant of R. felis as the sequences are closely related to it and it appears to be associated with hedgehogs and their fleas [58]. Moreover, Rickettsia asembonensis DNA was identified in 55/117 (47%) A. erinacei fleas sampled from European hedgehogs (E. europaeus) captured in seven districts of north and center Portugal [13]. Further investigations are needed to determine the involvement of hedgehogs and their fleas in the epidemiology and circulation of R. felis-like organisms. Although a R. felis-like organism has previously been reported in a human (blood sample from a Malaysian patient), the pathogenicity of these bacteria for humans and animals remains to be determined [13, 58].

Rickettsia typhi

Rickettsia typhi, the etiological agent of murine typhus, has been detected in one A. erinacei flea sampled from an E. europaeus hedgehog in Spain [32]. This bacterium is usually associated with rodents and Xenopsylla fleas, which are considered to be the main vectors [32]. Further investigations and experimental models should be performed to find out whether this flea species could be a suitable reservoir and vector for R. typhi.

Bartonella spp.

Bartonella are emerging Gram-negative fastidious oxidase-negative bacteria [59, 60]. Eleven species have been reported to be involved in various human diseases worldwide [59]. They are associated with different arthropod species, mainly fleas [35]. Transmission usually occurs through infected feces [60].

Bartonella henselae, the etiological agent of cat scratch disease in humans, has been detected in an A. erinacei flea collected on northern white-breasted hedgehogs (E. roumanicus) in Budapest, Hungary [61]. In addition, Bartonella elizabethae and Bartonella clarridgeiae have been detected in A. erinacei fleas collected from hedgehogs in Algeria (Ouled Ben Aouali and Tafraoui districts) [60]. A potential new uncultivated Bartonella spp. which is phylogenetically close to B. clarridgeiae has also been detected in the same flea species sampled from A. algirus hedgehogs in Algeria (Bouira province) [21].

Different Bartonella species have also been reported in hedgehogs. Atelerix algirus hedgehog spleens from Algeria have tested positive for B. elizabethae and B. tribocorum [59, 60]. Bartonella washoensis and B. melophagi have been reported in E. europaeus hedgehogs in urban and suburban areas of the Czech Republic [62]. Furthermore, several potential new Bartonella species have been reported, including clones which are phylogenetically close to B. taylorii, B. clarridgeiae, and B. rochalimae detected in the northern white-breasted hedgehog (E. roumanicus), the European hedgehog (E. europaeus), the southern white-breasted hedgehog (E. concolor) and the north African hedgehog (A. algirus) from different countries [21, 62,63,64,65]. The aforementioned studies highlight that Bartonella species have been reported in hedgehogs as well as in the fleas collected from them, suggesting that hedgehogs maybe potential reservoirs. The role of fleas as vectors of these different Bartonella species is deserving of further investigation through experimental models.

Wolbachia spp.

Wolbachia are endosymbiotic bacteria of the Anaplasmataceae family which have been associated with various arthropod species [66]. Wolbachia spp. has been detected in A. erinacei fleas sampled from A. algirus and E. europaeus hedgehogs from Algeria and Spain, respectively [21, 32]. These bacteria are known to be transmitted through transovarian and transstadial routes in arthropod populations [67]. However, they have no direct impact on human and animal health.

Mycobacterium spp.

Mycobacteria are Gram-positive bacilli bacteria. The diseases and symptoms that they cause in humans and animals depend on the bacterial species involved [3]. Only one published study has reported Mycobacterium spp. in 1/18 (5.5%) of A. erinacei fleas sampled from E. europaeus hedgehogs in Seville, Spain, but sequencing failed to identify this bacteria to the species level [32]. Different mycobacterial species, such as the causative agent of paratuberculosis in ruminants (Johne’s disease) Mycobacterium avium paratuberculosis, the agent of bovine tuberculosis M. bovis and M. avium, have been already reported in hedgehogs [3]. Two other studies reported M. marinum in both an African pygmy hedgehog (A. albiventris) in Japan and a European hedgehog [3]. These animals are, therefore, strongly suspected to be involved in the propagation of these bacteria. However, the involvement of fleas is still unknown, and further epidemiological investigations, together with experimental models, could help reveal whether the fleas have a vectorial capacity and competence, or whether the A. erinacei fleas in the study of Zurita et al. were positive only because they had ingested infected blood [3].

Coxiella burnetii

As described above, C. burnetii is a pathogenic agent distributed worldwide [39]. Only one study has reported the presence of this bacterium in four A. erinacei fleas sampled from A. algirus hedgehogs in the Bouira province in Algeria [21]. Organs as well as ticks sampled from the same hedgehogs that provided the fleas also tested positive for this bacterium [21]. Fleas are unusual hosts for C. burnetii, and it can be assumed that they acquired this pathogen by co-feeding with infected ticks or by ingesting blood from an infected host [21]. Further studies are needed to determine the role of fleas in the transmission cycle of Q fever.

All of the microorganisms reported in the different flea species sampled from hedgehogs are summarized in Fig. 4 and in Table 1.

Conclusions

This review provides information available in the literature on microorganisms detected in arthropods sampled from hedgehogs worldwide. Several microorganisms have been reported in ticks and fleas collected from these animals, including pathogenic agents which are responsible for zoonosis in animals and humans. The detection of these microorganisms in arthropods does not necessarily mean that they are vectors and that they can transmit the microorganisms to humans and animals. While the vector capacity and competence of fleas and ticks for some of these microorganisms has been proven, for others, such as Leptospira spp. and Mycobacterium spp., their detection in ticks and fleas must be viewed with some caution. They may simply have been ingested together with blood taken from an infected host. For this reason, further field epidemiological investigations, together with experimental models, are needed to clarify whether or not arthropods play a role in the maintenance and transmission of these bacteria. Until such evidence is forthcoming, these microorganisms detected in arthropods, in particular pathogenic ones, should nevertheless be added to the repertoire of microorganisms to be considered in the context of the epidemiological surveillance and diagnostic of hedgehog zoonoses.

In the present state of our knowledge, we have only a blurred picture of the role of hedgehogs as a reservoir host. Epidemiological studies on hedgehogs are difficult to conduct since they are protected animals and handling them is, therefore, highly regulated. Accordingly, their ectoparasites represent a very interesting source of information about the microorganisms circulating in these animal populations, especially vector-borne ones, without endangering them. Hedgehogs should also be dewormed to limit the risk of transmission of these pathogens to humans and other animals.

Data availability

All data regarding this study are included in the manuscript.

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Acknowledgements

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Funding

This study was supported by the Institut Hospitalo-Universitaire (IHU) Méditerranée Infection, the National Research Agency under the program “Investissements d’avenir”, reference ANR-10-IAHU-03, the Région Provence Alpes Côte d’Azur and European funding FEDER PRIMI.

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  1. Aix Marseille Univ, IRD, AP-HM, SSA, Vecteurs–Infections Tropicales et Méditeranéennes (VITROME), Marseille, France

    Linda Benkacimi, Adama Zan Diarra, Jean-Michel Bérenger & Philippe Parola

  2. IHU-Méditerranée infection, Marseille, France

    Linda Benkacimi, Adama Zan Diarra, Jean-Michel Bérenger & Philippe Parola

  3. Société Française d’Études et de Protection des Mammifères (SFEPM), Bourges, France

    Jean-Michel Bompar

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LB did the bibliography, wrote, and edited the original manuscript, constructed the figures and particpated in taking the arthropod photographs. PP and AZD supervised, validated, reviewed, and edited the manuscript. JMB and JMB took hedgehog pictures, reviewed and edited the manuscript. All authors reviewed and approved the final version of the manuscript.

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Correspondence to Philippe Parola.

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Benkacimi, L., Diarra, A.Z., Bompar, JM. et al. Microorganisms associated with hedgehog arthropods. Parasites Vectors 16, 211 (2023). https://doi.org/10.1186/s13071-023-05764-7

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Parasites & Vectors

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