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Systematic Review

Rickettsiales in Italy

by
Cristoforo Guccione
1,
Claudia Colomba
1,2,
Manlio Tolomeo
1,
Marcello Trizzino
2,
Chiara Iaria
3 and
Antonio Cascio
1,2,*
1
Department of Health Promotion, Mother and Child Care, Internal Medicine and Medical Specialties- University of Palermo, 90127 Palermo, Italy
2
Infectious and Tropical Disease Unit, AOU Policlinico “P. Giaccone”, 90127 Palermo, Italy
3
Infectious Diseases Unit, ARNAS Civico-Di Cristina-Benfratelli Hospital, 90127 Palermo, Italy
*
Author to whom correspondence should be addressed.
Pathogens 2021, 10(2), 181; https://doi.org/10.3390/pathogens10020181
Submission received: 31 December 2020 / Revised: 3 February 2021 / Accepted: 4 February 2021 / Published: 8 February 2021
(This article belongs to the Collection Updates on Rickettsia and Coxiella)
Browse Figure
Review Reports Versions Notes

Abstract

:
There is no updated information on the spread of Rickettsiales in Italy. The purpose of our study is to take stock of the situation on Rickettsiales in Italy by focusing attention on the species identified by molecular methods in humans, in bloodsucking arthropods that could potentially attack humans, and in animals, possible hosts of these Rickettsiales. A computerized search without language restriction was conducted using PubMed updated as of December 31, 2020. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology was followed. Overall, 36 species of microorganisms belonging to Rickettsiales were found. The only species identified in human tissues were Anaplasma phagocytophilum, Rickettsia conorii, R. conorii subsp. israelensis, R. monacensis, R. massiliae, and R. slovaca. Microorganisms transmissible by bloodsucking arthropods could cause humans pathologies not yet well characterized. It should become routine to study the pathogens present in ticks that have bitten a man and at the same time that molecular studies for the search for Rickettsiales can be performed routinely in people who have suffered bites from bloodsucking arthropods.

1. Introduction

Rickettsiales is an order of α-proteobacteria characterized by intracellular tropism with a wide variety of hosts. They are small, gram-negative bacteria that reside free in the host cell cytoplasm, and some of them can be transmitted to human hosts by arthropod vectors such as ticks, lice, fleas, and mites. As suggested by Szokoli et al. we considered included in this order only 3 families: Rickettsiaceae, Anaplasmataceae, and Candidatus Midichloriaceae. Rickettsiales encompass human and animal pathogens as well a lot of endosymbiont of arthropods, helminths, and algae with various, pathogenic or not manifestation in the host. The family Rickettsiaceae includes 2 genera: Rickettsia and Orientia. A modern classification based on whole-genome analysis divides the species of the genus Rickettsia in four groups: spotted fever group (R. rickettsii, R. conorii, R. parkeri, and several others), typhus group (R. prowazekii and R. typhi), ancestral group (R. bellii and R. canadensis, not known to be pathogenic), and transitional group (R. akari, R. australis, and R. felis) [1,2,3] Orientia tsutsugamushi is the etiologic agent of scrub typhus, a rickettsiosis that is widespread in Asia, the islands of the western Pacific and Indian Oceans, and foci in northern Australia [4]. The family Anaplasmataceae includes the genera Ehrlichia, Anaplasma, Wolbachia, and Neorickettsia. Only the members of the first two genera have been associated to human diseases. The genus Ehrlichia includes six species: E. canis, E. chaffeensis, E. ewingii, E. muris, E. ovis, and E. ruminantium. The genus Anaplasma includes A. marginale, A. centrale, A. ovis, A. mesaeterum, A. platys, and A. phagocytophilum; only the last is associated to human diseases. The family Candidatus Midichloriaceae does not include any bacteria associated to human disease.
Almost all the cases of human rickettsial diseases in Italy are cases of Mediterranean spotted fever (MSF) caused by R. conorii transmitted by the brown dog tick Rhipicephalus sanguineus. In Italy, about 400 cases of MSF are reported every year, most of which in people residing in Sicily, Sardinia and Southern Italy with a lethality of less than 3% [5] However, other pathologies such as Tibola/Debonel (Tick Borne Lymphadenopathy/Dermacentor Borne Necrosis Erythema and Lymphadenopathy [6]) and many other Rickettsia spp. or subspecies have been identified in recent years in humans, vector arthropods and animals [6]. Other rickettsioses that have been historically documented in Italy are murine typhus and epidemic typhus [5]. Since 1950, only sporadic cases of murine typhus have been reported, and Italy currently appears to be free of epidemic typhus. As in other European countries, imported cases of rickettsial pox, African tick-bite fever (ATBF), and scrub typhus have been reported [5].
The purpose of this study is to take stock of the situation on Rickettsiales in Italy by focusing attention on the genera until now identified by molecular methods in humans, in bloodsucking arthropods that could potentially attack humans, and in animals possible hosts of these Rickettsiales. Our research has therefore mainly focused on the genera Rickettsia, Anaplasma, Ehrlichia, and Orientia as these are the ones notoriously associated with human pathology until now.

2. Materials and Methods

For the writing of this review a computerized search without language restriction was conducted using PubMed. The search was performed combining the terms “Ricketts * AND Italy”, “Ehrlichi * AND Italy” and “Anaplasma AND Italy”, Orientia AND Italy”. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) methodology was followed [7]. Only studies that provided data about Rickettsiales identified by molecular methods in Italy were included in the review. All molecular methods which reached the species level were considered. A flow chart summarizing the literature research approach is reported in Figure 1.

3. Results

A total of 818 papers were retrieved by our search, of these 220 were duplicate and removed; the remains were assessed through their title and abstract and so other 273 were excluded; the selected 325 articles were assessed for eligibility through full text analysis and 168 were excluded as reported in Figure 1; finally, 157 published from 1997 to 2021 studies were included in this review.
The results of our search could be divided in four sections and are analytically reported in Table 1, Table 2, Table 3 and Table 4.
A total of 36 different Rickettsiales species belonging to genus Anaplasma, Ehrlichia and Rickettsia; never Orientia spp. were reported in Italy. 32 of them were identified in arthropods, 9 in animal samples, and 10 in human samples (Table 1, Table 2, Table 3 and Table 4).

3.1. Rickettsiales and Arthropod Vectors

Rickettsiales were identified in 29 species of arthropods, most of them were Ixodidae ticks, and 4 species of fleas. The reports present in the scientific literature are resumed in Table 1 and Table 2. Table 1 offer a view centered on the microorganism, for each Rickettsiales we report the known association with arthropods and from where it was collected. Indeed, Table 2 offers a point of view centered on the arthropods and for each we report which microorganism and host were associated.

3.2. Rickettsiales Identified in Animals

Rickettsiales have been identified 179 times in various animal infections, most of which were Anaplasma spp. especially in livestock, and R. conorii and E. canis especially in companion animals. Fifteen species of mammals with or without symptoms were found infected with Rickettsiales most of them where A. phagocytophilum and A. platy. Symptomatic animals were most often pets, with fever and blood count abnormalities (CBC) being the most frequently observed clinical findings; while asymptomatic animals were more often livestock. In Table 3 are resumed the findings in animal samples with clinical manifestations and the number of animals found positive for each Rickettsiales. When the original study was done on asymptomatic animals, with the aim of screening, we report also the number of total tested animals and the percentage of prevalence; when the studies was more than one, we report the highest and lowest percentage.

3.3. Rickettsiales Involved in Human Disease

Rickettsiales were detected 29 times in samples from human patients: 6 cases of anaplasmosis, and 23 cases of rickettsiosis. Rickettsiales species identified from human sample and their clinical manifestation are resumed in Table 4. Rickettsia spp. associated with MSF were R. conorii, R. conorii subsp. israelensis, R. conorii subsp. indica, R. massiliae, R. slovaca, and R. monacensis. Rickettsia spp. associated with TIBOLA/DEBONEL were R. slovaca, and R. massiliae. R. africae was identified only once in a traveler from Zimbabwe. R. aeschlimannii was associated to a case of acute hepatitis. A. phagocytophilum was identified in 6 cases of human illness.
Symptoms mostly associated with MSF were fever, maculopapular rash, and the presence of a necrotic eschar in site of the tick bite “tache noire” in French black spot. Cases of MSF caused by R. conorii subsp. israelensis were more severe, the rash was petechial and the tache noire was not always present. TIBOLA was characterized by the presence of an eschar in the scalp, and enlargement of suboccipital or neck lymph nodes; the eschar in the scalp typically resulted in an area of alopecia.
All the Italian case reports, with the identification of a Rickettsiales with molecular method, until species level are reported in Table 4 with the clinical manifestations and number of cases.

4. Discussion

The purpose of this article was to analyze all Rickettsiales identified in Italy and which could potentially cause disease in humans and to suggest doctors check whether Rickettsiales that infect arthropods or the animals they parasite can cause disease in man.
In this section, the findings of the single Rickettsiales species are analytically discussed.

4.1. Anaplasma spp.

Anaplasma spp. identified in Italy were A. marginale, A. ovis, A. platy and A. phagocytophilum, A. centrale, and A. bovis. The latter two were found only in sample from animals [98,99,100]. The other four, with the exception of A. platy, found only in ticks, were identified both in ticks and fleas. A. marginale and A. ovis were not a common detection the first was found in the ticks Haemaphysalis punctata and Rhipicephalus turanicus [93], and in the flea Xenopsylla cheopis [9]; the second in the ticks Ha. punctata [10], Rhipicephalus bursa [11] and in two fleas X. cheopis and Ctenocephalides canis [9].
The majority of largest report are about A. phagocytophilum, found in fleas as X. cheopis [9] and ticks belonging to Ha. punctata [10], Hyalomma marginatum from migratory birds [11], different species of Rhipicephalus like Rh. Bursa [13], Rh. turanicus [13,27] and Rh. Sanguineus [13,26,96]; while it was very often found in Ixodes ticks, of these the most common was I. ricinus. Ixodes spp. is the most diffused tick genera in Italy, it is present almost in every Italian region and climatic areas, from island to continental Italy and in both Tyrrhenian and Adriatic coast. Ixodes spp. was found infected with almost all Rickettsiales, from the most to the less common, also with the apparent foreign R. africae [36] and R. felis [48], usually most common in fleas than ticks. Furthermore, I. ricinus is the only tick in which Candidatus Ehrlichia walkerii was found in Italy [12,16,23,33]. I. ricinus was not found mostly on one animal than another, however, seems that it the only tick studied in Italy to be infected when feeding on lizards [78]. I. ventalloi is a tick collected from small animals and found infected both with Ehrlichia, Anaplasma and Rickettsia in Sicily [35,75] and Tuscany [50]; it has also been found in southern Italy to feed on humans [51]. I. acuminatus and I. festai are rare and have been found infected with some Anaplasma spp. [13,32]. Lastly, A. platy is a common detection in animal samples, and it was detected less frequently in arthropods; it was found in Hy. marginatum [11] from migratory bird, I. hexagonus [12] and in same tick belonging to Rhipicephalus [11,29,30,31]. Furthermore, co-infection by A. phagocytophilum and R. monacensis was detected in I. ricinus [22]. No animals are an evident favorite host for Anaplasma infected ticks. Studies about animal infection with Anaplasma spp. are prevalently screening ones conducted on livestock; however, there were also studies about symptomatic animals; A. phagocytophilum was identified in horses with flu-like presentation and in some cases with anemia, thrombocytopenia, jaundice, anorexia and leukocytosis [26,96,118,120,121]; A. phagocytophilum and A. ovis were identified in sheep with a poor general health condition [104] A. phagocytophilum was also identified in cows with acute anaplasmosis and presentation that includes hypo-galactia, mucosal paleness, fever and depression [98]. Other cases were diagnosed in pets, mostly infected by A. phagocytophilum and A. platy [28,29,102,103,108,112,126] less often infected by A. ovis, and A. marginale in screening studies in asymptomatic dogs [102]. A. phagocytophilum was found both in cats and dogs in which depression, fever, weakness and CBC abnormalities like thrombocytopenia, leukocytosis and neutrophilia were described [26,96,107,108,110,111,143] A. platy was found twice in cats [136], but there were no differences in the clinical presentation between cats and dogs; A. platy infects platelets and classically causes also thrombocytopenia, and monocytosis or neutropenia [29,96,126,127,128,129,130,131,132,134,135,136]. A. phagocytophilum was found both in cats and dogs, but more commonly in cats than A. platy; less common are the severe thrombocytopenia, and the symptoms were more non-specific.
Human granulocytic anaplasmosis (HGA) caused by A. phagocytophilum in Europe is not uncommon since the first identification of human illness linked to it in Slovenia in 1997, and human positivity before in 1995. Furthermore, serological surveys show that the illness could be underreported and a good number of asymptomatic patients do not have a diagnosis of anaplasmosis [164]. In humans the most common clinical presentation of anaplasmosis is febrile illness, with fever, weakness and sometimes CBC abnormalities [165] without rash or eschar in the site of tick bite. Differently to rickettsiosis, the clinical course can be subacute and persist for months. In Italy, cases of HGA were diagnosed in northeastern Italy, Sardinia and Sicily; of note the case of a patient misdiagnosed for months and treated also for depression before the correct diagnosis was achieved [163,164,165].

4.2. Ehrlichia spp.

In Italy Ehrlichia spp. has never been identified in human samples. Worldwide, Ehrlichia spp. is more often associated with canine pathology. In United States E. chaffeensis is the agent human monocytic ehrlichiosis and E. ewingii, a canine pathogen, cause of human illness only in immunodeficient or immunosuppressed patients [166].
In arthropods, three Ehrlichia spp. were identified in Italy, once E. ovina in a tick collected from a healthy sheep [10], more often E. canis both in ticks and fleas and Candidatus Ehrlichia walkerii, found in I. ricinus only in the northernmost regions [12,16,23,33]. E. canis was more commonly found in Rhipicephalus [12,27,34,46], Haemaphysalis [27,32,33], Hyalomma [34] and Dermacentor [27,34]; only once in Ixodes ticks, namely in I. ventalloi collected from a cat [35]. Haemaphysalis ticks carry prevalently Ehrlichia and Anaplasma; the genus is not very common, more often found in South and insular Italy. Three tick genera were found infected: Ha. punctata, Ha. sulcata more frequently, and only once Ha. inermis [51], nonetheless this latter is the only of the three collected from humans. Ha. punctata, the commonest species, seems to prefer the livestock and carry often Anaplasma [10,32,93] and Ehrlichia [10,32,97]. Ha. sulcata was found only in Sardinia and carries only two species: E. canis [27,34] and R. hoogstraalii [45,46]. Not frequently, Ehrlichia was found also in ticks non endemic in Italy, collected from migratory birds like Amblyomma spp. [36], Hyalomma rufipes [36] and Hy. marginatum [36,67]. No animal host preference is evident for ticks infected by Ehrlichia.
E. canis, identified in Italy only in samples from dogs, is the etiological agent of canine monocytic ehrlichiosis (CME), typically characterized by fever, depression, anorexia lymph adenomegaly, splenomegaly, hemorrhagic tendencies, pale mucosa, weight loss, ophthalmologic lesions, neurologic disorders, CBC abnormalities like anemia, leukopenia with lymphocytosis, hypoalbuminemia with hyperglobulinemia and increase in alanine aminotransferase, alkaline phosphatase and C-reactive protein [111,126,132,133,134,136,139,140,141,142]. Of note, E. canis in Venezuela has been identified in blood of humans with clinical signs compatible with human monocytic ehrlichiosis [167,168]. Furthermore, E. ruminantium, known as ruminant pathogen; has been recently considered an emergent pathogen for human after the report of three deaths associated with it in Africa [169].

4.3. Rickettsia spp.

4.3.1. R. africae

It is common in Sub-Saharan Africa and South Africa; in Italy it is a recent finding. Indeed, it was found in ticks endemic of African continent, like Amblyomma and Hyalomma, more often removed from migratory birds [19,36,39] and less often from terricolous animals like sheep and cattle [38,40]. R. africae has been identified also in I. ricinus removed from migratory birds in Italy [36]. Amblyomma has been recently introduced in Italy. Recent studies have documented that this tick can reproduce and could be became endemic also in Italy [37].
The human illness associated to R. africae is the African Tick Bite Fever (ATBF), similar to MSF but milder and without maculopapular rash; sometimes the eschars may be two. Occasionally, it can cause neuropathy [170]. R. africae has been identified in Italy in a woman returning from Zimbabwe, with fever, tache noire and rash in the limb ipsilateral to the eschar; the symptomatology was identified as a sacral syndrome, evident in the same side of the eschar [161].

4.3.2. R. aeschlimannii

It is often identified in Hyalomma ticks removed in small and big animals [32,34,36,38,41,43,44,45,46,48] and less commonly in Hyalomma ticks removed from humans [32,42,51], less common it was identified in other ticks as Amblyomma [36,41], D. marginatus [42], I. ricinus [42,52,53], and R. turanicus [53]. Its main host, Hyalomma, is an African tick typically found when feeding on migratory birds [36,39,41], nonetheless it is common to find these ticks in terricolous animal like sheep, wild boar, or other. It is usually found in Italy in the Tyrrhenian coast on the route of migratory birds. The species of Hyalomma found infected in Italy were Hy. marginatum, Hy. rufipes, Hy. lusitanicum, Hy. detritum, Hy. sulcata, Hy. truncatum. R. aeschlimannii was found mainly in Tyrrhenian Italy, on the route of migratory birds. Furthermore, R. aeschlimannii was identified in A. marmoreum [41], another African tick, removed from migratory birds. The first findings of R. aeschlimannii was in a Hyalomma tick in Morocco, Zimbabwe, Mali and Niger in 1996 [171,172]. The first report of human infection dates back to 2000 in a French traveler returning from Morocco; clinical findings were fever, tache noire, and elevated serum liver enzymes; the only Italian case was reported in a man with a strong increase in hepatic enzymes [162]. In the above case, R. aeschlimannii was identified in the liver biopsy. PCR on whole blood was negative, differently to the case reported in France. Of note, R. aeschlimannii was also identified in the skin of a Greek patient with a single skin manifestation similar to “erythema chronicum migrans” of Lyme disease [173].

4.3.3. R. conorii

It is the Rickettsia spp. classically associated with MSF. R. conorii subsp. israelensis and R. conorii subsp. indica have also been associated with MSF in Italy.
R. conorii has been identified in domestic and wild animals, in domestic dogs, and in wild in a road killed otter [145]. R. conorii in dogs has been associated with illness in dogs, with fever, anemia, and thrombocytopenia being the main symptoms, sometimes associated with lethargy [106,112,132,144].
Generally, the clinical symptoms of MSF caused by R. conorii begin 4 to 10 days following the tick bite and the signs of the disease may be fever (95%–100%), flu-like symptoms (78%), sore head and muscle aches (64%), skin rash within 6 to 10 days (87%–96%), and eschar (tache noire), blackish ulcero-necrotic area at the site of the tick bite (52%–77%). In most subjects, the rash is maculo-papular and also affects the soles of the feet and palms of the hands. The typical signs of these rickettsioses, with the formation of papules, petechiae and rash, are a direct consequence of the colonization and damage of the vascular endothelium by these pathogens. MSF may be complicated by cardiac symptoms (coronary artery ectasia, myocarditis and atrial fibrillation), ocular symptoms (uveitis, retinal vasculitis and retinopathy), neurological symptoms (cerebral infarction, meningoencephalitis have been reported and, sensorineural hearing loss), pancreatic involvement, splenic rupture and acute renal failure, and by hemophagocytic syndrome [146,148,149,150,151,152,153,174,175,176,177,178,179,180,181,182]
MSF caused by R. conorii subsp. israelensis is a more severe disease than R. conorii’s one; the rash is often petechial and the tache noire is almost always absent. Many complications have been reported like neurological involvement [155]. R. conorii subsp. indica was identified only once from an inoculation eschar sample of MSF patient in Sicily [154].

4.3.4. R. helvetica

R. helvetica has been identified mountainous territory, more often in northern Italy and in areas far from the coast. It was identified in I. ricinus removed from small animals [22,55,62,67,72,74,76], deers [62,76], vegetation [64,65,66,68,70,71,73] and human [14,23,51,77]. It was also identified in I. festai [32,34,45] I. acuminatus [50], I. ventalloi [50,51,75] and I. trianguliceps [62]. However, the geographical distribution of these last three Ixodes is different: I. acuminatus was found in central-north Italy, far from the coast. I. festai only in Sardinia and I. trianguliceps in the eastern alps. Only once it was found in R. sanguineus collected in vegetation [68]
In humans, R. helvetica infection presents as a mild disease associated with fever, headache, and myalgia but not with a cutaneous rash. In Italy only one human case of disease caused R. helvetica presenting with fever, headache, myalgia and arthralgia was diagnosed only by serology [183]. However, R. helvetica has been identified in Sweden in two case of meningitis, in one of these R. helvetica was identified in the cerebrospinal fluid [182,184].

4.3.5. R. massiliae

R. massiliae belongs to the spotted fever group rickettsiae, and is distributed worldwide. The ticks in which R. massiliae was more commonly identified in Italy were R. sanguineus [32,42,43,45,46,47,48,49,56,67,79], and R. turanicus [42,43,47,48,53]. Less commonly it was found in I. ricinus [48,52,53], never this happened in Sicily or in Sardinia.
The first human case of R. massiliae infection was diagnosed in a Sicilian patient with MSF; the second case was in a patient in southern France who had MSF complicated by acute loss of vision; and the third case was in a woman in Argentina who had fever, a palpable purpuric rash, and tache noire. Two cases of TIBOLA/DEBONEL caused by R. massiliae have been described in Italy: one in in north Italy, the other in Sicily [157,158].

4.3.6. R. monacensis

In contrast with the other species, most common in the south and insular regions, R. monacensis is most common in the inland. I. ricinus [22,48,49,52,54,55,64,66,68,69,70,71,72,74,75,76,78,80,81,82,84] and I. ventalloi [75] were found infect by this species. Less often R. monacensis was found in D. marginatus [51,53], Ha. punctata [48,80], R. sanguineus [48,68,75], and R. turanicus [53]. Furthermore, R. monacensis was detected inside Crataerina pallida, a hematophagous diptera [54]. Sometimes R. monacensis has been found coinfecting a tick, and another time with R. tamurae [62]. In humans, R. monacensis may cause MSF-like illness as described by Jado et al. [185] in Spain. In Italy, it has been identified only once, in the eschar biopsy of an anaeructive MSF in Sardinia [160].

4.3.7. R. slovaca and Other Agents of TIBOLA/DEBONEL/SENLAT

The first identification of R. slovaca, and the related illness, was in France in 1996 from a woman bitten by a D. marginatus in the scalp; the woman complained of fatigue, lymphadenopathy, fever, eschar with erythematous halo and no rash; later, also R. raoultii and R. rioja were associated with this syndrome [186,187,188].
Dermacentor ticks infected with the above rickettsiae were found prevalently in Tyrrhenian coast and western alps and have a period of activity cold season (from late fall to mid spring [186]). The tick species found infected were D. reticulatus [89] and D. marginatus [32,34,40,42,43,45,46,51,61,72,80,83,84,85,86,87,88,90,92], the first was found only once in the western alps on a wild boar, the second was more commonly found. Other ticks involved in ecology of R. slovaca are Ha. punctata [40], Hy. sulcata [34], I. ricinus [48,80,87], I. hexagonus [48], and R. sanguineus [42,51]. Wild boar appears to be the favorite host for infected Dermacentor spp., nonetheless R. slovaca was not found in ticks collected more often from one animal than others.
R. raoultii [46,51,61,72,83,84,85,86,87] and R. rioja [88], were both found in Italy in D. marginatus and, R. raoultii in other ticks like Ixodes spp. [48,52,62], Rhipicephalus spp. [46] and Hyalomma spp. [41].
For TIBOLA and DEBONEL, was proposed by the Marseille group the name SENLAT (scalp eschar and neck lymphadenopathy after tick bite) to bring together the clinical manifestation without etiological differentiation. Indeed, others tick-borne pathogen than R. slovaca as R. massiliae, Bartonella henselae and Borrelia burgdorferi have been associated with this syndrome [157,158,189,190].
R. slovaca has been documented as agent of TIBOLA also in Italy [92]. Of note, R. slovaca was also identified in Sicily in a “MSF like” case [154].

4.3.8. R. felis

R. felis is typically found in Ctenocephalides felis [9,35,58,59,60], the common flea of the cat. Of note, C. felis can parasite also other mammals like dogs or foxes. R. felis in Italy has been sometimes identified in I. hexagonus [48] and in R. turanicus [61], but never in humans. The disease caused by R. felis is similar to murine typhus, with fever, myalgia, headache, and rash [189,190]; the eschar may be present. Severe complication, like meningoencephalitis, may occur [191]. R. felis has also been identified in a cutaneous swab of a Senegalese 8-month-old girl with “yaaf”, a febrile illness associated with a cutaneous eruption [192].
The only Italian case of R. felis infection occurred in a traveler from Nepal and was confirmed with indirect fluorescent antibody tests in 2015. The patient complained headache, fever, nausea and vomiting, a raising in liver enzymes was also observed. Interestingly Nepal’s altitude is not well suitable for ticks or fleas, the patients report multiple attack by aquatic leeches, removed with water and salt [193]. The most recent review worldwide that describe the diffusion of R. felis was published in 2016 [194]. In consideration of the spread of flea infection found in Italy, it is possible that the disease may be present in Italy even if it is generally not sought.

4.3.9. Other Rickettsia spp.

Other Rickettsia spp. identified in arthropods in Italy were R. belli [54] R. hoogstraalii [32,45,78], R. limoniae [70], R. peacockii [51], R. rhipicephali [79], R. sp. Strain S [40], R. sp. strainTwKm01 [53], Candidatus R. barbariae [32,43,47], Candidatus R. siciliensis [89], Candidatus R. mendelii [74], R. honei [40], R. tamurae [42], R. rioja [88], R. limoniae [70], R. raoultii [41,46,48,51,52,61,62,72,83,84,85,86,87]. R. belli, interestingly, was identified in Crataerina pallida, an Hippoboscidae hematophagous dipter [54]. None of the above Rickettsia spp. has ever been associated with human disease all over the world.
R. sibirica mongolotimoniae and R. akari have never been identified in Italy. R. sibirica mongolotimoniae is etiological agent of Lymphangitis Associated Rickettsiosis (LAR) [195]. It is frequently associated with Hyalomma spp., ticks widely distributed across the Tyrrhenian coast of Italy. Since the discovery in 1996 of a case of human illness associated with it, it has been documented in France, Spain and Greece and other country. The disease could be present also in Italy and for this reason it is under surveillance according to the report of European Centre for Disease Prevention [196].
R. akari is the agent of rickettsial pox and is transmitted by the Lyponyssoides sanguineus, the house-mouse-mite. Cases of rickettsial pox have been reported from all continents. R. akari infection presents with a triad of fever, vesicular rash, and eschar. Between the first and fourth day of fever a papulovesicular eruption occurs on many parts of the body except the palms of the hands and soles of the feet. The eruption is nonpruritic and resolves without leaving scars. In Italy, R. akari has never been identified in humans, in mite or in animal [186].
R. prowazekii, the agent of louse-borne typhus. This disease occurs in colder regions of central and eastern Africa, central and South America, and Asia. In recent years, most outbreaks have taken place in Burundi, Ethiopia and Rwanda. Typhus fever occurs in conditions of overcrowding and poor hygiene, such as in prisons and refugee camps. Cases of louse-borne typhus in Italy were reported before World War II. R. prowazekii has never been identified in Italy by molecular methods. Symptoms of epidemic typhus begin within 2 weeks after contact with infected body lice. Signs and symptoms may include: headache, confusion, fever and chills, rapid breathing, cough, vomiting, muscle aches, and rash. R. prowazekii can remain dormant for years or even decades in patients who recover from the primary infection. In certain individuals, stress or waning immunity are likely to reactivate this persistent infection, and cause a recrudescent form of typhus known as Brill-Zinsser disease [197]. A case of seroconversion to R. prowazekii in a homeless person has been reported in France in 2005 [198]. The current migratory flows from Africa to Italy require us to pay attention to this disease which could reactivate in people exhausted by the travel and the discomfort suffered in the prison camps.
R. typhi, the agent of flea-borne typhus. It occurs in tropical and subtropical climates around the world including areas of the United States. Symptoms of flea-borne typhus begin within 2 weeks after contact with infected fleas. Signs and symptoms may include: Fever and chills, body aches and muscle pain, vomiting, cough, and rash that typical occurs around day 5 of illness. Since 1950, only sporadic cases of murine typhus have been reported, and R. typhi has never been identified in Italy by molecular methods. However, a case murine typhus diagnosed only by serology in a 75-year-old woman presenting with spotted fever followed by acute renal failure and septic shock was recently described in south Italy [199].

4.4. Orientia spp.

Orientia tsutsugamushi is the etiologic agent of scrub typhus, a rickettsiosis that is widespread in Asia, the islands of the western Pacific and Indian Oceans, and foci in northern Australia. It is transmitted by the bites of larval trombiculid mites (chiggers) of the genus Leptotrombidium. Recent evidences from Africa, France, the Middle East, and South America, have led to the supposition that scrub typhus should no longer be considered restricted to Asia and Western Pacific [200]. Besides, cases of travel-associated scrub typhus have been reported from Europe, North America, and Japan [201]. Symptoms of scrub typhus usually begin within 10 days of being bitten. Signs and symptoms generally include: headache, fever and chills, muscle pain, a black eschar in the site of the chigger bite, enlarged lymph nodes and maculopapular rash [202]. In Italy, Orientia spp. has never been identified neither in man nor in animals nor in mites.

5. Conclusions

Rickettsiales found in humans in Italy were: R. aeschlimannii, R. africae, R. massiliae, R. monacensis, R. slovaca, R. conorii, R. conorii subsp. israelensis, R. conorii subsp. indica and A. phagocytophilum. MSF and TIBOLA and HGA were the most frequent clinical manifestations. E. canis, A. platy and A. phagocytophilum were the most frequently identified Rickettsiales found in dogs and cattle, respectively. Other Rickettsiales identified were: A. bovis, A. ovis, A. marginale, A. centrale, A. platy, E. ovina, Candidatus N. mikurensis, Candidatus R. siciliensis, Candidatus R. barbariae, Candidatus. R. mendelii, R. hoogstraalii, R. limoniae, R. peacockii, R. rhipicephali, R. sp. Strain S, R. sp. strainTwKm01, R. belli, R. tamurae, R. rioja, R. limoniae, R. raoultii, R. honei; some of them, even if it has not yet been demonstrated, could in the future be shown to be capable of causing in humans not yet well characterized syndromic pictures. That’s why molecular studies for the search for Rickettsiales should be routinely performed in people who have been bitten by bloodsucking arthropods.

Author Contributions

Conceptualization, A.C.; methodology, A.C.; software, C.G.; validation, A.C., C.C. and C.I.; formal analysis, C.G.; investigation, C.G.; resources, C.C, C.G.; data curation, C.C., C.G., M.T. (Manlio Tolomeo) and M.T. (Marcello Trizzino); writing—original draft preparation, C.G.; writing—review and editing, C.C., C.I., C.G., M.T. (Manlio Tolomeo) and M.T. (Marcello Trizzino); visualization, C.C., C.I. and M.T. (Manlio Tolomeo); supervision, A.C.; project administration, A.C.; funding acquisition, A.C. All authors have read and agree to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created or analyzed in this study. Data sharing is not applicable to this article.

Conflicts of Interest

The authors declare no conflict of interest.

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Pathogens 10 00181 g001 550
Figure 1. Process of selection of articles for the review according to PRISMA methodology [7]. *: Bibliography.
Figure 1. Process of selection of articles for the review according to PRISMA methodology [7]. *: Bibliography.
Pathogens 10 00181 g001
Table
Table 1. Species of Rickettsiales, arthropods from which they were identified and corresponding hosts.
Table 1. Species of Rickettsiales, arthropods from which they were identified and corresponding hosts.
RickettsialesArthropodCollected FromReference
Anaplasma marginaleHaemaphysalis punctataCattle[8]
Rhipicephalus turanicusCattle[8]
Xenopsylla cheopisFox[8]
A. ovisCtenocephalides canisFox[9]
Haemaphysalis punctataSheep[10]
Rhipicephalus bursaGoat, mouflon[11]
Rhipicephalus sanguineus s.l.Dog[12]
Xenopsylla cheopisFox[9]
A. phagocytophilumHaemaphysalis punctataSheep[10]
Ixodes ricinusBird, cat, dog, fallow deer, free life, horse, human, red deer, rodent, roe deer, sheep, vegetation[12,13,14,15,16,17,18,19,20,21,22,23,24]
Ixodes ventalloiVegetation[25]
Hyalomma marginatumMigratory birds[11]
Ixodes acuminatusDog[13]
Rhipicephalus sanguineusDog[13,26]
Rhipicephalus turanicusDog, horse, sheep, goat[13,27]
Rhipicephalus bursaDog[13]
Xenopsylla cheopisFox[9]
A. platyIxodes hexagonusDog[12,28]
Hyalomma marginatumWild boar[11]
Rhipicephalus bursaGoat[11]
Rhipicephalus sanguineusDog[29,30]
Rhipicephalus sp. IIDog[31]
Anaplasma spp.Haemaphysalis punctataMouflon[32]
Ixodes festaiHedgehog[32]
Rhipicephalus bursaMouflon, cattle, fox[32]
Rhipicephalus sanguineus s.l.Cat, fox, goat, marten, mouflon[32]
Candidatus Ehrlichia walkeriiIxodes ricinusDog, goat, human, sheep, vegetation,[12,16,23,33]
E. ovinaHaemaphysalis punctataSheep[10]
E. canisCediopsylla inaequalisFox[9]
Dermacentor marginatusMouflon, wild boar[27,34]
Haemaphysalis punctataMouflon[32]
Haemaphysalis sulcataGoat, mouflon[27,34]
Hyalomma marginatumSheep, swine[34,35]
Ixodes ventalloiCat[35]
Rhipicephalus bursaDeer, sheep, goat[32,34]
Rhipicephalus sanguineus s.l.Dog, fox, sheep[12,32,34]
Rhipicephalus sanguineusDog[27]
Xenopsylla cheopisFox[9]
Ehrlichia spp.Amblyomma spp.Migratory birds[36]
Hyalomma marginatumMigratory birds[36]
Hyalomma rufipesMigratory birds[36]
Rickettsia africaeAmblyomma marginatusSheep[37]
Amblyomma variegatumMigratory birds[38,39]
Hyalomma marginatumCattle[40]
Hyalomma rufipesMigratory birds[41]
Hyalomma spp.Migratory birds[36]
Ixodes ricinusMigratory birds[36]
R. aeschlimanniiAmblyomma marmoreumMigratory birds[41]
Dermacentor marginatusHuman[41]
Hyalomma marginatumBird, cattle, dog, free life, goat, hedgehog, migratory birds, horse, human, mouflon, red deer, sheep, vegetation[32,34,36,38,40,42,43,44,45,46,47,48,49,50]
Hyalomma lusitanicumHuman, free life[42,46,51]
Hyalomma rufipesMigratory birds[36,38,39,41]
Hyalomma truncatumMigratory birds[38]
Hyalomma detritumVegetation[50]
Ixodes ricinusFree life, human[42,52,53]
Rhipicephalus turanicusFree life[53]
R. barbarie (candidatus)Rhipicephalus sanguineus s.l.Dog, fox, goat[32]
Rhipicephalus turanicusGoat, sheep[43,47]
R. belliHippoboscidae Crataerina pallidaBird[54]
R. conoriiIxodes ricinusFree life[53]
Rhipicephalus turanicusBrown Hare, cattle, free life, human[40,42,48,53]
Rhipicephalus sanguineusDog, free life[49,55,56]
Rhipicephalus sanguineus s.l.Human[42]
R. conorii subsp. israelensisRhipicephalus sanguineusDog[43,57]
Rhipicephalus sanguineus s.l.Dog, fox, goat[32]
R. felisCtenocephalides felisDog, cat, fox[9,35,58,59,60]
Ixodes hexagonusFox, hedgehog[48]
Rhipicephalus turanicusSheep[61]
R. helveticaIxodes ricinusBird, cat, dog, fox, free life, human, lizard, migratory birds, red deer, rodent, roe deer, vegetation[22,23,48,51,52,55,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78]
Ixodes ventalloiBird, cat, human[50,51,75]
Ixodes festaiCat, hedgehog[45,46,67]
Ixodes acuminatusCat, red partridge[50]
Ixodes triangulicepsRodent[62]
Rhipicephalus sanguineusVegetation[68]
R. honeiHyalomma marginatumCattle[40]
R. hoogstraaliiHaemaphysalis punctataMouflon, sheep[45,46]
Haemaphysalis sulcataMouflon, sheep[45,46]
Ixodes ricinusLizard[78]
R. IRS3Ixodes ricinusMigratory birds, vegetation[64,74]
Ixodes ventalloiCat[50]
R. limoniaeIxodes ricinusVegetation[70]
R. massiliaeIxodes ricinusFree life, human[48,52,53]
Rhipicephalus turanicusBrown hare, cattle, free life, goat, human[42,43,47,48,53]
Rhipicephalus sanguineus s.l.Dog, fox, goat, human, sheep[32,36,42,46,48]
Rhipicephalus sanguineusDog, fox, human, cat[43,45,49,56,79]
R. mendelii (candidatus)Ixodes ricinusMigratory birds[74]
R. monacensisDermacentor marginatusFree life, human[51,53]
Haemaphysalis punctataChamois, fallow deer[48,80]
Hippoboscidae Crataerina pallidaBird[54]
Ixodes ricinusBear, cat, chamois, dog, fallow deer, free life, goat, hare, human, lizard, migratory birds, red deer, rodent, roe deer, vegetation, wild boar, wolf[22,48,51,52,53,55,62,64,66,68,69,70,71,72,74,75,76,77,78,80,81,82]
Rhipicephalus sanguineus s.l.Cat, dog[48,75]
Rhipicephalus turanicusFree life[53]
Rhipicephalus sanguineusVegetation[68]
R. tamuraeIxodes ricinusHuman, red deer[62]
R. peacockiiDermacentor marginatusHuman[51]
R. raoultiiDermacentor marginatusDeer, human, rodent, wild boar[45,51,61,72,83,84,85,86,87]
Hyalomma spp.Migratory birds[41]
Ixodes hexagonusBadger[48]
Ixodes ricinusFree life, red deer[52,62]
Rhipicephalus sanguineus s.l.Dog[46]
R. rhipicephaliRhipicephalus sanguineusCat[79]
R. riojaDermacentor marginatusVegetation, wild boar[88]
Candidatus R. siciliensisRhipicephalus turanicusHuman[89]
R. slovacaDermacentor marginatusCattle, chamois, deer, dog, human, red deer, rodent, roe deer, sheep, swine, vegetation, wild boar[32,34,39,42,43,45,46,48,51,61,72,80,83,84,85,86,87,88,90]
Dermacentor reticulatusWild Boar[88]
Haemaphysalis punctataCattle[40]
Hyalomma sulcataDog, sheep[34]
Ixodes ricinusHuman, red deer, wild boar[48,80,87]
Rhipicephalus sanguineus s.l.Human[42]
Rhipicephalus sanguineusHuman[51]
R. sp strain SHyalomma marginatumCattle[42]
R. sp. strain TwKm01Ixodes ricinusFree life[53]
Rhipicephalus turanicusFree life[53]
Rickettsia spp.Haemaphysalis inermisHuman[51]
Rhipicephalus annulatusCattle[91]
Rhipicephalus bursaCattle[91]
Rhipicephalus turanicusFox[49]
Table
Table 2. Arthropod species found infected with Rickettsiales in Italy.
Table 2. Arthropod species found infected with Rickettsiales in Italy.
ArthropodsRickettsialesArthropods Collected FromReference
Amblyomma marginatusR. africaeSheep[37]
Amblyomma marmoreumR. aeschlimanniiMigratory birds[41]
Amblyomma spp.Ehrlichia spp.Migratory birds[36]
R. aeschlimanniiMigratory birds[36]
Amblyomma variegatumR. africaeMigratory birds[38,39]
Cediopsylla inaequalisE. canisFox[9]
Ctenocephalides canisA. ovisFox[9]
Ctenocephalides felisR. felisCat, dog, fox[9,35,58,59]
Dermacentor marginatusE. canisMouflon, wild boar[27,34]
R. aeschlimanniiHuman[42]
R. monacensisFree life, human[51,53]
R. peacockiiHuman[51]
R. raoultiiDeer, human, rodent, wild boar[23,46,51,83,84,85,86,87]
R. riojaVegetation, wild boar[88]
R. slovacaCattle, chamois, deer, dog, human, red deer, rodent, roe deer, sheep, swine, vegetation, wild boar[32,34,40,42,43,46,48,51,61,72,80,83,84,85,86,87,88,90,92]
Dermacentor reticulatusR. slovacaWild Boar[88]
Haemaphysalis inermisRickettsia spp.Human[51]
Haemaphysalis punctataA. marginaleCattle[8,93]
A. ovisSheep[10]
A. phagocytophilumSheep[10]
Anaplasma spp.Mouflon[32]
E. canisMouflon[32]
E. ovinaSheep[10]
R. hoogstraaliiMouflon, sheep[32,45]
R. monacensisChamois, fallow deer[48,80]
R. slovacaCattle[40]
Hippoboscidae Crataerina pallidaR. belliBird[54]
R. monacensisBird[54]
Hyalomma detritumR. aeschlimanniiVegetation[50]
Hyalomma lusitanicumR. aeschlimanniiHuman, free life[42,46,51]
Hyalomma marginatumA. platyMigratory birds[11]
A. phagocytophilumMigratory birds[11]
E. canisSheep, swine[34]
Ehrlichia spp.Migratory birds[36]
R. africaeCattle[40]
R. aeschlimanniiBird, cattle, dog, free life, goat, hedgehog, horse, human, migratory birds, mouflon, red deer, sheep, vegetation[32,34,36,38,40,42,43,44,45,46,47,48,50]
R. honeiCattle[40]
R. sp strain SCattle[40]
Hyalomma rufipesEhrlichia spp.Migratory birds[36]
R. africaeMigratory birds[41]
R. aeschlimanniiMigratory birds[36,38,39,41]
Hyalomma spp.R. raoultiiMigratory birds[41]
Hyalomma sulcataR. slovacaDog, sheep[34]
Hyalomma truncatumR. aeschlimanniiMigratory birds[38]
Ixodes acuminatusA. phagocytophilumDog[13]
R. helveticaCat, red partridge[50]
Ixodes hexagonusA. platyDog[12]
R. felisFox, hedgehog[48]
R. raoultiiBadger[48]
R. slovacaBadger[48]
Ixodes festaiAnaplasma spp.Hedgehog[32]
R. helveticaCat, hedgehog[32,34,45]
Ixodes ricinusA. phagocytophilumBird, cat, dog, fallow deer, free life, horse, human, red deer, sheep, vegetation[12,13,15,16,17,19,20,21,22,23,24,62,94,95]
Candidatus Ehrlichia walkeriiDog, goat, human, sheep, vegetation, human[12,16,23,33]
R. africaeMigratory birds[36]
R. aeschlimanniiFree life, human[42,52,53]
R. conoriiFree life[53]
R. helveticaBird, cat, dog, fox, free life, human, lizard, migratory birds, red deer, roe deer, vegetation[23,51,52,55,61,62,63,64,65,66,67,68,69,70,71,72,73,74,76,78]
R. hoogstraaliiLizard[78]
R. IRS3Migratory birds, vegetation[64,74]
R. limoniaeVegetation[70]
R. massiliaeFree life, human[48,52,53]
Candidatus R. mendeliiMigratory birds[74]
R. monacensisBear, cat, chamois, dog, fallow deer, free life, goat, hare, human, lizard, migratory birds, red deer, roe deer, rodent, vegetation, wild boar, wolf[22,48,49,51,52,53,55,64,66,68,69,70,71,72,74,75,76,78,80,81,82,84]
R. tamuraeHuman, red deer[62]
R. raoultiiFree life, red deer[52,62]
R. slovacaHuman, red deer, wild boar[48,80,87]
R. sp. strain TwKm01Free life[53]
Ixodes triangulicepsR. helveticaRodent[62]
Ixodes ventalloiA. phagocytophilumVegetation[25]
E. canisCat[35]
R. helveticaBird, cat, human[50,51,75]
R. IRS3Cat[50]
R. monacensisCat[75]
Rhipicephalus annulatusRickettsia spp.Cattle[91]
Rhipicephalus bursaA. phagocytophilumDog[11]
A. platyGoat[11]
Anaplasma spp.Mouflon[11]
A. ovisGoat, mouflon[11]
Anaplasma spp.Cattle, fox, goat[11]
E. canisDeer, goat, sheep[32,34]
Rickettsia spp.Cattle[91]
Rhipicephalus sanguineusA. phagocytophilumDog[13,96]
A. platyDog[29,30]
E. canisDog[27]
R. conoriiDog, free life[49,55,56]
R. conorii subsp. israelensisDog[43,57]
R. helveticaVegetation[68]
R. massiliaeCat, fox, human[43,45,47,49,56,79]
R. rhipicephaliCat[79]
R. monacensisVegetation[68]
R. slovacaHuman
Rhipicephalus sanguineus s.lA. ovisDog[12]
Anaplasma spp.Cat, fox, goat, marten, mouflon[32]
E. canisDog, fox, sheep[12,32,34]
Candidatus R. barbariaeDog, fox, human[32]
R. conoriiHuman[42]
R. conorii subsp. israelensisDog, fox, goat[32]
R. massiliaeDog, fox, goat, human, sheep[32,34,42,46,48]
R. monacensisCat, dog[48,75]
R. raoultiiDog[46]
R. slovacaHuman[42]
Rhipicephalus sp. IIA. platyDog[31]
Rhipicephalus turanicusA. marginaleCattle[8]
A. phagocytophilumDog, horse, sheep, goat[13,27]
R. aeschlimanniiFree life[53]
Candidatus R. barbariaeGoat, sheep[43]
R. conoriiBrown Hare, cattle, free life, human[40,42,48,53]
R. felisSheep[61]
R. massiliaeBrown Hare, cattle, free life, goat, human[42,43,47,48,53]
R. monacensisFree life[53]
Candidatus R. siciliensisHuman[89]
R. sp. strain TwKm01Free life[53]
Rickettsia spp.Fox[97]
Xenopsylla cheopisA. marginaleFox[9]
A. ovisFox[9]
A. phagocytophilumFox[9]
E. canisFox[9]
Table
Table 3. Rickettsiales identified in wild and domestic animal tissues in Italy.
Table 3. Rickettsiales identified in wild and domestic animal tissues in Italy.
RickettsialesAnimalClinical ManifestationNumber of Positive/Tested Animals (%)Reference
Anaplasma bovisCattleNo symptoms1/51 (1.9%)[98]
SheepNo symptoms3/20 (15%)[99]
A. centraleCattleAcute anaplasmosis: hypo-galactia, mucosal paleness, depression high temperature (40–45 °C), anemia, thrombocytopenia, erythrocytic inclusion26/270 (8–21%)[98,100]
A. marginaleCattleNo symptoms535/2500 (2.3–76,4%)[8,93,98,99,100,101,102,103,104,105]
DogNo symptoms2/46 (4.3%)[102]
GoatNo symptoms95/184 (27–85%)[99,102,106]
HorseNo symptoms26/134 (19.4%)[102]
RodentNo symptoms3/69 (4.3%)[102]
SheepNo symptoms35/286 (12.2%)[102]
A. ovisCattleNo symptoms22/374 (5.9%)[102]
DogNo symptoms2/46 (4.3%)[102]
GoatNo symptoms113/468 (14.9–85%)[99,101,102]
HorseNo symptoms23/134 (17.1%)[102]
RodentNo symptoms23/69 (33%)[102]
SheepNo symptoms164/716 (11–81.8%)[10,93,99,101,102,103,104]
A. phagocytophilumCattleNo symptoms233/984 (2–88%)[99,100,101,102,105,106]
CatLymphadenomegaly, pale mucous, stomatitis, sign of respiratory involvement47/360 (1–31.9%)[101,107]
ChamoisNo symptoms6/9 (66.6%)[19]
DogFever, acute lameness to right forelimb, depression, jaundice, dysorexia, leukocytosis, neutrophilia, thrombocytopenia, mild anemia15[26,96,102,107,108,109,110,111,112]
DonkeyNo symptoms3/3 (100%)[93]
Fallow deerNo symptoms42/80 (40%)[24,113]
FoxNo symptoms18/277 (0.8–10.8%)[114,115,116]
GoatNo symptoms55/203 (16.9–72%)[103,117]
HorseHyperthermia, anemia, anorexia, jaundice, myalgia, reluctance to move, thrombocytopenia, leukocytosis45[26,96,103,118,119,120,121,122]
Red deerNo symptoms66/119 (54–59%)[116,123]
RodentNo symptoms56/2259 (3–5.3%)[12,103,124]
Roe deerNo symptoms32/116 (19–75%)[103,116,125]
SheepScreening or poor health condition166/1496 (0.1–81%)[10,99,103,104,117,118,119]
A. platyDogDepression, myalgia, anorexia, fever, epistaxis, rough coat, reluctance to move, diarrhea, lymphadenomegaly, weight loss, pale mucous membranes, high hepatic enzymes, splenomegaly, ascites, thrombocytopenia, anemia, mono-cytosis, eosinophilia, neutropenia or neutrophilia hypoalbuminemia; evidence of vertical transmission181[26,29,30,56,96,103,112,126,127,128,129,130,131,132,133,134,135,136]
CatThrombocytopenia, anemia, or leukopenia/ leukocytosis14[135]
Candidatus Neoehrlichia mikurensisRodentNo symptoms1/34 (2.9%)[125]
Ehrlichia canisCatNo symptoms2/85 (2.3%)[19]
FoxNo symptoms113/225 (52–56%)[137,138]
DogPulmonary hypertension, fever, anemia, tongue ulcer, lymphadenopathy, polyclonal gammopathy, weight loss, anorexia, dermatitis, epistaxis78[111,126,132,133,134,136,139,140,141,142]
Gray wolvesNo symptoms3/6 (50%)[138]
E. ovinaSheepNo symptoms1/87 (1.1%)[10]
Ehrlichia spp.Catlymphadenopathy, pale mucous, stomatitis, sign of respiratory involvement14/260 (5.3%)[143]
Rickettsia conoriiDogFever, anemia, thrombocytopenia, leukocytosis, hunched posture, abdominal pain, orchitis, splenomegaly, lymphadenopathy, vomiting, diarrhea, hyperglobulinemia, elevated liver enzyme27[106,112,133,144]
Eurasian OtterCarcass1/1 (100%)[145]
Rickettsia spp.Catlimp adenomegaly, pale mucous, stomatitis, sign of respiratory involvement83/260 (31.9%)[143]
Table
Table 4. Rickettsiales identified by molecular methods in clinically ill patients in Italy.
Table 4. Rickettsiales identified by molecular methods in clinically ill patients in Italy.
SpeciesFeverTacheNoireRashClinical NotesNumber of CasesReference
RickettsiaconoriiYesYesYesMSF, Sepsis, respiratory insufficiency and quadriplegia1[146]
YesYesYesMSF, PCR positive on eschar while negative on whole blood1[147]
YesYes (two)YesMSF, Rhabdomyolysis, acute kidney injury and Encephalitis1[148]
YesYesYesMSF, acute kidney injury and herpetic esophagitis1[149]
YesYesYesMSF, Myocarditis-sepsis induced multi organ failure1[150]
YesYesYesMSF5[151]
YesYesYesMSF, HIV patient1[152]
YesYesYesMSF1[153]
R. conorii subsp. indicaYesYesYesMSF1[154]
R. conorii subsp. israelensisYesNoYesPetechial rash, severe sepsis and multi organ failure1[155]
YesNoYesDysarthria, dysdiadochokinesis, mild neck stiffness, meningism1[155]
YesYesYes 1[156]
R. massiliaeYesYesNoTIBOLA, bite on eyelid, PCR positive on lesion and swab1[157]
YesYesNoTIBOLA; palpable liver, PCR positive on eschar1[158]
YesYesYesMSF1[159]
R. monacensisYesYesNoMSF, PCR positive on tache noir and negative in whole blood1[160]
R. africaeYesYesOnly ipsilateral limbSacral syndrome, traveler from Zimbabwe1[161]
R. slovacaNoNoNoasymptomatic1[92]
YesYesNoTIBOLA, alopecia and painful lymph node1[92]
NoYesNoTIBOLA, myalgia, weariness and painful lymph node1[92]
NoYesNoTIBOLA, itching1[92]
NoYesNoTIBOLA, painful cervical lymph node1[92]
YesYesYesMSF-like1[154]
R.aeschlimanniiYesYesNoHepatitis, PCR positive on liver biopsies1[162]
AnaplasmaphagocytophilumYesNoYesAtypical pneumonia, leukopenia and thrombocytopenia, high liver enzyme1[163]
YesNoYesOral erythema, edema of labium, leukopenia and thrombocytopenia1[163]
YesNoNo6-month illness-misdiagnosis1[164]
YesNoNoMyalgia1[165]
YesNoNoNuchal rigidity and myalgia1[165]
NoNoNoAsymptomatic1[165]
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Guccione, C.; Colomba, C.; Tolomeo, M.; Trizzino, M.; Iaria, C.; Cascio, A. Rickettsiales in Italy. Pathogens 2021, 10, 181. https://doi.org/10.3390/pathogens10020181

AMA Style

Guccione C, Colomba C, Tolomeo M, Trizzino M, Iaria C, Cascio A. Rickettsiales in Italy. Pathogens. 2021; 10(2):181. https://doi.org/10.3390/pathogens10020181

Chicago/Turabian Style

Guccione, Cristoforo, Claudia Colomba, Manlio Tolomeo, Marcello Trizzino, Chiara Iaria, and Antonio Cascio. 2021. "Rickettsiales in Italy" Pathogens 10, no. 2: 181. https://doi.org/10.3390/pathogens10020181

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