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cross-section of the palpebral conjunctiva of a capybara infected with Philophthalmus lachrymosus . Longitudinal section of a parasite with the ventral sucker attached to a papilla (Pp). HE. Bar = 0.5 mm.
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The avian eye trematode Philophthalmus lachrymosus Braun, 1902 is for the first time referred naturally occurring in a non-human mammalian host. Previously, natural infections with P. lachrymosus and other species of Philophthalmus have been occasionally reported from man, with few data on experimental infections of non-human mammals. Results prese...
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... the center of the papillae feeble ves- sels were observed. Frequently, trematodes were found attached to these projections by the ventral sucker; this attachment provoked a remarkable constriction of the papillae ( Figs 5, 6, 7). Caliciform cells, although absent in the areas of cellular proliferation were well observed around these sites. ...
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Citations
... Trematodes of the genus Philophthalmus Looss, 1899 are parasites of the conjunctival sacs of several species of birds and mammals, including human beings [1]. Infection with these eye flukes can cause eye irritation and blepharospasm, conjunctivitis, secondary bacterial infections, and even blindness and the loss of the eye [1][2][3][4][5][6][7][8][9]. Some studies reveal that the pathological changes caused by eye flukes can influence the population dynamics of wild species that act as definitive hosts [7,10]. ...
... The original description by Braun (1902) [26] was based on specimens found in Chroicocephalus maculipennis (= Larus maculipennis) from Brazil. Subsequently, throughout the twentieth century, P. lacrymosus was reported in different host species in the Americas, including other bird species (Ardea alba, Nyctanassa violacea, Sterna hirundo) [27][28][29], humans [30] and capybaras [2,31]. In these reports, the specific epitope has been frequently misspelt as 'lachrymosus', in disagreement with the nomenclatural rules of the International Commission on Zoological Nomenclature (ICZN, Article 32.5.) ...
... Despite that the life cycle of this species is unknown, we consider the find of infected gulls is a strong evidence that P. lacrymosus is a species maintained in the marine environment. Thus, we suggest previous reports of P. lacrymosus in capybaras from Brazil [2,31] be evaluated with reservation, as this aquatic rodent is found in freshwater environments. Sequences here generated for P. lacrymosus may be useful for advancing these complex issues and the overall knowledge about the diversity and biology of species of Philophthalmus found in the New World. ...
Species of the genus Philophthalmus are eye flukes with a complex taxonomy, which began to be improved with the help of molecular data only recently. However, most described species have never been placed into a phylogenetic context. In this study, eye flukes previously found on kelp gulls, Larus dominicanus, from Brazil and identified as Philophthalmus lacrymosus were subjected to molecular analysis.
For the molecular analyses, we analyzed parasites found in six infected gulls (one worm per bird) collected from different municipalities of the state of Santa Catarina, Brazil. We carried out the amplification and sequencing of the partial region of the 28S and cox1 genes and the data obtained were compared with sequences available to philophthalmid species and subjected to phylogenetic analysis.
The isolates of P. lacrymosus from Brazil grouped in well-supported clades with five other species of Philophthalmus with sequences available for comparison. Interspecific divergences of 0.1–1.6% in 28S and 8.2–14.9% in cox1 were found in relation to other isolates of Philophthalmus spp. Two cox1 haplotypes differing in one nucleotide (0.1%) were found between the six eye flukes isolates in gulls from different localities. The Brazilian isolates grouped in a subclade with parasites identified as P. lacrymosus in Portugal; however, the molecular divergences found in cox1 (8.2–8.5%) strongly suggest that these isolates belong to different species. The phylogenetic trees obtained and the intergeneric divergences to species of the genera Cloacitrema and Parorchis did not support the validity of the genus Natterophthalmus, for which P. lacrymosus was proposed as the type species in the past.
As P. lacrymosus was described from Brazil, we recommend that this name be applied to the South American isolates and that the Portuguese isolates be provisionally considered as Philophthalmus sp., a probable cryptic species. Moreover, data obtained supports the previous morphology-based synonymizing between Natterophthalmus and Philophthalmus. Considering our results and most of previous reports of P. lacrymosus in South America, we suggest this species presents a marine life cycle.
... Reports from natural (Mukaratirwa et al. 2005) and experimental (Diaz et al. 2002) infections have demonstrated the potential of trematodes to cause eye illnesses. Philophthalmus gralli is the most common infectious species causing conjunctivitis (Pinto et al. 2005). ...
... In Brazil, only one study has described the occurrence of the parasites as an outbreak in ostriches (Verocai et al. 2009). However, outbreaks with similar clinicopathological features have been described in other domestic and wild waterfowl species, including muskrats and mallard ducks, African geese, moorhens (Assis et al. 2022), ducklings, redfooted ducks (Muniz-Pereira & Amato 1993), and capybaras (Pinto et al. 2005). ...
... The ocular histopathological findings associated with the presence of parasites are essential for the diagnosis (Church et al. 2013). Findings included marked hyperplasia of the bulbar and palpebral conjunctival mucosa; inflammatory infiltrate in the submucosa; and several specimens of Philophthalmus sp. on the surface of the conjunctival mucosa (Pinto et al. 2005). In chronic evolution, ocular tissue is lost and is replaced by fibrous connective tissue (Rojas et al. 2013). ...
This study discusses the epidemiological, clinical, and pathological characteristics of two outbreaks of ocular infection in ostriches (Struthio camelus) caused by the trematode Philophthalmus sp. The outbreaks occurred in the states of Ceará and Rio Grande do Norte in Northeast Brazil. Ostrich farming was categorized as semi-intensive farming with free access to the weir and river. The clinical symptoms for infection included nictitating membrane inflammation, epiphora (tearing), eyelid edema, ocular congestion, eyeball destruction, emaciation, and death, and the infection period ranged from 8 to 16 months. Macroscopically, thickening of the eyelids and conjunctiva were observed, with orange parasites infestation. Histologically, the lesions were characterized as lymphoplasmacytic and heterophilic, multifocal to coalescing, moderate, chronic conjunctivitis associated with hyperplasia and ectasia of the Harderian gland, and numerous parasites. The parasites were oval and flattened with an oral suction cup, acetabulum, and thick cuticle containing spicules. The diagnosis of philophthalmiasis was based on epidemiological, clinical, and pathological findings associated with the morphological characteristics of the parasites present in the conjunctival sacs which were similar to the trematode Philophthalmus sp. Philophthalmiasis can occur in ostriches raised on urban and rural properties in Northeastern Brazil, probably associated with the contact of birds with contaminated water, and is characterized by severe conjunctivitis that can result in the loss of the eyeball and death of the animals.
... Regarding the species closest genetically found in specimens from the Ivaí River, Philophthalmus species also use gastropods belonging to M. tuberculata as the first intermediate host, as does A. chloroticum (Pinto and Melo 2010;Onaca et al. 2019;Pulido-Murillo et al. 2022). Most adult trematodes belonging to Philophthalmidae Looss (1899), are found in the eyes of birds and mammals, and there are reports of parasitism in humans (Freitas 1955;Muniz-Pereira and Amato 1993;Kanev et al. 1993;Nollen and Kanev 1995;Pinto et al. 2005;Verocai et al. 2009;Pinto and Melo 2010). The digenean P. lutzi was recorded using A. chloroticum as an intermediate host in its life cycle, as was the case with gastropods from the Ivaí River (Quintana and Núñez 2014;Onaca et al. 2019). ...
Thiarids are pantropical gastropods distributed from South America to Australia and found in lentic and lotic freshwater environments. These gastropods act as intermediate hosts for several species of digeneans. There are difficulties in the correct identification of these digeneans in certain stages of the life cycle as the larvae have a reduced size and few morphological characteristics for diagnosis. Because of this, techniques based on molecular markers have become an extremely useful tool. Our objective was to molecularly characterize the digeneans found in gastropods from the Ivaí River, Paraná, Brazil, using the mitochondrial molecular marker cytochrome c oxidase (COI) and the 28S ribosomal marker. With the molecular marker COI, gastropods showed high genetic similarity with Aylacostoma chloroticum. For the parasites, four different taxa were characterized with both markers. The 28S ribosomal marker proved to be more effective for the identification of Ivaí River parasites, being possible to suggest the identification of two species among the four groups found. Considering that there are no records in the literature of studies involving parasites and gastropods as intermediate hosts in the Ivaí River, this study is the first regarding these relationships.
... In the present study, ophthalmic findings are described in free living, wild-caught individuals. Philophthalmus lachrymosus may cause severe ocular lesions, including deep corneal ulcers, even blindness and loss of the globe [11,14,28]. Ocular surface lesions observed in our study were most likely due to the attachment of the ventral suckers of the eye fluke [7,26]. ...
... The most frequent ocular clinical sign observed was conjunctival hyperemia (85%), similar to what has been previously described in other works with Philophthalmus spp. [7,28,29]. Subjectively the severity of hyperemia appears to correspond with the number of parasites found in each eye. It was not possible to determine if the corneal ulcers present in one case were primary or secondary, although it was thought to be due to self-inflicted trauma secondary to the conjunctivitis and the presence of parasites. ...
... It was not possible to determine if the corneal ulcers present in one case were primary or secondary, although it was thought to be due to self-inflicted trauma secondary to the conjunctivitis and the presence of parasites. Overall, the clinical features described in the present study were supportive of previous studies [7,14,19,22,23,[27][28][29]. ...
In this study, clinical, parasitological and histopathological findings of thirteen kelp gulls (Larus dominicanus) found infected with eyeflukes in Brazil are presented. Parasites detected in the ventral conjunctival fornix were identified as Philophthalmus lachrymosus [mean intensity of infection: 16 (5–36) worms/bird]. Eleven birds (85%) presented signs of systemic disease, such as emaciation, dehydration and depressed consciousness. Conjunctival hyperemia was observed in 22 eyes (85%). Keratitis, corneal ulcers, corneal abscess and chemosis were also detected in some eyes (4–8%). Histopathologic lesions, likely due to the parasite attachment to the conjunctiva, were found in the eyes of one infected bird that died from unrelated causes. Philophthalmosis by P. lachrymosus is here reported as a clinically relevant eye disease in kelp gulls.
... Also, has been found Venezuela (Diaz et al., 2002), Brazil (Verocai et al., 2009) and in Zimbabwe (Mukaratirwa et al., 2005) (Nadar et al., 2017). It is usually minimally pathogenic in natural hosts; heavy burdens and/or infections inaberrant hosts may be associated with conjunctivitis, epiphora, hemorrhage, and itching/swelling of the eyelids (Pinto et al., 2005 andHeneberg et al., 2018). Despite the increasing number of cases reported in birds and human, studies related to the diagnosis of subclinical philophthalmosis are lacking, and there are no effective therapeutic regimens available (Assis et al., 2018). ...
... Most Philophthalmus species utilize freshwater snails, but a few species infect marine snails, including Philophthalmus andersoni, Philophthalmus larsoni, and Philophthalmus hegeneri (Penner and Fried, 1963;Penner and Trimble, 1970;Nollen and Kanev, 1995;Abdul-Salam et al., 2004). Although a variety of wild and domestic bird species can serve as definitive hosts for Philophthalmus (Nollen and Kanev, 1995), rarer infections have been detected in mammals such as capybara (Hydrochaeris hydrochaeris; Pinto et al., 2005;Souza et al., 2015), Galapagos sea lions (Zalophus wollebaeki; Meise and Garcia-Parra, 2015), and humans (Table I), though this paucity of human cases may be due to misdiagnoses (Amin et al., 2019). ...
... In contrast, several Philophthalmus species have been detected across continents. For example, Philophthalmus lacrymosus was first described in Serbia (Ching, 1961), and more recently this species has been reported in Brazil in capybara (Hydrochaeris hydrochaeris; Nollen and Kanev, 1995;Pinto et al., 2005;Souza et al., 2015), along with a recent outbreak in gulls (Larus fuscus, Larus michahellis) in Spain (Heneberg et al., 2018). Philophthalmus hegeneri, like P. lacrymosus, also appears to have a distribution across new and old worlds. ...
... Fagotia acicularis and M. praemorsa both yielded successful infections, whereas infection of M. tuberculata with P. lucipetus was unsuccessful (Nollen and Kanev, 1995). Furthermore, M. tuberculata is known to yield successful infections with P. gralli through experimental evidence (Nollen and Kanev, 1995;Mukaratirwa et al., 2005;Pinto et al., 2005) and P. gralli is the only Philophthalmus species that has been recovered from natural philophthalmid eye-fluke infections described in M. tuberculata and T. granifera (Table III). ...
Philophthalmus is a genus of globally distributed parasitic eye flukes with some members of the genus found in disparate locales. In particular, Philophthalmus gralli, a zoonotic trematode, appears to be a relatively new introduction to the Americas, facilitated by spillover from the invasive snails Melanoides tuberculata (red-rimmed melania) and Tarebia granifera (quilted melania), which were introduced via the aquarium trade, and perhaps furthered by avian dispersal. Given that two known intermediate hosts of Philophthalmus flukes are actively expanding their range as a result of human activities, we hypothesize that this spread is also associated with the spread of Philophthalmus flukes. To address this, we systematically reviewed the literature and examined whether the global expansion of P. gralli flukes is associated with the spread of invasive snails M. tuberculata and T. granifera. Here, we show that (1) specimens of P. gralli are only found in intermediate snail hosts M. tuberculata or T. granifera, suggesting intermediate host specificity for these 2 species, and (2) specimens of P. gralli have rarely been found outside the ranges (native and introduced) of M. tuberculata or T. granifera. Given the importance of distribution information of parasites in the role of identifying parasite invasions, we also review the known distribution of all Philophthalmus species. Considering recent outbreaks in humans and wild and domestic animal species, the continued spread of Philophthalmus presents a potential threat to veterinary and public health and conservation.
... Philophthalmus spp are small trematodes that mostly parasitize conjunctival and orbital tissues of their typical avian hosts. Commonly associated with waterbirds and wading birds, occasional infections in other birds, and rare infections in nonavian species have been identified [1][2][3][4]. Transmission to birds occurs via ingestion of encysted metacercariae on substrates (vegetation, crustacean shells, etc) or direct ocular contact with cercariae or metacercariae in water [2]. It is usually minimally pathogenic in natural hosts; heavy burdens and/or infections in aberrant hosts may be associated with conjunctivitis, epiphora, subconjunctival hemorrhage, and itching/swelling of the eyelids [4][5][6][7]. ...
... Transmission to birds occurs via ingestion of encysted metacercariae on substrates (vegetation, crustacean shells, etc) or direct ocular contact with cercariae or metacercariae in water [2]. It is usually minimally pathogenic in natural hosts; heavy burdens and/or infections in aberrant hosts may be associated with conjunctivitis, epiphora, subconjunctival hemorrhage, and itching/swelling of the eyelids [4][5][6][7]. ...
... Several freshwater and marine Philophthalmus spp occur in the Americas [3]; in the United States and Mexico, P gralli, Philophthalmus megalurus, Philophthalmus hegeneri, Philophthalmus larsoni, Philophthalmus andersoni, and P lacrymosus have been reported [1,3,12,13]. Philophthalmus lacrymosus has previously been detected in natural mammalian infections in the Americas, including 1 human case from western Mexico (spelled P lacrimosus) and a capybara (Hydrochaeris hydrochaeris) in Brazil [4,11]. Although generic diagnosis of Philophthalmus is straightforward given the salient characteristics of the group (eg, conjunctival location, large OS and VS, large pharynx, tandem testes, eyespot-bearing miracidia in ovo) [1], specific diagnosis is often challenging, particularly in clinical settings. ...
A trematode identified as a Philophthalmus sp was extracted from the bulbar conjunctiva of a patient in southern Texas with short-distance travel to Mexico. This parasite is very rarely reported from humans, and species identification is challenging. Aspects of diagnosis, zoonotic transmission, and unresolved questions about Philophthalmus spp are discussed.
... Philophthalmus spp are small trematodes that mostly parasitize conjunctival and orbital tissues of their typical avian hosts. Commonly associated with waterbirds and wading birds, occasional infections in other birds, and rare infections in nonavian species have been identified [1][2][3][4]. Transmission to birds occurs via ingestion of encysted metacercariae on substrates (vegetation, crustacean shells, etc) or direct ocular contact with cercariae or metacercariae in water [2]. It is usually minimally pathogenic in natural hosts; heavy burdens and/or infections in aberrant hosts may be associated with conjunctivitis, epiphora, subconjunctival hemorrhage, and itching/swelling of the eyelids [4][5][6][7]. ...
... Transmission to birds occurs via ingestion of encysted metacercariae on substrates (vegetation, crustacean shells, etc) or direct ocular contact with cercariae or metacercariae in water [2]. It is usually minimally pathogenic in natural hosts; heavy burdens and/or infections in aberrant hosts may be associated with conjunctivitis, epiphora, subconjunctival hemorrhage, and itching/swelling of the eyelids [4][5][6][7]. ...
... Several freshwater and marine Philophthalmus spp occur in the Americas [3]; in the United States and Mexico, P gralli, Philophthalmus megalurus, Philophthalmus hegeneri, Philophthalmus larsoni, Philophthalmus andersoni, and P lacrymosus have been reported [1,3,12,13]. Philophthalmus lacrymosus has previously been detected in natural mammalian infections in the Americas, including 1 human case from western Mexico (spelled P lacrimosus) and a capybara (Hydrochaeris hydrochaeris) in Brazil [4,11]. Although generic diagnosis of Philophthalmus is straightforward given the salient characteristics of the group (eg, conjunctival location, large OS and VS, large pharynx, tandem testes, eyespot-bearing miracidia in ovo) [1], specific diagnosis is often challenging, particularly in clinical settings. ...
A trematode identified as a Philophthalmus sp. was extracted from the bulbar conjunctiva of a patient in southern Texas with short-distance travel to Mexico. This parasite is very rarely reported from humans, and species identification is challenging. Aspects of diagnosis, zoonotic transmission, and unresolved questions about Philophthalmus spp. are discussed.
... This parasite genus is associated with ophthalmic disease in avian and mammalian species and typically uti- lizes an invertebrate intermediate host. 1,9,15,21,23 In the islet of Caamã no on Santa Cruz Island, Galapagos sea lions ages 4-8 mo had the highest probability of infection with P. zalophi, and clinical signs included mild to severe blepharitis, conjunc- tivitis, and keratitis with purulent discharge. 16 Peaks of infection were associated with months of high sea surface temperature. ...
... Over 40 different species of Philophthalmus are reported, affecting both avian and mammalian hosts in North and South America. 15,20,22,23 The life cycle typically involves an invertebrate interme- diate host, such as an aquatic or terrestrial snail. Many species of marine gastropods are found in the Galapagos archipelago, and this includes known intermediate hosts of Philophthalmus sp. ...
The Galapagos sea lion (Zalophus wollebaeki) is an otariid species endemic to the Galapagos archipelago and is currently listed as endangered. The ocular trematode Philophthalmus zalophi was recently reported to affect the survival of juvenile Galapagos sea lions on Santa Cruz Island, resulting in marked ophthalmic changes. This study evaluated the ophthalmic disease and histopathologic effects of P. zalophi on juvenile Galapagos sea lions in the largest rookery located on San Cristóbal Island. Twenty juvenile Galapagos sea lions (10 male and 10 female) were evaluated among five sites in the rookery El Malecón. Ophthalmic examination, including fluorescein staining and evaluation of the adnexa, cornea, and sclera, were performed on each eye. The presence, number, and location of ocular parasites were determined, and parasites were collected for identification. Conjunctival biopsy was performed on 11 animals: 2 that lacked parasites and gross lesions and 9 with both parasites and gross lesions. All parasites collected were confirmed as P. zalophi and identified in 80% (16/20) of the study animals and 70% (28/40) of the examined eyes. Philophthalmus zalophi was most frequently found attached to the nictitating membrane but also located on the palpebral conjunctiva or cornea. The most common clinical signs were varying degrees of conjunctival hyperemia (28/40 eyes), most frequently of the nictitating membrane and mucoid ocular discharge (12/40 eyes). The number of parasites was significantly associated with the degree of conjunctival hyperemia (P < 0.001). Histopathology of conjunctival biopsies revealed organized lymphoid follicles and lymphoplasmacytic infiltrates. The histopathologic changes and gross lesions were likely due to the parasite's attachment to the conjunctiva. This study provides additional details of P. zalophi infection in juvenile Galapagos sea lions. Further research is warranted to detail the life cycle of this parasite, transmission to sea lions, and potential treatment protocols.
... The pharynx length that represented from 104% to 125% of oral sucker length ( Table 3), and the short follicular vitellarium were consistent with the diagnosis of P. lacrymosus [28]. However, the cirrus pouch length was highly variable and was in agreement with previous descriptions (extending to post-acetabular zone [28,29]) in only some of the individuals, whereas in the others, it reached only a posterior half of ventral sucker. The latter individuals were likely subadults as they did not have eggs. ...
... Measurement This study Sonin [28] Kanev et al. [5] Shakarbayev et al. [37] Literák et al. [1] This study Sonin [28] Pinto et al. [29] Body size 3003-5710 (4899) × 626-2029 The newly provided measurements are based on 17 (P. lucipetus) and 6 individuals (P. ...
... Note that some measurements are inconsistent across the cohorts compared in Table 3; particularly the egg size displays huge variability between (but not within) the hitherto performed studies. The individuals of P. lacrymosus originated from highly infected birds, and were smaller than previously reported, showing longer testes, ovary and eggs [29]. Note that the previously reported Peruvian P. lucipetus [1] was later reclassified as P. gralli (for a more detailed discussion on reasons for this reclassification, cf. ...
Trematodes of the genus Philophthalmus Loos, 1899 are the eye parasites of birds and mammals, which use freshwater snails as their first intermediate hosts. Here we examined the presence of philophthalmids in a total of 1515 gulls (589 Larus fuscus and 926 Larus michahellis) admitted between January 2010 and October 2016 for rehabilitation at Olhão (Portugal), by the use of combined morphological and molecular analysis. We recorded the first infected L. fuscus and L. michahellis in July and November 2015, respectively. The philophthalmids were located in the conjunctival sac or under the nictitating membrane. Gulls infected with Philophthalmus lucipetus Rudolphi, 1819 presented no clinical signs, while those infected with Philophthalmus lacrymosus Braun, 1902 presented serious eye damage in the same host species. The prevalence of P. lucipetus reached 3.6% in L. fuscus and 0.8% in L. michahellis; the prevalence of P. lacrymosus reached 0.3% and 0.0%, respectively. The outbreak of P. lucipetus likely started in a narrowly defined area, since the first six cases, found between July and October 2015, originated from a single municipality, and only later more cases started to be retrieved from other municipalities of Portugal. These findings represent the first record of both philophthalmids in the Iberian Peninsula, their first record in L. michahellis and the first record of P. lacrymosus in L. fuscus. Further follow-up of the outbreak, and the identification of intermediate hosts are needed.
