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Dipylidium caninum in the twenty-first century: epidemiological studies and reported cases in companion animals and humans

Abstract

Background

Dipilidiosis is a parasitic disease caused by the tapeworm Dipylidium caninum. Fleas and, less frequently, lice act as an intermediate host, and their ingestion is required for infection to occur. While the disease mainly affects domestic and wild carnivores, it is also considered a zoonotic disease, with most human cases reported in children. Dipylidium caninum is considered to be the most common tapeworm infesting companion animals, but dipilidosis in humans is rare. The aims of this review were to improve current understanding of the epidemiology of this parasitosis and its management by the medical and veterinary community.

Methods

A comprehensive review of the published literature during the last 21 years (2000–2021) on the epidemiology, clinical features, diagnosis, treatment and prevention measures of D. caninum infection and dipilidiosis in companion animals and humans was conducted.

Results

Using predefined eligibility criteria for a search of the published literature, we retrieved and screened 280 publications. Of these, 161 (141 epidemiological studies, 20 case reports [16 human cases]) were considered for inclusion in this review. This parasitosis is present worldwide; however, despite being the most frequent cestode infection in animals, it is often underdiagnosed using common coprological techniques. Its diagnosis in humans has also proved challenging, being frequently confused with pinworm infection, leading to inappropriate treatment and to the persistence of the disease over time. Prevention measures include control of ectoparasites in animals and the environment, as well as regular deworming of animals, most commonly with praziquantel.

Conclusions

The diagnosis of dipilidiosis remains challenging in both animals and humans, primarily due to the low sensitivity of the diagnostic methods currently available and a lack of knowledge of the morphological characteristics of the parasite. Although treatment with the appropriate anti-cestode compounds is well tolerated and results in resolution of the infection, indiscriminate use of these compounds may predispose to an increase in resistance. Given the worldwide distribution of this parasite, it is essential to act on several fronts, with a focus on health education for children and animal owners and the control of intermediate hosts, both in animals and in the surrounding environment.

Graphical Abstract

Background

Dipilidiosis is an underrated disease caused by the cestode Dipylidium caninum. The transmission of this parasite is complex as it involves an intermediate invertebrate host (flea or louse), which subsequently needs to be ingested by the definitive hosts, normally carnivores, but occasionally humans, for the infection to develop [1, 2]. In both cases, the infection is asymptomatic or the clinical signs or symptoms are non-specific and, consequently, proper diagnosis, treatment and prevention are challenging.

Climate change, coupled with increased urbanisation and the increased number of pets, both those with close relationships with their owners and also of sheltered or stray animals, may affect the prevalence and endemicity of the intermediate hosts [3,4,5]. If there is no effective ectoparasite control, the prevalence of pathogens they transmit, such as D. caninum, may also increase. This fact underlines the importance of raising awareness among the medical community, and the population in general, of the need for greater clinical suspicion of this cestode, as well as of the appropriate methods of diagnosis, treatment and prevention.

The aim of the present study was to summarise and analyse the epidemiology, pathogenesis, diagnosis and control measures of D. caninum infection and dipilidiosis in companion animals and humans, through a comprehensive review of the literature in the last 21 years (2000–2021), in order to raise awareness of the medical and veterinary community on the challenges associated with the management of this parasitosis.

Search strategy, eligibility, and review

An online search was conducted of the MEDLINE® database on 10 November 2021 using the PubMed® (https://pubmed.ncbi.nlm.nih.gov/) search tool. The following search terms were used: ("Dipylidium" [MeSH Terms] OR "Dipylidium" [All Fields] OR “Dipilidi*” [MeSH Terms] OR “Dipilidi*” [All Fields]) AND ("dogs" [MeSH Terms] OR "dogs" [All Fields] OR "dog" [All Fields] OR "cani*" [All Fields] OR "cani*" [MeSH Terms] OR "cats" [MeSH Terms] OR "cats" [All Fields] OR "cat" [All Fields] OR "feli*" [All Fields] OR "feli*" [MeSH Terms] OR "human*" [MeSH Terms] OR "human*" [All Fields] OR "child*" [MeSH Terms] OR "child*" [All Fields] OR "people" [All Fields]). The search results were then filtered for the period 2000 to the present (10 November 2021) and extracted into a database in Microsoft Excel® (Microsoft Corp., Redmond, WA, USA) under a comma-separated-value (CSV) format.

All records were screened according to the title and abstract, if available. Two types of research were included: (i) epidemiological studies of D. caninum in dogs, cats, humans, fleas, lice and soil or food contamination studies; (ii) reported cases of dipilidiosis in dogs, cats and humans. Rejection criteria were: (i) studies of other parasites, i.e. not including D. caninum, or studies of D. caninum but in animal species other than dog or cat (e.g. wild hosts); (ii) review articles, guidelines, meta-analyses, historical studies and requests; (iii) unavailable articles or written in languages other than English, Spanish and Portuguese; (iv) duplicate studies; and (v) experimental studies. The study selection process is shown in Fig. 1.

Fig. 1
figure 1

Schematic overview of the screening and selection process of the studies included in this review

When coprological methods were mentioned in the articles included in this review (Additional file 1: Table S1; Additional file 1: Table S2), we refer to them in a generic manner as one or more of the following: faecal smear, flotation and sedimentation. The reason for this is that different solutions, concentrations and protocols were used by the authors of the various studies, and the inclusion of such details would have made the overview of Tables S1 and S2 difficult.

Parasite characteristics

Aetiology and life-cycle

The helminth D. caninum is a cestode belonging to the order Cyclophyllidea and family Dipylidiidae. The biological cycle of this parasite is heteroxenous, occurring in the definitive host (carnivores and occasionally in humans) and intermediate host (fleas [Ctenocephalides spp. and Pulex irritans] and chewing lice [Trichodectes canis and Felicola subrostratus]) [6,7,8,9]. Carnivores, both domestic (dog [Canis lupus familiaris] and cat [Felis catus]) and wild, are the typical definitive hosts. In the latter, the parasite has been identified in several sylvatic species, namely foxes, wolves, jackals, hyaenas, coyotes, racoon dogs and cheetahs [10,11,12]. Transmission of and infestation by this parasite in both directions (wild to domestic and domestic to wild) is possible due to shared habitats, particularly at night, when wild animals come close to human populations in their forage for food [11, 12].

The infective larval form corresponds to a cysticercoid, which develops in the body cavity of the intermediate host [13]. The definitive host becomes infected through the ingestion of an infected flea or louse. In the small intestine of the mammalian host, the cysticercoid larva is digested and becomes fixed to intestinal wall by the scolex, initiating the adult developmental process. Wthin 2–3 weeks (prepatent period), the ovigerous proglottids detach from the strobilus and pass into the faeces [1, 2, 6, 13]. When the proglottids disintegrate, the larval stages of the intermediate hosts ingest the ovigerous capsules. The hexacanth embryos hatch and develop into cysticercoids in parallel with the invertebrate development [2, 6, 14].

Morphology

Similar to other cestodes, D. caninum consists of a chain (strobilus) of segments (proglottids) that are independent of each other, with maturation progressing along the chain. Macroscopically, the adult parasite is a whitish flat worm ranging in length from 10 to 70 cm. The scolex is the narrower part of the parasite (diameter: < 0.5 mm) and is responsible for fixation of the parasite to the intestinal wall [1, 2, 6]. This attachment is possible due to its protruding and retractable rostellum, which bears three to four rows of hooks in the shape of a thorn, as well as four suckers [1, 2, 6, 13]. As the parasite matures, the proglottids become larger (size: 12 × 3 mm) and have mature genital organs. The seed-shaped ovigerous proglottids are loaded with eggs and ready to detach from the strobilus [6]. The eggs contain the first larval stage, also known as hexacanth embryo, and are grouped in thin-shelled capsules (size: 200 × 400 µm), with each containing five to 30 eggs (size: 40 × 50 µm [2, 6, 13, 15]. This tapeworm differs from other cestodes by having double genital pores, located slightly behind the middle of the lateral margins of each proglottid, and typical ovigerous capsules [2, 6, 13].

Due to the shape of the adult D. caninum and its biological characteristics, it is also known as the flea tapeworm, cucumber tapeworm and/or double-pored tapeworm [6].

Epidemiology, prevalence, and distribution

Dipylidium caninum is distributed worldwide, occurring on all continents (with the exception of Antarctica) and detected either in vertebrates, including humans, and insects, namely fleas and lice [7, 16,17,18,19,20,21] (Fig. 2; Addotopma;file: Table S1). Several studies have shown soil contamination with this cestode (0.1–26.3%) [22,23,24,25,26,27,28,29,30,31], as well as food contamination (1.7%) [32]. The wide geographical distribution of this parasite is unsurprising, as invertebrate intermediate hosts are also found throughout the world, with fleas being the most frequent ectoparasite of dogs and cats [5, 21, 33]. The studies included in the present review were conducted in 50 countries, with most studies being from European (44/161, 27%), Asian (42/161, 26%) and North (27/161, 17%) and South (27/161, 17%) American countries (Fig. 2; Additional File 1: Table S1).

Fig. 2
figure 2

Global distribution of Dipylidium caninum between 2000 and 2021

Dogs and cats

Two distinct genotypes of D. caninum were have been identified in dogs and cats, suggesting the presence of two distinct species [34, 35]. In Spain, another species of the same genus, Dipylidium carracidoi, was also reported in necropsied cats, with a higher percentage of infection (32.8%) than reported for D. caninum (3%) [36]. According to the authors of this latter study, D. carracidoi is a relatively unknown species and there are very few reports on it; it seems to occur in this Spain and its life-cycle might be the same as that of D. caninum [36]. As the authors refer to the existence of morphological differences that allow the two species to be distinguished, it is possible that in some studies classification was incorrect, and that D. carracidoi was misidentified as D. caninum, and vice-versa [36].

The risk of D. caninum infection may vary depending on the vertebrate species and its lifestyle. Stray and shelter animals are less likely to have access to veterinary care and thus have a higher risk of infection [37,38,39,40]. Dogs and cats that are parasitised with fleas or lice have an increased risk of D. caninum infection [37]. Beugnet et al. [41] reported that in their study dogs had a higher percentage of fleas infected with the parasite. Regarding cats, their more pronounced grooming behaviour could lead to a higher flea intake compared to dogs and, consequently, a higher risk of D. caninum infection [41]. However, cats have been reported to show lower rates of D. caninum parasitism [16].

Few studies have assessed D. caninum prevalence according to the age of the animal, and the results of these studies are discordant. Some studies report a higher prevalence of the disease in young individuals [39, 42,43,44], which might be related with a protective immunity in older individuals [10], and others report higher prevalence with increasing age of the animals [1, 17, 45,46,47,48,49,50], which suggests a lack of post-infection protection [49]. Prevalence has also been reported to be associated with the animal's body temperature [14, 50]. Younger animals may have more difficulty in maintaining their body temperature, which impairs the development of cysticercoids inside the fleas [14, 50]. It has been suggested that differences in prevalence between sexes are more related to the social characteristics of the animals than to the sex itself [1, 17, 50, 51], as increased contact with other animals might be a risk factor for D. caninum infection [1, 51, 52].

Higher prevalence in rural or suburban areas (1.3–13.1%), compared to urban areas (0.7–5.7%), may be related to environmental conditions and a lower control of ecto- and endoparasites due to poorer veterinary care hampered by a greater distance to veterinary clinics/hospitals [53,54,55,56,57].

Humans

Although humans are accidental hosts, children seem to be the most vulnerable to infection with D. caninum [21, 58] (Additional file 1: Table S2). This increased vulnerability of children is probably related to their close contact with animals, not only domestic animals but also stray animals and those without any veterinary care, as well as their poor hygiene habits, such as infrequent hand washing and playing and eating on the floor.

Adults may also become infected, with factors such as an immunosuppressive condition, bad hygiene habits and contact with animals without veterinary care being contributing factors [21, 59,60,61]. Contact with animals, either household animals or those outside the home, is considered a risk factor for infection [21, 62,63,64]. However, when there is no contact with animals, other means of transmission cannot be discarded, including the role of other ectoparasite vectors, such as the human flea (P. irritans) [9]; in addition, consideration must be given to immunosuppressive conditions or poor hygiene, both of which may facilitate infection [13, 59, 65]. The presence of proglottids or ovigerous capsules in soil or food [25, 28, 32, 58], as well as co-habitation with other infected people or companion animals [60], only represents an indirect risk of infection as the life-cycle of D. caninum is heteroxenous, and the infective cysticercoid larvae are only present in the intermediate host [2, 6].

Clinical presentation

Dogs and cats

The infection in dogs and cats is generally asymptomatic, even proglottids can be observed in the faeces [66,67,68]. However, a number of clinical signs are commonly associated with this parasitosis, such as anal pruritus, recognisable by scratching of the perineal region against a wall, as the ovigerous proglottids force/pass through the anal folds [67, 68]. This scratching behaviour is commonly known as scooting behaviour [67]. Other clinical signs that have been described include diarrhoea [67, 69], anorexia, weight loss [68, 69], dullness and poor hair coat [67]. Of note: there are often co-infections (Additional file 1: Table S1; Additional file 1: Table S2) with other gastrointestinal parasites, which may interfere with an understanding the true aetiology of the clinical signs [66, 69]. These co-infections may be particularly relevant not only for the clinical condition and synergic effects, which might lead to death [66, 69], but also due to their zoonotic potential, such as infections with Ancylostoma spp., Toxocara spp. and Echinococcus spp. [43, 48, 49, 51, 52, 57, 70,71,72,73,74,75,76,77,78,79,80,81,82,83,84].

Humans

In humans, as in animals, infection with D. caninum can be asymptomatic [21, 58, 65, 85, 86], or non-specific symptoms may be observed, such as abdominal pain and discomfort [58, 59, 61, 62, 64, 87,88,89], bloating [64, 90], diarrhoea [17, 58, 59, 64, 90, 91], difficulty in defecation [60], anal itching [62,63,64, 92] that may lead to scratching of the perianal area and the development of abrasions and dermatitis [92], loss of appetite and less weight gain [58, 87] and occasional vomiting [17, 61] and fever [90]. Sleep disturbances, sadness, hyperactivity and irritability are also described [87, 88, 90, 92]. A few studies have reported haematological changes, namely leucocytosis [58], eosinophilia [58, 88], low haematocrit and/or haemoglobin [61, 64, 91], thrombocytopaenia, an increased erythrocyte sedimentation rate [61] and higher level of serum IgE [91]. It is also hypothesised that in humans it may be a self-limiting disease, with spontaneous cure [60]. In most of the clinical cases (Additional file 1: Table S2), proglottids were observed in the stool or perianal region, and described as grains of rice or as cucumber or other vegetable seeds, appearing individually or forming a chain [6, 21, 58, 60, 61, 63,64,65, 85,86,87,88,89, 91, 92]. In some cases, worm mobility was observed [65, 89, 92].

The detection of proglottids in the stool is one of the most frequent findings in infants and children due to caregivers observing the stool and the perianal region of children, particularly during diaper changes or bathing [60, 87, 89]. Since adults do not normally inspect their own stool, or at least not as often as they do their own children’s stool, more infections may go undetected in adults [59,60,61]. The lower prevalence of disease in adults is also likely to be related to their stronger immune system and fewer risk behaviours for acquiring the infection [58].

Diagnosis

Traditional diagnosis is based on coprological methods, which are techniques that allow for the macroscopic and microscopic observation of parasites in the faeces. These methods are simple and inexpensive and can be performed in the setting of the veterinary surgery [15]. For the diagnosis of D. caninum, the coprological techniques performed are qualitative, such as faecal smear, flotation and sedimentation. The former, although fast, has the disadvantage of being not sensitive since the amount of stool analysed is very small and there is a lot of debris [15]. Flotation and sedimentation can be performed with different types of solutions and with or without a centrifugation step, ultimately the aim is to concentrate the parasitic elements present in a faecal sample to be observed under a microscope. With these techniques, diagnosis is based on the observation of ovigerous capsules, with five to 30 eggs [2]. Táparo et al. [93] evaluated the efficacy of different coprological methods for detecting the parasitic forms and found that sedimentation was the most efficient technique compared to faecal smear and flotation techniques. Possible explanations for these differences may be related to a higher specific gravity and the easy crystallisation of flotation solutions, leading to egg disintegration [94], as well as to the inability of egg capsules to float sufficiently due to their weight [6]. An additional disadvantage of coprology is that if the ovigerous capsule breaks, the eggs are indistinguishable from other taeniid eggs, possibly leading to an underestimation of D. caninum prevalence [15, 29].

In terms of other cestodes, quantitative techniques are of no value since the number of eggs found cannot be related to the number of adult parasites in the intestine and the excretion of proglottids occurs intermittently [13, 15, 95].

However, for the reasons described above, these traditional diagnostic methods generally present low sensitivity for D. caninum, which not only compromises diagnosis of the parasitosis but also leads to an underestimation of the real prevalence of the disease, as shown in the various epidemiological studies using these techniques [4, 43, 95, 96]. Studies based on coprological methods have obtained a prevalence ranging between zero and 39.1% [48, 97,98,99,100,101], whereas in necropsy-based studies the prevalence ranged between 0.9 and 83.3% [20, 102]. During necropsies, a more detailed analysis is performed, making this method more sensitive and reliable when compared with coprological techniques, as the adult parasites are observed in the small intestine of the animals [19, 29, 49, 77, 78, 82, 94, 103,104,105,106,107,108,109,110]. Therefore, epidemiological studies on animals based on necropsies will provide a more realistic insight into the prevalence of this cestode in the general population [94, 111,112,113,114]. In live animals, epidemiological studies are equally relevant, and to compensate for the lack of sensitivity of coprological methods, one or more of the following approaches can be adopted: increase sample size, apply molecular diagnostic methods and repeat the sampling of the same individuals over time [110]. In an individual diagnosis, and to increase the chances of finding proglottids or ovigerous capsules, the collection of fresh faeces for the coprological examination should preferably be done on 3 consecutive days, both in humans and other animals [37, 58, 94].

A detailed observation of the anal/perianal region and of faeces and/or gastrointestinal contents (during necropsies) is valuable for the detection of isolated proglottids or the strobilus of the cestode. After such samples have been recovered, the parasite can be identified by using appropriate stains (acid carmine) and further observation under the microscope or stereomicroscope [20, 81, 109, 115]. The typical features of D. caninum that will support the diagnosis include the presence of two sets of reproductive organs and double genital pores in the middle of each lateral edge, and, in ovigerous proglottids, the presence of ovigerous capsules [2, 6, 37, 65, 88].

Applying adhesive tape to the anal and perianal regions and subsequently observing what is attached to the tape under a microscope may be another diagnostic method. This procedure is extremely easy and inexpensive, but it should not be used exclusively, but rather as a complementary method to other methods, as its efficacy is debatable [52, 94, 101]. When performed during animal necropsies, if the perianal area is contaminated with fluid from the anal sacs, the eggs will not adhere properly to the adhesive [101].

More recently, molecular methods have been used for species identification of taeniid eggs [116], detection of cestode infection [10, 117] and in genetic studies of Dipylidium spp. [34, 35]. Zhu et al. [117] reported the simultaneous detection of Taenia sp. and D. caninum from dog faecal samples and adult parasites by a multiplex PCR assay using mitochondrial genes as molecular markers. The method stands out for its ability to discriminate and diagnose the different cestodes simultaneously, and in a single reaction, which makes the diagnosis faster and more sensitive. The sensitivity of this method may be increased if, before DNA extraction, the eggs are concentrated using a flotation or sedimentation technique [117].

In the studies included in this review, molecular methods were used for the detection of D. caninum in the intermediate hosts: fleas and lice [3, 7, 41] (Additional file 1: Table S1). Detection of the parasite’s genetic material in the invertebrate host represents only a potential infection, as it must be ingested by the vertebrate host [3]. However, this study emphasises the need to combine regular flea and lice control measures with tapeworm control measures [41]. Molecular approaches can also be used to identify potential new intermediate hosts capable of becoming infected and/or transmitting this tapeworm [3].

The presence of antibodies against D. caninum in serum can also be assessed by indirect haemagglutination (sensitivity of 73% and specificity of 90%) [1] or by specific enzyme-linked immunosorbent assays (sensitivity ranging from 50% to 100% and specificity ranging from 75% to 100%) [118]. The results of these tests indicate past and/or present infection, can guide diagnosis and treatment and can indicate the need for prevention [1]. However, the existence of cross-reactions, such as with Ancylostomatidae specimens, cannot be ruled out [118].

The anamnesis and a detailed clinical history can also be crucial to reaching the diagnosis of the disease. In animals, the presence of fleas or lice, and the infrequency of internal and external deworming, associated with clinical signs, may lead to the suspicion of D. caninum infection [67, 68, 80, 119, 120]. The presence of fleas or lice can be interpreted as a sign that sustains the infection by D. caninum since this parasitosis presupposes infestation by ectoparasites containing cysticercoid larvae [77, 80, 105, 108, 121]. However, the animal may no longer have fleas or lice, or the fleas or lice may not be detected at clinical examination [108, 121]. Also, the animal may have acquired the infection by contact with prey that were infested by infected arthropods [121].

As mentioned above, the clinical diagnosis of dipilidiosis can be challenging as the disease has a subclinical expression or the clinical signs and symptoms are predominantly non-specific, both of which preclude a diagnosis based on them [95]. Although the observation/report of rice-like worms in the faeces or in the anal, perianal, and tail regions (animals [81]) or in the stool, underwear, diapers and bath water (in humans) may be quite relevant, the intermittent elimination of proglottids and misdiagnosis, especially in humans [61, 87], often means that laboratory techniques are required to confirm the diagnosis.

In humans, contact with domestic or stray animals, frequent playing on the street or in playgrounds (especially children), immunosuppressive conditions and signs indicative of poor hygiene can also support the diagnosis [21, 59, 62,63,64,65, 122].

Proglottids have a physical resemblance to rice grains when dried, and to cucumber, pumpkin or watermelon seeds when humid; this may result in the proglottids being mistaken for vegetable matter, undigested food, maggots or fly larvae [6, 21, 65, 86, 88]. However, in humans, the most common misdiagnosis is that of the oxyurid nematode Enterobius vermicularis (pinworm), which causes symptoms identical to those caused by D. caninum and whose macroscopic appearance resembles that of D. caninum proglottids [21, 85, 88, 89, 92]. It is therefore important to distinguish between these two parasites, as different therapeutic options and prevention measures are required. Despite both moving actively up to the anus, they differ slightly in size (ovigerous proglottids of D. caninum: 2–3 mm; E. vermicularis specimens: 0.3–0.5 mm), and D. caninum ovigerous proglottids make an expanding and contracting movement along their length and have a flattened dorso-ventrally barrel shape compared to E. vermicularis that moves like a serpent and has a cylindrical shape [15, 58, 89].

Other differential diagnoses should also be taken into consideration, namely infection with other cestodes that can infect humans, such as Hymenolepis spp., Taenia solium, T. saginata and Railletina spp. [58, 85]. The correct diagnosis of each species can be achieved by a rigorous microscopic examination of the proglottids or by using molecular techniques [58, 85, 123]. In humans, D. caninum infection is considered to be rare, which may be related to the few symptoms it causes and the lack of knowledge about the disease, with consequent misdiagnosis. These factors possibly lead to disease underdiagnosis and underreporting [1, 58].

In companion animals, other differential diagnoses should be considered and may include bacterial, viral, fungal or parasitic infections, or other gastrointestinal diseases. Although scooting behaviour due to anal itching is characteristic of tapeworm infection, other conditions should also be discarded: anal sac disorders or allergic conditions, such as atopic dermatitis, flea bite allergic dermatitis or adverse food reaction [2, 67, 124].

Treatment

Dogs and cats

Although D. caninum infection is not very pathogenic in animals, with few clinical signs, the infection should be treated, especially due to its zoonotic potential [2, 37].

The drug of choice for the treatment of D. caninum infection in dogs and cats is praziquantel, administered either orally or subcutaneously at a single dose of 5 mg/kg [2, 8, 37, 67]. Other effective therapeutic options include epsiprantel at 2.75 mg/kg in cats and 5.5 mg/kg in dogs, and nitroscanate in dogs at a single dose of 50 mg/kg [2, 8, 37]. Despite praziquantel and epsiprantel being very effective, resistance to these two drugs has recently been reported in dogs infected with D. caninum, raising some concern, particularly as there are relatively few effective molecules to treat cestode infections in animals and humans [125]. If the anthelmintic used, either prophylactically or therapeutically, has no action against tapeworms, the animals will remain untreated for D. caninum, which not only delays diagnosis but also prolongs the disease and increases the risk to other animals and people. In addition, and as re-infection may occur, treatment with an anti-cestode should be combined with flea and lice control measures [2, 13].

Telluric fungi and bacteria can be used in biological control measures against parasites. When administered to animals, they are subsequently excreted in the faeces, thereby acting on the environment by eliminating possible immature stages of helminths present therein [13, 126,127,128,129]. Their use has been consistently reported in the control of parasitosis in large animals [126, 127]. This form of treatment could also be used in companion animals, particularly as a means to control D. caninum environmental contamination [13], as demonstrated by the in vitro studies with the nematophagous fungus Pochonia chlamydosporia [129], and with the bacterium Bacillus thuringiensis [128].

Humans

The drug of choice to treat dipilidiosis in humans is also praziquantel [58, 65], at an oral single dose of 400–600 mg in adults and 10–20 mg/kg body weight in children [16, 21, 64, 65, 87, 92]. In heavy or persistent infections, a second dose may be necessary, administered at an interval of 2 to 4 weeks [16, 58]. There have also been reports of cases treated with higher doses (25 mg/kg) [85, 91], with multiple doses [61] or with a combination of different drugs (i.e. praziquantel + niclosamide) [58]. The reported decrease in the effectiveness of the recommended dosage may be related to the indiscriminate use of praziquantel in veterinary medicine, leading to the development of tolerance or resistance to the drug, or to cases of reinfection [58, 125]. Praziquantel is well-tolerated, but its use is not advised in pregnant or breastfeeding women [16, 58, 65].

Treatment with niclosamide, although effective, is more laborious as it requires prior preparation of the intestine with a liquid-based diet beginning in the afternoon of the day preceding treatment [16, 59, 60, 65].

The misdiagnosis of pinworm leads to the prescription of benzimidazoles, such as albendazole and mebendazole, or pyrantel and levamisole [21, 85, 88, 89, 92]. These molecules have no effect against tapeworms, and the incorrect diagnosis and subsequent non-effective treatment have resulted in a prolongation of the disease over time, which can vary from 1 month to 1 year [21, 61, 64, 86, 87, 89, 91, 92].

One possible approach in the diagnosis and treatment of D. caninum in animals and humans is schematised in Fig. 3.

Fig. 3
figure 3

A schematic overview of the diagnostic and treatment procedures in animals and humans with suspected D. caninum infection

Preventive measures

In animals, a multi-pronged approach to control and prevent D. caninum is required. Most importantly, it is necessary to act at the level of the intermediary host. Light infestations of fleas or lice can easily go unnoticed, so a careful examination of the animal should be made at regular intervals with an appropriate comb, with the aim to detect these ectoparasites and/or their eggs and faeces in the animal's fur [130]. The administration of ectoparasiticides to all animals in the household all year round is also advised [85, 88, 130,131,132]. In addition to treatment, suggestions include the regular cleaning and vacuuming of the animal's resting areas, the proper cleaning of grooming utensils and the application, to the animal and/or in the animal’s environment, of insect growth regulators which, by acting on the immature forms, accelerate flea elimination [130]. Other preventive measures include coprological examinations once or twice a year to detect any infection, or when there is symptomatology that justifies it, and the prescription of an anthelminthic drug against tapeworms [37, 85, 131]. A veterinary examination, in combination with the recommended use of ectoparasiticides and anthelmintics throughout the year, can have a major impact on the prevalence of parasites in companion animals [133].

We highlight the fact that sometimes the lack of communication between physicians and veterinarians, or the omission of important parts of the clinical history and lifestyle, may lead to a missed or delayed diagnosis. In some human case reports [63, 88, 89], household pets were appropriately diagnosed and treated for D. caninum 2–3 months before symptoms appeared in the child; however, due to lack of communication or knowledge of the zoonotic capacity of this parasite, infants were diagnosed on more than one occasion with pinworm infection and treated with mebendazole, which did not cure the tapeworm infection. Both the medical and veterinary community should therefore raise awareness of zoonotic diseases and their prevention measures, with education of sanitation and hygienic measures being a priority [134]. Physicians should also ask about contact with animals inside and outside the house and whether these animals have recently presented any similar clinical signs [21].

The detection of D. caninum in children's playgrounds emphasises the need for greater protection of these places against the entry of animals, as well as the importance of removing animal excrements from public areas and thus preventing soil contamination [26, 58, 85, 122, 135]. Children should be advised to avoid touching or playing with stray animals as they are usually poorly protected against parasites [21, 85, 88]. In addition, children should wash their hands frequently, particularly after playing on the floor or with animals, and should not eat on the floor, as contamination of the food with the intermediate hosts may occur [21, 26]. Humans should avoid being licked by animals [88] as their saliva may be contaminated with the cysticercoid larva [88, 89, 136, 137]. In one study from Brazil, D. caninum was present in one vegetable from a supermarket (1.7%, 1/60). Although D. caninum eggs present in soil or food are not the infective form of the parasite, their detection in these types of samples reveals human or animal faecal contamination and highlights, once again, the importance of good hygiene practices, particularly during food preparation and consumption [32].

Conclusions

Dipylidium caninum has been detected worldwide, which is a consequence of the global distribution of its intermediate hosts. Its infection has complex characteristics in terms of transmission, clinical signs, diagnosis, treatment and prevention. Only with a comprehensive knowledge of these characteristics can the clinical suspicion of this parasitosis in animals and humans be increased, appropriate treatments and effective preventive measures implemented and a greater sanitary education secured. It is therefore essential to alert the medical and veterinary community to this zoonotic parasite, which has been underrated, but which may become more frequent in the future.

Availability of data and materials

The references supporting the conclusions of this review are cited in the text, and data are also available in additional files.

References

  1. Martínez-Barbabosa I, Quiroz MG, González LAR, Presas AMF, Cárdenas EMG, Venegas JMA, et al. Dipilidiasis: una zoonosis poco estudiada. Rev Latinoam Patol Clin Med Lab. 2014;61:102–7. [Article in Spanish].

    Google Scholar 

  2. Bowman DD. Class Cestoda. In: Bowman DD, editors. Georgi’s Parasitology for Veterinarians. 10th ed. St Louis, Missouri: Saunders Elsevier; 2014. p. 137–55.

    Google Scholar 

  3. Abdullah S, Helps C, Tasker S, Newbury H, Wall R. Pathogens in fleas collected from cats and dogs: distribution and prevalence in the UK. Parasit Vectors; 2019;12:71.

  4. Dantas-Torres F, Otranto D. Dogs, cats, parasites, and humans in Brazil: opening the black box. Parasit Vectors. 2014;1:22.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rust MK. The biology and ecology of cat fleas and advancements in their pest management: a review. Insects. 2017;8:118.

    Article  PubMed Central  Google Scholar 

  6. US Centers for Disease Control and Prevention. DPDx: Dipylidium caninum. 2019. https://www.cdc.gov/dpdx/dipylidium/index.html. Accessed 22 Dec 2021.

  7. Low VL, Prakash BK, Tan TK, Sofian-Azirun M, Anwar FHK, Vinnie-Siow WY, et al. Pathogens in ectoparasites from free-ranging animals: Infection with Rickettsia asembonensis in ticks, and a potentially new species of Dipylidium in fleas and lice. Vet Parasitol. 2017;245:102–5.

    Article  PubMed  Google Scholar 

  8. Ribeiro VM. Controle de helmintos de cães e gatos. Rev Bras Parasitol Vet. 2004;13:88–95.

    Google Scholar 

  9. Hu L, Zhao Y, Yang Y, Zhang W, Guo H, Niu D. Molecular identification, transcriptome sequencing and functional annotation of Pulex irritans. Acta Parasitol. 2021;66:605–14.

    CAS  Article  PubMed  Google Scholar 

  10. East ML, Kurze C, Wilhelm K, Benhaiem S, Hofer H. Factors influencing Dipylidium sp. infection in a free-ranging social carnivore, the spotted hyaena (Crocuta crocuta). Int J Parasitol. 2013;2:257–65.

    Google Scholar 

  11. Kumar S, Sundararaj P, Kumara HN, Pal A, Santhosh K, Vinoth S. Prevalence of gastrointestinal parasites in bonnet macaque and possible consequences of their unmanaged relocations. PLoS ONE. 2018;13:e0207495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dalimi A, Sattari A, Motamedi G. A study on intestinal helminthes of dogs, foxes and jackals in the western part of Iran. Vet Parasitol. 2006;142:129–33.

    CAS  Article  PubMed  Google Scholar 

  13. Alho AM, Cruz R, Gomes L, de Carvalho LM. Dipylidium caninum, da ingestão da pulga ao controlo do céstode mais comum do cão e do gato. Clín Anim. 2015;1:26–9. [Article in Portuguese]

    Google Scholar 

  14. Pugh RE. Effects on the development of Dipylidium caninum and on the host reaction to this parasite in the adult flea (Ctenocephalides felis felis). Parasitol Res. 1987;73:171–7.

    CAS  Article  PubMed  Google Scholar 

  15. Beugnet F, Polack B, Dang H. Atlas of coproscopy. Paris: Kalianxis; 2008.

    Google Scholar 

  16. García-Agudo L, García-Martos P, Rodríguez-Iglesias M. Dipylidium caninum infection in an infant: a rare case report and literature review. Asian Pac J Trop Biomed. 2014;4:S565-7.

    Article  Google Scholar 

  17. Gutema FD, Yohannes GW, Abdi RD, Abuna F, Ayana D, Waktole H, et al. Dipylidium caninum infection in dogs and humans in Bishoftu Town Ethiopia. Diseases. 2020;9:1.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Yakhchali M, Hajipour N, Malekzadeh-Viayeh R, Esmaeilnejad B, Nemati-Haravani T, Fathollahzadeh M, et al. Gastrointestinal helminths and ectoparasites in the stray cats (Felidae: Felis catus) of Ahar Municipality Northwestern Iran. Iran J Parasitol. 2017;12:298–304.

    PubMed  PubMed Central  Google Scholar 

  19. Trasviña-Muñoz E, López-Valencia G, Monge-Navarro FJ, Herrera-Ramírez JC, Haro P, Gómez-Gómez SD, et al. Detection of intestinal parasites in stray dogs from a farming and cattle region of northwestern Mexico. Pathogens. 2020;9:516.

    Article  CAS  PubMed Central  Google Scholar 

  20. Jenkins DJ, Allen L, Goullet M. Encroachment of Echinococcus granulosus into urban areas in eastern Queensland, Australia. Austr Vet J. 2008;86:294–300.

    CAS  Article  Google Scholar 

  21. Bronstein AM, Fedyanina LV, Lukashev AN, Sergeev AR. Nine cases of human dipylidiasis in Moscow region during 1987 to 2017. Trop Biomed. 2020;37:194–200.

    CAS  PubMed  Google Scholar 

  22. Maikai BV, Umoh JU, Ajanusi OJ, Ajogi I. Public health implications of soil contaminated with helminth eggs in the metropolis of Kaduna Nigeria. J Helminthol. 2008;82:113–8.

    CAS  Article  PubMed  Google Scholar 

  23. Siyadatpanah A, Pagheh AS, Daryani A, Sarvi S, Hosseini SA, Norouzi R, et al. Parasitic helminth infections of dogs, wolves, foxes, and golden jackals in Mazandaran Province, North of Iran. Vet World. 2020;13:2643–8.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Khademvatan S, Abdizadeh R, Rahim F, Hashemitabar M, Ghasemi M, Tavalla M. Stray cats gastrointestinal parasites and its association with public health in Ahvaz city, South Western of Iran. Jundishapur J Microbiol. 2014;7:e11079.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Sadowska N, Tomza-Marciniak A, Juszczak M. Soil contamination with geohelminths in children’s play areas in Szczecin, Poland. Ann Parasitol. 2019;65:65–70.

    PubMed  Google Scholar 

  26. Felsmann MZ, Michalski MM, Felsmann M, Sokół R, Szarek J, Strzyżewska-Worotyńska E. Invasive forms of canine endoparasites as a potential threat to public health—a review and own studies. Ann Agric Environ Med. 2017;24:245–9.

    Article  PubMed  Google Scholar 

  27. Vélez-Hernández L, Reyes-Barrera K, Rojas-Almaráz D, Calderón-Oropeza MA, Cruz-Vázquez JK. Arcos-García JL [Potential hazard of zoonotic parasites present in canine feces in Puerto Escondido, Oaxaca]. Salud Publica Mex. 2014;56:625–30. [Article in Spanish].

    Article  PubMed  Google Scholar 

  28. Polo-Terán LJ, Cortés-Vecino JA, Villamil-Jiménez LC. Prieto YE [Zoonotic nematode contamination in recreational areas of Suba, Bogotá]. Rev salud pública. 2007;9:550–7. [Article in Spanish].

    Article  PubMed  Google Scholar 

  29. Luzio Á, Belmar P, Troncoso I, Luzio P, Jara A, Fernández Í. Parasites of zoonotic importance in dog feces collected in parks and public squares of the city of Los Angeles, Bío-Bío Chile. Rev Chilena Infectol. 2015;32:403–7. [Article in Spanish]

    Article  PubMed  Google Scholar 

  30. Soriano SV, Pierangeli NB, Roccia I, Bergagna HFJ, Lazzarini LE, Celescinco A, et al. A wide diversity of zoonotic intestinal parasites infects urban and rural dogs in Neuquén, Patagonia Argentina. Vet Parasitol. 2010;167:81–5.

    Article  PubMed  Google Scholar 

  31. Gillespie S, Bradbury RS. A survey of intestinal parasites of domestic dogs in central Queensland. Trop Med Infect Dis. 2017;2:60.

    Article  PubMed Central  Google Scholar 

  32. Rocha LFN, Rodrigues SS, Santos TB, Pereira MF, Rodrigues J. Detection of enteroparasites in foliar vegetables commercialized in street-and supermarkets in Aparecida de Goiânia, Goiás Brazil. Braz J Biol. 2022;82:e245368.

    Article  Google Scholar 

  33. Bitam I, Dittmar K, Parola P, Whiting MF, Raoult D. Fleas and flea-borne diseases. Int J Infect Dis. 2010;14:e667-76.

    Article  PubMed  Google Scholar 

  34. Beugnet F, Labuschagne M, de Vos C, Crafford D, Fourie J. Analysis of Dipylidium caninum tapeworms from dogs and cats, or their respective fleas: Part 2. Distinct canine and feline host association with two different Dipylidium caninum genotypes. Parasite. 2018;25:31.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Labuschagne M, Beugnet F, Rehbein S, Guillot J, Fourie J, Crafford D. Analysis of Dipylidium caninum tapeworms from dogs and cats, or their respective fleas: Part 1. Molecular characterization of Dipylidium caninum: Genetic analysis supporting two distinct species adapted to dogs and cats. Parasite. 2018;25:30.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Millán J, Casanova JC. High prevalence of helminth parasites in feral cats in Majorca Island (Spain). Parasitol Res. 2009;106:183–8.

    Article  PubMed  Google Scholar 

  37. European Scientific Counsel Companion Animal Parasites (ESCCAP). Worm control in dogs and cats. European Scientific Counsel Companion Animal Parasites guideline 1. 6th ed. 2021. https://www.esccap.org/uploads/docs/oc1bt50t_0778_ESCCAP_GL1_v15_1p.pdf. Accessed 20 Dec 2021.

  38. Zottler EM, Bieri M, Basso W, Schnyder M. Intestinal parasites and lungworms in stray, shelter and privately owned cats of Switzerland. Parasitol Int. 2019;69:75–81.

    Article  PubMed  Google Scholar 

  39. Martínez-Moreno FJ, Hernández S, López-Cobos E, Becerra C, Acosta I, Martínez-Moreno A. Estimation of canine intestinal parasites in Córdoba (Spain) and their risk to public health. Vet Parasitol. 2007;143:7–13.

    Article  PubMed  Google Scholar 

  40. Loftin CM, Donnett UB, Schneider LG, Varela-Stokes AS. Prevalence of endoparasites in northern Mississippi shelter cats. Vet Parasitol. 2019;18:100322.

    Google Scholar 

  41. Beugnet F, Labuschagne M, Fourie J, Jacques G, Farkas R, Cozma V, et al. Occurrence of Dipylidium caninum in fleas from client-owned cats and dogs in Europe using a new PCR detection assay. Vet Parasitol. 2014;205:300–6.

    CAS  Article  PubMed  Google Scholar 

  42. López-Arias Á, Villar D, López-Osorio S, Calle-Vélez D, Chaparro-Gutiérrez JJ. Giardia is the most prevalent parasitic infection in dogs and cats with diarrhea in the city of Medellín, Colombia. Vet Parasitol. 2019;18:100335.

    Google Scholar 

  43. Rodríguez-Vivas RI, Gutierrez-Ruiz E, Bolio-González ME, Ruiz-Piña H, Ortega-Pacheco A, Reyes-Novelo E, et al. An epidemiological study of intestinal parasites of dogs from Yucatan, Mexico, and their risk to public health. Vector-Borne Zoon Dis. 2011;11:1141–4.

    Article  Google Scholar 

  44. Nagamori Y, Payton ME, Looper E, Apple H, Johnson EM. Retrospective survey of parasitism identified in feces of client-owned cats in North America from 2007 through 2018. Vet Parasitol. 2020;277:109008.

    CAS  Article  PubMed  Google Scholar 

  45. Emamapour SR, Borji H, Nagibi A. An epidemiological survey on intestinal helminths of stray dogs in Mashhad, North-east of Iran. J Parasit Dis. 2015;39:266–71.

    Article  PubMed  Google Scholar 

  46. Xhaxhiu D, Kusi I, Rapti D, Kondi E, Postoli R, Rinaldi L, et al. Principal intestinal parasites of dogs in Tirana, Albania. Parasitol Res. 2011;108:341–53.

    Article  PubMed  Google Scholar 

  47. Eguía-Aguilar P, Cruz-Reyes A, Martínez-Maya JJ. Ecological analysis and description of the intestinal helminths present in dogs in Mexico City. Vet Parasitol. 2005;127:139–46.

    Article  PubMed  Google Scholar 

  48. Rabbani IAR, Mareta FJ, Kusnoto, Hastutiek P, Lastuti NDR, Mufasirin, et al. Zoonotic and other gastrointestinal parasites in cats in Lumajang, East Java, Indonesia. Infect Dis Rep. 2020;12:8747.

  49. Cantó GJ, García MP, García A, Guerrero MJ, Mosqueda J. The prevalence and abundance of helminth parasites in stray dogs from the city of Queretaro in central Mexico. J Helminthol. 2011;85:263–9.

    Article  PubMed  Google Scholar 

  50. Merlo RH, Núñez FÁ, Durán LP. Zoonotic potential of intestinal helminth infections in stray dogs from City of Havana. Rev Cubana Med Trop. 2007;59:234–40. [Article in Spanish]

    Google Scholar 

  51. Cantó GJ, Guerrero RI, Olvera-Ramírez AM, Milián F, Mosqueda J, Aguilar-Tipacamú G. Prevalence of fleas and gastrointestinal parasites in free-roaming cats in central Mexico. PLoS ONE. 2013;8:e60744.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cossío TLI, Luna ADM, Mejia MR, Ortega AF, Cárdenas RH, Núñez CR. Risk factors associated with cat parasites in a feline medical center. J Feline Med Surg Open Rep. 2021;7:1–9.

    Google Scholar 

  53. Ugbomoiko US, Ariza L, Heukelbach J. Parasites of importance for human health in Nigerian dogs: high prevalence and limited knowledge of pet owners. BMC Vet Res. 2008;4:49.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Dubná S, Langrová I, Nápravník J, Jankovská I, Vadlejch J, Pekár S, et al. The prevalence of intestinal parasites in dogs from Prague, rural areas, and shelters of the Czech Republic. Vet Parasitol. 2007;145:120–8.

    Article  PubMed  Google Scholar 

  55. De-La-Rosa-Arana J-L, Tapia-Romero R. Frequency of helminth eggs in faeces of puppies living in urban or rural environments of Mexico City. Iran J Parasitol. 2018;13:632–6.

    PubMed  PubMed Central  Google Scholar 

  56. Sulieman Y, Zakaria MA, Pengsakul T. Prevalence of intestinal helminth parasites of stray dogs in Shendi area, Sudan. Ann Parasitol. 2020;66:115–8.

    PubMed  Google Scholar 

  57. Bwalya EC, Nalubamba KS, Hankanga C, Namangala B. Prevalence of canine gastrointestinal helminths in urban Lusaka and rural Katete Districts of Zambia. Prev Vet Med. 2011;100:252–5.

    Article  PubMed  Google Scholar 

  58. Portokalidou S, Gkentzi D, Stamouli V, Varvarigou A, Marangos M, Spiliopoulou I, et al. Dipylidium caninum infection in children: clinical presentation and therapeutic challenges. Pediatr Infect Dis J. 2019;38:e157–9.

    Article  PubMed  Google Scholar 

  59. Sahin I, Köz S, Atambay M, Kayabas U, Piskin T, Unal B. A rare cause of diarrhea in a kidney transplant recipient: Dipylidium caninum. Transpl Proc. 2015;47:2243–4.

    CAS  Article  Google Scholar 

  60. Xaplanteri P, Gkentzi D, Stamouli V, Kolonitsiou F, Anastassiou ED, Marangos M, et al. Rare worm in an infant’s nappy. Arch Dis Child. 2017;103(2):199.

    Article  PubMed  Google Scholar 

  61. Meena S, Singh A, Kumar VP, Gupta R, Gupta P. Dipylidium caninum: first case in an adult female from Uttarakhand and review of literature. Trop Parasitol. 2020;10:153–7.

    Article  PubMed  Google Scholar 

  62. Elmonir W, Elaadli H, Amer A, El-Sharkawy H, Bessat M, Mahmoud SF, et al. Prevalence of intestinal parasitic infections and their associated risk factors among preschool and school children in Egypt. PLoS ONE. 2021;16:e0258037.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  63. Hogan CA, Schwenk H. Dipylidium caninum infection. New Engl J Med. 2019;380:e39.

    Article  PubMed  Google Scholar 

  64. Narasimham MV, Panda P, Mohanty I, Sahu S, Padhi S, Dash M. Dipylidium caninum infection in a child: a rare case report. Indian J Med Microbiol. 2013;31:82–4.

    CAS  Article  PubMed  Google Scholar 

  65. Neira OP, Jofré ML. Muñoz SN [Dipylidium caninum infection in a 2 year old infant case report and literature review]. Rev Chil Infect. 2008;25:465–71. [Article in Spanish].

    Article  Google Scholar 

  66. Lima JCMP, Piero FD. Severe concomitant Physaloptera sp., Dirofilaria immitis, Toxocara cati, Dipylidium caninum, Ancylostoma sp. and Taenia taeniaeformis infection in a cat. Pathogens. 2021;10:109.

    Article  Google Scholar 

  67. Saini VK, Gupta S, Kasondra A, Rakesh RL, Latchumikanthan A. Diagnosis and therapeutic management of Dipylidium caninum in dogs: a case report. J Parasit Dis. 2016;40:1426–8.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Wani ZA, Allaie IM, Shah BM, Raies A, Athar H, Junaid S. Dipylidium caninum infection in dogs infested with fleas. J Parasit Dis. 2015;39:73–5.

    CAS  Article  PubMed  Google Scholar 

  69. Gal A, Harrus S, Arcoh I, Lavy E, Aizenberg I, Mekuzas-Yisaschar Y, et al. Coinfection with multiple tick-borne and intestinal parasites in a 6-week-old dog. Can Vet J. 2007;48:619–22.

    PubMed  PubMed Central  Google Scholar 

  70. Okoye IC, Obiezue NR, Okorie CE, Ofoezie IE. Epidemiology of intestinal helminth parasites in stray dogs from markets in south-eastern Nigeria. J Helminthol. 2011;85:415–20.

    CAS  Article  PubMed  Google Scholar 

  71. Khan W, Nisa NN, Ullah S, Ahmad S, Mehmood SA, Khan M, et al. Gastrointestinal helminths in dog feces surrounding suburban areas of Lower Dir district, Pakistan: a public health threat. Braz J Biol. 2020;80:511–7.

    CAS  Article  PubMed  Google Scholar 

  72. Budke CM, Campos-Ponce M, Qian W, Torgerson PR. A canine purgation study and risk factor analysis for echinococcosis in a high endemic region of the Tibetan plateau. Vet Parasitol. 2005;127:43–9.

    Article  PubMed  Google Scholar 

  73. Qadir S, Dixit AK, Dixit P, Sharma RL. Intestinal helminths induce haematological changes in dogs from Jabalpur, India. J Helminthol. 2011;85:401–3.

    CAS  Article  PubMed  Google Scholar 

  74. Ngui R, Lee SC, Yap NJ, Tan TK, Aidil RM, Chua KH, et al. Gastrointestinal parasites in rural dogs and cats in Selangor and Pahang states in Peninsular Malaysia. Acta Parasit. 2014;59:737–44.

    Article  Google Scholar 

  75. Mateus TL, Castro A, Ribeiro JN, Vieira-Pinto M. Multiple zoonotic parasites identified in dog feces collected in Ponte de Lima, Portugal—a potential threat to human health. Int J Environ Res Public Health. 2014;11:9050–67.

    Article  PubMed  Google Scholar 

  76. Ilić T, Nišavić U, Gajić B, Nenadović K, Ristić M, Stanojević D, et al. Prevalence of intestinal parasites in dogs from public shelters in Serbia. Comp Immunol Microbiol Infect Dis. 2021;76:101653.

    Article  PubMed  Google Scholar 

  77. Arruda IF, Ramos RCF, Barbosa AS, Abboud LCS, dos Reis IC, Millar PR, et al. Intestinal parasites and risk factors in dogs and cats from Rio de Janeiro, Brazil. Vet Parasitol. 2021;24:100552.

    Google Scholar 

  78. Saldanha-Elias AM, Silva MA, Silva VO, Amorim SLA, Coutinho AR, Santos HA, et al. Prevalence of endoparasites in urban stray dogs from Brazil diagnosed with Leishmania, with potential for human zoonoses. Acta Parasitol. 2019;64:352–9.

    CAS  Article  PubMed  Google Scholar 

  79. Pereira PF, Barbosa AS, de Moura APP, Vasconcellos ML, Uchôa CMA, Bastos OMP, et al. Gastrointestinal parasites in stray and shelter cats in the municipality of Rio de Janeiro, Brazil. Rev Bras Parasit Vet. 2017;26:383–8.

    Article  Google Scholar 

  80. de Souza FB, Nakiri IM, de Lourenço N, da Silva GG, Paschoalini DR, Guimarães-Okamoto PTC, et al. Prevalence of intestinal endoparasites with zoonotic potential in domestic cats from Botucatu, SP, Brazil. Top Comp Anim Med. 2017;32:114–7.

    Article  Google Scholar 

  81. Coelho WMD, do Amarante AFT, de Soutello RVG, Meireles MV, Bresciani KDS. Occurrence of gastrointestinal parasites in fecal samples of cats in Andradina City, São Paulo. Rev Bras Parasitol Vet. 2009;18:46–9. [Article in Portuguese].

    Article  PubMed  Google Scholar 

  82. El-Shehabi FS, Kamhawi SA, Schantz PM, Craig PS, Abdel-Hafez SK. Diagnosis of canine echinococcosis: comparison of coproantigen detection with necropsy in stray dogs and red foxes from Northern Jordan. Parasite. 2000;7:83–90.

    CAS  Article  PubMed  Google Scholar 

  83. Symeonidou I, Gelasakis A, Arsenopoulos KV, Schaper R, Papadopoulos E. Regression models to assess the risk factors of canine gastrointestinal parasitism. Vet Parasitol. 2017;248:54–61.

    CAS  Article  PubMed  Google Scholar 

  84. Ramos NV, Silva MLE, Barreto MS, Barros LA, Mendes-De-Almeida F. Endoparasites of household and shelter cats in the city of Rio de Janeiro, Brazil. Rev Bras Parasitol Vet. 2020;29:1–15.

    Google Scholar 

  85. Cabello RR, Ruiz AC, Feregrino RR, Romero LC, Feregrino RR, Zavala JT. Dipylidium caninum infection. BMJ Case Rep. 2011;2011:bcr0720114510.

    PubMed  PubMed Central  Google Scholar 

  86. Molina CP, Ogburn J, Adegboyega P. Infection by Dipylidium caninum in an infant. Arch Pathol Lab Med. 2003;127:e157–9.

    Article  PubMed  Google Scholar 

  87. Szwaja B, Romańsk L, Ząbczyk M. A case of Dipylidium caninum infection in a child from the southeastern Poland. Wiadomoœci Parazytol. 2011;57:175–8.

    Google Scholar 

  88. Taylor T, Zitzmann MB. Dipylidium caninum in a 4-month old male. Clin Lab Sci. 2011;24:212–4.

    Article  PubMed  Google Scholar 

  89. Samkari A, Kiska DL, Riddell SW, Wilson K, Weiner LB, Domachowske JB. Dipylidium caninum mimicking recurrent Enterobius vermicularis (pinworm) infection. Clin Pediatr. 2008;47:397–9.

    Article  Google Scholar 

  90. Rincon MJ, Gonzalez-Granado LI. [Pets and dipylidiasis]. An Pediatr (Barc). 2011;74(6):420. [Article in Spanish].

  91. Jiang P, Zhang X, Liu RD, Wang ZQ, Cui J. A human case of zoonotic dog tapeworm, Dipylidium caninum (Eucestoda: Dilepidiidae), in China. Kor J Parasitol. 2017;55:61–4.

    Article  Google Scholar 

  92. Chong HF, Hammoud R, Chang ML. Presumptive Dipylidium caninum infection in a toddler. Case Rep Pediatr. 2020;2020:1–3.

    Google Scholar 

  93. Táparo C, Perri SH, Serrano ACM, Ishizaki MN, da Costa TP, do Amarante AFT, et al. Comparison between coproparasitological techniques for the diagnosis of helminth eggs or protozoa oocysts in dogs. Rev Bras Parasitol Vet. 2006;15:1–5.

    PubMed  Google Scholar 

  94. Minnaar WN, Krecek RC, Fourie LJ. Helminths in dogs from a peri-urban resource-limited community in Free State Province, South Africa. Vet Parasitol. 2002;107:343–9.

    CAS  Article  PubMed  Google Scholar 

  95. Diakou A, Sofroniou D, di Cesare A, Kokkinos P, Traversa D. Occurrence and zoonotic potential of endoparasites in cats of Cyprus and a new distribution area for Troglostrongylus brevior. Parasitol Res. 2017;116:3429–35.

    Article  PubMed  Google Scholar 

  96. Diakou A, di Cesare A, Accettura PM, Barros L, Iorio R, Paoletti B, et al. Intestinal parasites and vector-borne pathogens in stray and free-roaming cats living in continental and insular Greece. PLoS Negl Trop Dis. 2017;11:e0005335.

    Article  PubMed  PubMed Central  Google Scholar 

  97. Beiromvand M, Akhlaghi L, Massom SHF, Meamar AR, Motevalian A, Oormazdi H, et al. Prevalence of zoonotic intestinal parasites in domestic and stray dogs in a rural area of Iran. Prev Vet Med. 2013;109:162–7.

    Article  PubMed  Google Scholar 

  98. Zare-Bidaki M, Mobedi I, Ahari SS, Habibizadeh S, Naddaf SR, Siavashi MR. Prevalence of zoonotic intestinal helminths of canids in Mog-han Plain Northwestern Iran. Iran J Parasitol. 2010;5:42–51.

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Sherifi K, Rexhepi A, Hamidi A, Behluli B, Zessin K, Mathis A, et al. Detection of patent infections of Echinococcus granulosus (“sheep-strain”, G1) in naturally infected dogs in Kosovo. Berl Munch Tierarztl Wochenschr. 2011;124:518–21.

    PubMed  Google Scholar 

  100. Miró G, Montoya A, Jiménez S, Frisuelos C, Mateo M, Fuentes I. Prevalence of antibodies to Toxoplasma gondii and intestinal parasites in stray, farm and household cats in Spain. Vet Parasitol. 2004;126:249–55.

    Article  PubMed  Google Scholar 

  101. Minnaar WN, Krecek RC. Helminths in dogs belonging to people in a resource-limited urban community in Gauteng, South Africa. Onderstepoort J Vet Res. 2001;68:111–7.

    CAS  PubMed  Google Scholar 

  102. Knaus M, Kusi I, Rapti D, Xhaxhiu D, Winter R, Visser M, et al. Endoparasites of cats from the Tirana area and the first report on Aelurostrongylus abstrusus (Railliet, 1898) in Albania. Wien Klin Wochenschr. 2011;123:31–5.

    Article  PubMed  Google Scholar 

  103. Klimpel S, Heukelbach J, Pothmann D, Rückert S. Gastrointestinal and ectoparasites from urban stray dogs in Fortaleza (Brazil): high infection risk for humans? Parasitol Res. 2010;107:713–9.

    Article  PubMed  Google Scholar 

  104. El-Seify MA, Aggour MG, Sultan K, Marey NM. Gastrointestinal helminths of stray cats in Alexandria, Egypt: a fecal examination survey study. Vet Parasitol. 2017;8:104–6.

    Google Scholar 

  105. Heukelbach J, Frank R, Ariza L, Lopes ÍS, Silva AA, Borges AC, et al. High prevalence of intestinal infections and ectoparasites in dogs, Minas Gerais State (southeast Brazil). Parasitol Res. 2012;111:1913–21.

    Article  PubMed  Google Scholar 

  106. Gholami S, Daryani A, Sharif M, Amouei A, Mobedi I. Seroepidemiological survey of helminthic parasites of stray dogs in Sari City, Northern Iran. Pak J Biol Sci. 2011;14:133–7.

    Article  PubMed  Google Scholar 

  107. Zibaei M, Sadjjadi M, Sarkari B. Prevalence of Toxocara cati and other intestinal helminths in stray cats in Shiraz, Iran. Trop Biomed. 2007;24:39–43.

    PubMed  Google Scholar 

  108. Adolph C, Barnett S, Beall M, Drake J, Elsemore D, Thomas J, et al. Diagnostic strategies to reveal covert infections with intestinal helminths in dogs. Vet Parasitol. 2017;247:108–12.

    Article  PubMed  Google Scholar 

  109. Rodríguez-Ponce E, González JF, de Felipe MC, Hernández JN, Jaber JR. Epidemiological survey of zoonotic helminths in feral cats in Gran Canaria island (Macaronesian archipelago-Spain). Acta Parasitol. 2016;61:443–50.

    Article  PubMed  Google Scholar 

  110. Martínez-Carrasco C, Berriatua E, Garijo M, Martínez J, Alonso FD, Ybáñez RR. Epidemiological study of non-systemic parasitism in dogs in southeast Mediterranean Spain assessed by coprological and post-mortem examination. Zoon Pub Health. 2007;54:195–203.

    Article  Google Scholar 

  111. Dai RS, Li ZY, Li F, Liu DX, Liu W, Liu GH, et al. Severe infection of adult dogs with helminths in Hunan Province, China poses significant public health concerns. Vet Parasitol. 2009;160:348–50.

    CAS  Article  PubMed  Google Scholar 

  112. Borthakur SK, Mukharjee SN. Gastrointestinal helminthes in stray cats (Felis Catus) from Aizawl, Mizoram, India. Southeast Asian J Trop Med Public Health. 2011;42:255–8.

    CAS  PubMed  Google Scholar 

  113. Hajipour N, Baran AI, Yakhchali M, Khojasteh SMB, Hesari FS, Esmaeilnejad B, et al. A survey study on gastrointestinal parasites of stray cats in Azarshahr, (East Azerbaijan province, Iran). J Parasit Dis. 2016;40:1255–60.

    Article  PubMed  Google Scholar 

  114. Adinezadeh A, Kia EB, Mohebali M, Shojaee S, Rokni MB, Zarei Z, et al. Endoparasites of stray dogs in Mashhad, Khorasan Razavi Province, Northeast Iran with special reference to zoonotic parasites. Iran J Parasitol. 2013;8:459–66.

    PubMed  PubMed Central  Google Scholar 

  115. Labarthe N, Serrão ML, Ferreira AMR, Almeida NKO, Guerrero J. A survey of gastrointestinal helminths in cats of the metropolitan region of Rio de Janeiro Brazil. Vet Parasitol. 2004;123:133–9.

    Article  PubMed  Google Scholar 

  116. Hoggard KR, Jarriel DM, Bevelock TJ, Verocai GG. Prevalence survey of gastrointestinal and respiratory parasites of shelter cats in northeastern Georgia, USA. Vet Parasitol. 2019;16:100270.

    Google Scholar 

  117. Zhu GQ, Li L, Ohiolei JA, Wu YT, Li WH, Zhang NZ, et al. A multiplex PCR assay for the simultaneous detection of Taenia hydatigena, T. multiceps, T. pisiformis, and Dipylidium caninum infections. BMC Infect Dis. 2019;19:854.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Shin JW, Liao WT. Humoral immune response to Dipylidium caninum infection of stray dogs in Taiwan. Vet Parasitol. 2002;104:351–6.

    CAS  Article  PubMed  Google Scholar 

  119. Riggio F, Mannella R, Ariti G, Perrucci S. Intestinal and lung parasites in owned dogs and cats from central Italy. Vet Parasitol. 2013;193:78–84.

    Article  PubMed  Google Scholar 

  120. Torres-Chablé OM, García-Herrera RA, Hernández-Hernández M, Peralta-Torres JA, Ojeda-Robertos NF, Blitvich BJ, et al. Prevalence of gastrointestinal parasites in domestic dogs in Tabasco, southeastern Mexico. Rev Bras Parasitol Vet. 2015;24:432–7.

    Article  PubMed  Google Scholar 

  121. Little S, Adolph C, Downie K, Snider T, Reichard M. High prevalence of covert infection with gastrointestinal helminths in cats. J Am Anim Hosp Assoc. 2015;51:359–64.

    Article  PubMed  Google Scholar 

  122. Raičević JG, Pavlović IN, Galonja-Coghill TA. Canine intestinal parasites as a potential source of soil contamination in the public areas of Kruševac, Serbia. J Infect Dev Countr. 2021;15:147–54.

    Article  Google Scholar 

  123. Davis RE, Mathison BA, Couturier MR. Raillietiniaisis in a toddler from Hawaii: a case of mistaken tapeworm identity. Clin Infect Dis. 2019;69:1053–5.

    Article  PubMed  Google Scholar 

  124. Maina E, Galzerano M, Noli C. Perianal pruritus in dogs with skin disease. Vet Dermatol. 2014;25:e52.

    Article  Google Scholar 

  125. Chelladurai JJ, Kifleyohannes T, Scott J, Brewer MT. Praziquantel resistance in the zoonotic cestode Dipylidium caninum. Am J Trop Med Hyg. 2018;99:1201–5.

    CAS  Article  Google Scholar 

  126. Braga FR, de Araújo JV. Nematophagous fungi for biological control of gastrointestinal nematodes in domestic animals. Appl Microbiol Biotechnol. 2014;98:71–82.

    CAS  Article  PubMed  Google Scholar 

  127. Szewc M, de Waal T, Zintl A. Biological methods for the control of gastrointestinal nematodes. Vet J. 2021;268:105602.

    CAS  Article  PubMed  Google Scholar 

  128. Peña G, Jiménez FAA, Hallal-Calleros C, Morales-Montor J, Hernández-Velázquez VM, Flores-Pérez FI. In vitro ovicidal and cestocidal effects of toxins from Bacillus thuringiensis on the canine and human parasite Dipylidium caninum. BioMed Res Int. 2013;2013:174619.

    PubMed  Google Scholar 

  129. Araujo JM, de Araújo JV, Braga FR, Carvalho RO, Ferreira SR. Activity of the nematophagous fungi Pochonia chlamydosporia, Duddingtonia flagrans and Monacrosporium thaumasium on egg capsules of Dipylidium caninum. Vet Parasitol. 2009;166:86–9.

    Article  PubMed  Google Scholar 

  130. European Scientific Counsel Companion Animal Parasites (ESCCAP). Control of ectoparasites in dogs and cats. European Scientific Counsel Companion Animal Parasites guideline 3. 6th ed. 2019. https://www.esccapuk.org.uk/uploads/docs/ke4lxx07_0720_ESCCAP_Guideline_GL3_v9_1p.pdf. Accessed 20 Dec 2021.

  131. Nagamori Y, Payton ME, Looper E, Apple H, Johnson EM. Retrospective survey of endoparasitism identified in feces of client-owned dogs in North America from 2007 through 2018. Vet Parasitol. 2020;282:109137.

    CAS  Article  PubMed  Google Scholar 

  132. Nagamori Y, Payton ME, Duncan-Decocq R, Johnson EM. Fecal survey of parasites in free-roaming cats in northcentral Oklahoma, United States. Vet Parasitol. 2018;14:50–3.

    Google Scholar 

  133. Gates MC, Nolan TJ. Declines in canine endoparasite prevalence associated with the introduction of commercial heartworm and flea preventatives from 1984 to 2007. Vet Parasitol. 2014;204:265–8.

    Article  PubMed  Google Scholar 

  134. Katagiri S, Oliveira-Sequeira TCG. Prevalence of dog intestinal parasites and risk perception of zoonotic infection by dog owners in São Paulo State, Brazil. Zoon Public Health. 2008;55:406–13.

    CAS  Article  Google Scholar 

  135. Eslami A, Ranjbar-Bahadori S, Meshgi B, Dehghan M, Bokaie S. Helminth infections of stray dogs from Garmsar, Semnan Province, Central Iran. Iran J Parasitol. 2010;5:37–41.

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Guzman R. A survey of cats and dogs for fleas: with particular reference to their role as intermediate hosts of Dipylidium caninum. N Z Vet J. 1984;32:71–3.

    CAS  Article  PubMed  Google Scholar 

  137. Gopinath D, Meyer L, Smith J, Armstrong R. Topical or oral fluralaner efficacy against flea (Ctenocephalides felis) transmission of Dipylidium caninum infection to dogs. Parasit Vectors. 2018;11:557.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to acknowledge Prof. Silvana Belo and Dr. Pedro Ferreira, from the Department of Helminthology of IHMT, for giving us access to Dipylidium caninum specimens, which were used for the photographs in the graphical abstract. The paper is sponsored by Elanco Animal Health in the framework of the 16th CVBD® World Forum Symposium.

Funding

The Global Health and Tropical Medicine centre is funded by the Fundação para a Ciência e a Tecnologia, I.P. (FCT) (GHTM-UID/Multi/04413/2013), Portugal. JR was supported by the Portuguese Ministry of Science, Technology and Higher Education (via FCT) through a Ph.D. grant (2021.04669.BD). AC was supported by a grant (PRT/BD/152100/2021) under the MIT/FCT program.

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JR and CM conceptualised and designed the review. JR conducted the selection and analysis of the articles, performed the literature review and wrote the original draft. AC prepared the distribution map. JR, TN and CM prepared and collected parasites pictures. JR, TN and CM critically reviewed and amended the final manuscript. All authors read and approved the final manuscript.

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Correspondence to Carla Maia.

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Supplementary Information

Additional file 1: Table S1.

Epidemiological studies of Dipylidium caninum in dogs, cats, human, fleas, louses and soil and food contamination (2000–2021). Table S2. Case reports of Dipylidium caninum in humans, dogs and cats (2000–2021).

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Rousseau, J., Castro, A., Novo, T. et al. Dipylidium caninum in the twenty-first century: epidemiological studies and reported cases in companion animals and humans. Parasites Vectors 15, 131 (2022). https://doi.org/10.1186/s13071-022-05243-5

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Keywords

  • Dipylidium caninum
  • Dogs
  • Cats
  • Humans
  • Siphonaptera
  • Epidemiology
  • Diagnosis
  • Treatment
  • Prevention
  • Zoonosis