Toxocara canis infection in multiple types of animals: ophthalmological and pathological observations

doi:10.21203/rs.3.rs-3331032/v1

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Toxocara canis infection in multiple types of animals: ophthalmological and pathological observations

https://doi.org/10.21203/rs.3.rs-3331032/v1

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published 23 Feb, 2024

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Human ocular toxocariasis (OT), caused by pet roundworm Toxocara canis (Nematoda Ascaridoidea), is a worldwide ocular parasitic infection severe threat to eyesight, especially in school-aged children. However, the infection process and pathological mechanism of Toxocara canis on the ocular are difficult to study in human body.

This study was designed to explore long-term ocular manifestation in multiple types of animals infected with Toxocara canis, uncovering the specific pathological mechanism, migration pathway of larvae after infection. Three experinment animals including mice, gerbils and rats were selected and infected with Toxocara eggs, and ocular changes were closely observed and recorded for at least 2 months. The ocular infection rate and mortality tended to be stable at 7 day-post-infection (dpi). At 7dpi, the achievement ratio of mice infected with 2000 T. canis eggs (M2k), gerbils infected with 1000 (G1k), 2000 (G2k) and 4000 (G4k) T. canis eggs were higher, respectively 62.5%, 75%, 100% and 100%. Hemorrhagic lesions, mechanical injury of retina and larval migration can be observed after 3dpi. And the larval tissue, the structure disorder and the inflammation could be observed in the pathological sections. In conclusion, the mice infected with 2000 T. canis eggs and gerbils infected with 1000, 2000, 4000 T.canis eggs represented obvious ocular lesions, could be served for long-term observation.

Ocular Toxocariasis

Toxocara canis

ophthalmology

pathology

Parasitic infection of the eye is a major cause of blindness worldwide[1]. Toxocariasis is one of most common zoonotic infections mostly caused by Toxocara canis and less frequently by Toxocara cati[2], and the definite hosts are dogs and cats. Paratenic hosts include humans, mice, rats, lambs, poultry, pigs, flies and cockroaches[3]. Ocular Toxocariasis (OT) is the clinical manifestation of ocular infection caused by Toxocara larvae. According to Badri’s report[4], the pooled prevalence of OT was 9%. In immunological studies, the highest incidence is in Africa and the lowest in the Mediterranean region. Patients with OT were usually affected unilaterally, although occasionally, cases of bilateral disease have been reported. The most common complaint is blurry vision or loss of vision. OT is a common cause of vision loss and childhood blindness[5], especially for school-aged children from rural areas, with poor health conditions and dog-cat contact history[6].

The toxocariasis transmission cycle begins when an infected dog or cat sheds unembryonated eggs in their feces. Eggs are not infectious until embryonation 2 to 4 weeks later[7]. Human can be infected via the fecal-oral route through the ingestion of infective eggs or larvae[8, 9]. Ingestion results in the hatching of the eggs, and the larvae penetrate the intestinal wall before being carried by circulation to a variety of tissues, including liver, heart, lungs, brain, muscle and eyes[10, 11]. Toxocariasis can be asymptomatic or result in severe organ damage. These are referred to respectively as visceral (VLM), neurologic (NLM), and ocular larva migrans (OLM; also known as OT) and covert toxocariasis clinically[12, 13]. The most common clinical forms are VLM and OT[14]. Patients with VLM can present with fever, hepatomegaly, splenomegaly, respiratory symptoms, muscular pain and anorexia associated to eosinophilia and high titers of anti-Toxocara antibodies[7].

At present, the larval migration and specific pathological mechanism of OT, are still not clear. Previous animal models of OT include mice[15, 16], rats[17, 18], rabbits[19], gerbils[18, 20, 21], hamsters[22], guinea pigs[23] and monkeys[24]. However, these studies presented low incidence of ocular infection and lacked systematic observation and comparison[20], and the observation time of most studies relatively short. In this study, we carried out oral inoculation of Toxocara canis in mice, Mongolian gerbils and Brown Norway (BN) rats, observed their eye manifestations, conducted fundus angiography and pathological changes exploration, aimed to perform long-term eye changes in multiple types of animals infected with Toxocara canis.

Animals

Male C57BL/6 mice aged 3 weeks and BN rats aged 1 month were purchased from SPF Biotechnology (Beijing, China); Male gerbils aged 2 months were purchased from Hangzhou Medical College (Hangzhou, China). The animals were housed under specific pathogen-free condition and standard lighting conditions (12 hours alternating day and night cycles) in Sichuan Agricultural University Veterinary Medical Laboratory, and they had free access to food and water. The animals were maintained and infected in accordance with institutional and national guidelines. This study was approved by the Animal Ethics Committee of Sichuan Agricultural University (China; approval no. SYXK 2014 − 187).

Parasites

The infective T. canis eggs were provided by the parasite laboratory of Sichuan Agricultural University. In brief, the male and female adult worms of T. canis were obtained from the intestines of stray dogs without any deworming treatment under the Scientific Procedures Premises License for the College of Veterinary Medicine, Sichuan Agricultural University. After the male and female adult culture and mating in vitro, the fertilized eggs were obtained, followed by egg dilution using saline containing penicillin, streptomycin and Amphotericin B and egg culture placed in a 35mm diameter culture plate under 28°for 21 days. Egg developments into the second-stage larval stage were observed with optical microscope. Infective eggs were harvested, counted and resuspended in phosphate-buffered saline (PBS) with different concentrations for use.

Experimental grouping and infection

C57BL/6 mice were divided randomly into 5 groups (M1k, M2k, M4k, M8k, M10k) and orally infected with 1000, 2000, 4000, 8000, 10000 T. canis eggs in a total volume of 0.1 ml PBS, respectively. Gerbils were divided randomly into 4 groups (G1k, G2k, G4k, G10k) and orally infected with 1000, 2000, 4000, 10000 T. canis eggs in a total volume of 0.1 ml PBS, respectively. BN rats were divided randomly into 3 groups (R2k, R6k, R10k) and orally infected with 2000, 6000 and 10000 T. cains eggs in a total volume of 0.1 ml PBS, respectively.

Ophthalmologic examination

Ophthalmologic examination of all infected animals was carried out with pupils dilated with tropicamide (Santen Pharmaceutical, Japan) and cornea protected by Gatifloxacin Ophthalmic Gel (Shenyang Xingqi eye medicine Co., Ltd), under anesthesia with sodium pentobarbitone (50 mg/kg, Shanghai Hailing Biotechnology Co., Ltd). Comprehensive ocular examinations were performed as follows: the anterior segment was examined by portable slit lamp, the fundus was examined by MICRON IV retinal microscope (Phoenix Micron IV, Phoenix Research Labs, CA, USA); retinal vascular system was examined using MICRON IV retinal microscope after intraperitoneally injection with 2% fluorescein sodium (Health Manufacturing Services B.V., USA). After ocular observations, the animals were placed on the heat preservation pad for resuscitation, and then tobramycin eye ointment was applied to both eyes. The animals were put into the cages after they were fully awaked. All animals were observed and recorded, and the observation interval was every 2 hours within 3dpi, every 2 days between 4dpi and 14dpi, and every 1 week after 14 dpi. The observation period was 4 months for C57BL/6 mice and 2 months for gerbils and rats.

Hispathological examination

Eyeballs were enucleated immediately after cervical dislocation under anesthesia and fixed in FAS eyeball fixative solution or paraformaldehyde for more than 24 hours. Serial section was taken and stained with hematoxylin and eosin. The immunohistochemistry (IHC) analysis was followed the method in the previous study[25].

Incidence of ocular infection

The ocular infection rates at 3, 5, 7, 14, 35 and 56 days after T. canis challeging are shown in Table 1. No ocular lesions were found in animals before 3dpi. Afterwards, in mice, the ocular infection rate in M1k and M2k increased steadily after infection although a great number of infected mice died in M4k and M8k within 5dpi. In gerbils and BN rats, the ocular infection rates reached a high level and stabilized 5 to 7 days after T. canis infection. It seemed that the ocular infection rates of G1k, G2k, G4k, R2k and R6k groups increased during this infection course. The four groups, M4k, M8k, M10k and G10k had the highest ocular infection rates of, 83.3%, 77.8%, 77.3% and 90% respectively at 3dpi (Table 1 and Fig. 1). The animals in M10k, G10k, and R10k were all died within 5dpi because of systemic parasitic infection. The conditions of dead animals are showed in Fig. 2. The mortality varied by groups within 7pdi and the animal deaths usually occured within 7dpi, and then the mortality tended to be stable. It was clear that a higher infection dose led to a higher death rate. For example, all animals infected with 10000 T. canis eggs were died within 5dpi.

Table 1

Ocular infection rate of all groups at each time point
Group	2dpi (%)	3dpi (%)	5dpi (%)	7dpi (%)	14dpi (%)	35dpi (%)	56dpi (%)
M1k	0.0	8.3	44.4	47.2	55.6	45.8	54.5
M2k	0.0	40.0	80.0	82.4	75.0	95.5	100.0
M4k	0.0	83.3	94.4	75.0	66.7	66.7	100.0
M8k	0.0	77.8	75.0	66.7	75.0	66.7	100.0
M10k	0.0	77.3	100.0	-	-	-	-
G1k	0.0	12.5	62.5	75.0	37.5	62.5	66.7
G2k	0.0	62.5	87.5	100.0	100.0	100.0	-
G4k	0.0	62.5	87.5	100.0	100.0	100.0	100.0
G10k	0.0	90.0	100.0	-	-	-	-
R2k	0.0	8.3	16.7	45.8	-	-	-
R6k	0.0	8.3	62.5	71.4	69.2	56.3	50.0
R10k	0.0	20.0	75.0	-	-	-	-
M-Mice, G-Gerbil, R-Rat, dpi: day-post-infection

Ocular lesions

There are three phases which can be used to distinguish the somatic migration of Toxocara larvae in paratenic hosts[26]. Acute phase of infection is equivalent to the hepato-pulmonary phase which occurs from the time of infection to approximately 14dpi when larvae penetrate the intestinal wall. During the myotropic-neurotropic phase, larvae migrate and accumulate in somatic tissues, indicating the subacute phase of infection. The chronic stage begins approximately 28dpi. During this phase, larvae migrate throughout the entire body to species-dependent predilection sites, where they can remain viable for months to years.

In our study, hyphema, preretinal hemorrhage, retinal hemorrhage, retinal lesion, vitreous opacity, larva migration in vitreous or subretinal tissues were observed across the whole infection process (Fig. 3). The abnormality of retina vessels was detected by fluorescein angiography after 3dpi. Among the ocular lesions, focal hemorrhage, retinal lesions and larva migration were the main manifestations.

Acute phase(7dpi)

The incidence of major ocular manifestations in different groups of 7dpi is shown in Table 2. Hyphema was commonly found in C57 mice (Fig. 3-A) but rarely observed in gerbils and rats. Nevertheless, retinal hemorrhage, preretinal hemorrhage, retinal lesions and larval migration could be detected in these three animals. It was notable that ocular lesions were milder in rats than in gerbils and mice.

Table 2

Ocular lesions at 7dpi
Group	Hyphema (%)	Preretinal hemorrhage (%)	Retinal hemorrhage (%)	Vitreous opacity (%)	Retinal lesion (%)	Larva migration (%)
M1k	0.0	13.9	41.7	38.9	0.0	11.1
M2k	14.7	50.0	64.7	70.6	2.9	14.7
M4k	25.0	25.0	62.5	62.5	0.0	0.0
M8k	0.0	16.7	16.7	33.3	0.0	0.0
M10k	-	-	-	-	-	-
G1k	0.0	12.5	25.0	75.0	0.0	25.0
G2k	0.0	12.5	75.0	75.0	0.0	12.5
G4k	0.0	25.0	62.5	100.0	0.0	25.0
G10k	-	-	-	-	-	-
R2k	12.5	4.2	41.7	12.5	0.0	8.3
R6k	3.6	3.6	64.3	25.0	0.0	3.6
R10k	-	-	-	-	-	-
M-Mice, G-Gerbil, R-Rat, dpi: day-post-infection

The larval moving was observed in the vitreous (Fig. 3-D) or retinal layer (Fig. 3-E, Fig. 3-K, Fig. 4), but the latter predominating. Video of larva migration was shown in Additional file 1. More than one larva was found in the eyes of some mice and gerbils (Fig. 5). However, most larvae eventually moved to the peripheral retina, making it impossible to make continuous observations. The larvae were easier detectable in the gerbils due to its dark grey fundi. Moreover, the larvae moved in the vitreous cavity were more active and moved faster than those in retina layer. The larvae can migrate into the retina layer freely and cause traces on the retina, causing mechanical damages to the retina (Fig. 4). Therefore, although we cannot capture the larval migrations, we could still infer the larvae-caused have damages to retina according to their traces in fundus.

Subacute and chronic phase(8dpi-60dpi)

As the experiments lasted, hyphema, retinal hemorrhage, preretinal hemorrhage partly or totally were absorbed, and retinal lesions were also gradually repaired (Fig. 6). However, vitreous opacification and retina lesions were observed, retinal detachment occurred in a few animals.

Fluorescein angiography

In the fundus of mice and gerbils, hyper fluorescence of the optic disc, vascular leakage, vascular breakage or rupture, vascular tortuosity and dilation, retinal telangiectasia were detected by fundus fluorescein angiography (FFA) (Fig. 7, Fig. 8). FFA could monitor abnormal segmental dilation of blood vessels at 2dpi before presenting significant eye manifestations (Fig. 8-B). The vascular abnormalities in FFA were most severe in mice, followed by rats and gerbils.

Pathological feature

In these three animals, retinal hemorrhage, preretinal hemorrhage and retinal lesion were the most common manifestation. In order to identify the retinal layers in which the larvae arrived, the retinal pathological changes were observed. The results showed that the larvae were mainly located in the outer nuclear layer and the photoreceptor cell layer of the retina (Fig. 9-B, Fig. 9-C). The outer retina showed vacuolar changes and the inner retina thickened with edema (Fig. 9-B, Fig. 9-D). Encouragingly, in a mouse with anterior chamber hemorrhage, ciliary vessel dilatation was observed (Fig. 9-A). Moreover, the outer layer of the retina was disorganized and edematous, and a large number of inflammatory cells infiltrated the optic nerve, anterior optic disc and preretinal tissue (Fig. 9-E, Fig. 9-F).

This study represented the comparison of three species infected with T. canis for the first time, with long-term comprehensive ophthalmologic observation, retinal fluorescein angiography and pathological observation. We also saw active larvae and subsequent mechanical damage of intraocular structure under retinal microscope in all three species throughout the experiment. In general, among all infected animals, M2k, G1k, G2k and G4k represented serious ocular lesions and lower mortality rate, which could be served for long-term observation.

Infection differences between three species of animals

The ocular manifestations appeared at 3dpi in all tested animals, with more significant changes at 5–7 dpi, which consistent with previous studies in which the larvae were found to reach the brain as early as 3-5dpi[27]. Larval migration could be observed in the retina or vitreous throughout the experiment process in these three animal species with more larval activities in vitreous. After animal death, the larvae gradually slow down peristalsis within a few minutes and finally stopped. We found for the first time that the larvae can wriggle in eyes for a long time in mice, rats and gerbils.

Ocular manifestations varied among three species. Hyphema, preretinal hemorrhage, retinal hemorrhage, retinal lesion, vitreous opacity and larva migration in vitreous and retinal layer were the main changes. In mice, the lesions were more serious in the acute phase and hyphema appeared more frequently. We guessed that that it may relate the diameter of the blood vessel through which the larvae migrate. In general, the diameter of the blood vessel in gerbils and rats are larger than that in mice, which reduces the possibility of mechanical damage to blood vessel wall by the larvae. Additionally, the body size of mice is smaller than that of gerbils or rats, and therefore under the same dosage of infectious eggs, the tolerance of the mouse was worse, and its damage was more serious.

Compared to rats, gerbils and mice infected with 2000 T. canis eggs were the ideal animal model for further observation of OT. Gerbils are more susceptible, and the fundus of their eyes are gray to facilitate the observation of lesions. Of course, we also found some problems when using gerbils. For instance, gerbils are more easily provoked and difficult to grasp, more tail breakage occurred during the experiment, moreover, when we took fundus photography, the eyeball of gerbils often rotated, even under anesthesia, which was not conducive to ocular image acquisition. In rats, the fundus of the eyes of rats was much closer to that of humans, but their ocular lesions were slight. The mortality of T. canis-infected animals arised with increasing egg doses. Most of animals died with symptoms of shortness of breath and epistaxis, anatomy revealed bleeding in the lungs. It was considered that the main cause of death was the larval lung invasion in dead animals. A tremendous dose of larval infection could cause larval load to exceed the immune ability of the body or the limiting ability of the liver, then larval escape into the eyes or other organs and causing damages[10].

Pathological findings

In pathological sections, we observed larval tissues, hemorrhagic changes, ocular vascular dilation and disorganized retinal architecture. The structural disorder and folds of the retina indicated the occurrence of related inflammatory reactions. As the observation time prolonged, inflammatory cells infiltration were observed, which was consistent with the absorption of hemorrhagic lesions, vitreous opacity, and white sheath like changes in blood vessels during subacute and chronic phase. In the whole observation period, no obvious granuloma lesions were seen in the retina and choroid of mice and gerbils.

The route of larval migration

The possible routes of the larvae entering the eyes were reported in previous studies which included via arteries, brain to optic nerve or brain to the cerebrospinal fluid and then arriving the choroid[10]. Although there is no direct evidence on larvae passing through the blood vessels in this study, we found a large amount of blood vessel damage in the fundus which resulted in hemorrhagic lesions. Fluorescein angiography showed that some animals could have abnormal segmental dilation (Fig. 8-B) or segmental tumor like dilation of blood vessels (Fig. 8-D) before obvious eye damage, which was suspicious vascular inflammation. In addition, the angiography also was observed as signs of vascular rupture (Fig. 8-F), which may be the mechanical damage caused by larvae. In pathological sections, we also found the vasodilatation of the ciliary body (Fig. 9-A). Based on the above findings, we speculated that the larvae may enter the eye through the arteries. Tortuosity and dilation of the retina blood vessels may result from an inflammatory reaction which was caused by secreted/excreted proteins by larvae, which would facilitate their migrations in the blood vessels.

As an infectious disease, ocular toxocariasis can cause great damage to human eyes, however, the process of ocular toxocarasis infection in the human body is difficult to be tested. Experiment animals could mimic the process of human infection of T. canis. In this study, we selected three different animal species for T. canis infection and found wriggling T. canis larvae and their-caused lesions in animal eyes. Through comparisons of these animals, the mouse M2k and gerbil G1k, G2k and G4k had more serious ocular manifestation and lower mortality rate. Both animals can be used for further exploration related to ocular toxocariasis, including the routes of larval migration to the eye, pathological mechanism and the curative treatment in the future.

Acknowledgements

Not applicable.

Author contributions

Study concept and design: XD, LS, YX, SZ. Drafting of the manuscript and experiment performing: SZ, LS. Revision of the manuscript: XD, YX and LH. Making the decision to submit the paper for publication: SZ, LS, LH, YX and XD.

Funding

This work was supported by the Construction Project of High-Level Hospitals in Guangdong Province (303020107, 303010303058); the National Natural Science Foundation of China (82271092, 32273028); Guangdong Basic and Applied Basic Research Foundation (2023A1515010430).

Availability of data and materials

All relevant data during this study are included in the article.

Ethics approval and consent to participate

This study was approved by the Animal Ethics Committee of Sichuan Agricultural University (China; approval no. SYXK 2014-187).

Consent for publication

Not applicable.

Competing interests

The authors declare that there are no conflicts of interest pertaining to the publication of this article.

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No competing interests reported.

Additionalfile1.avi
Additional file 1: Video of larva movement in eyes of animals. In the fundus recording of C57 mouse, two larvae located in the vitreous cavity and the retinal layer can be observed by adjusting the focal length. In the fundus recording of gerbil and rat, two larvae can be seen moving in the retinal layer

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You are reading this latest preprint version

Toxocara canis infection in multiple types of animals: ophthalmological and pathological observations

Status:

Journal Publication

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Abstract

Figures

Background

Methods

Animals

Parasites

Experimental grouping and infection

Ophthalmologic examination

Hispathological examination

Results

Incidence of ocular infection

Ocular lesions

Acute phase(7dpi)

Subacute and chronic phase(8dpi-60dpi)

Fluorescein angiography

Pathological feature

Discussion

Infection differences between three species of animals

Pathological findings

The route of larval migration

Conclusion

Declarations

References

Additional Declarations

Supplementary Files

Status:

Journal Publication

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