Ocular dirofilariasis: the increasing incidence in a temperate zone

Full Text

Dirofilariasis (Dirofilariasis, from Lat. diro, filum, “evil thread”) is a disease caused by infection with the parasitic nematode Dirofilaria. The sources of infection are typically infected domestic or stray dogs and cats, and less commonly, wild civets. The infection is transmitted through a vector-borne pathway via the bites of blood-sucking insects. The larvae of Dirofilaria mature in the Malpighian vessels of insects, primarily of mosquitoes of the genera Aedes (31%), Culex (17%), and Anopheles (2.5%) [6], until reaching the invasive stage [4–9]. The prevalence of this transmissible zoonotic infection has been increasing steadily in Russia since the 1990s [1–3]; numerous infections with Dirofilaria repens have been recorded in the Russian Federation.

Humans are accidental hosts for these nematodes; larval survival in human subjects is extremely low, and as such, humans serve as a biological “dead end” for Dirofilaria. Only two cases of simultaneous infection with several Dirofilaria organisms have been reported in the literature; in all remaining cases, only one organism develops and ultimately remains immature. Interestingly, in 99.7% of the cases, a single immature female was identified [4].

Typically, the infection is not recognized by health care practitioners, and the patient is provided with another diagnosis, such as atheroma, phlegmon, fibroma, boils, cyst, tumor, and/or one of several granulomatous diseases [1]. The most common complaint related to Dirofilaria infection are migrating painful swellings, which often occur at night. In some cases, this is accompanied by neurological pain of varying degrees of intensity [6]. In the ocular form, which accounts for 50% of all cases of human dirofilariasis, infection typically involves the subcutaneous tissue of the eyelid or the conjunctiva and can present with symptoms of acute conjunctivitis [3, 8, 9]. Helminth infections of the sclera, vitreous body, retina, or retrobulbar space are extremely rare and can be accompanied by serious complications [5, 10].

Due to the fact that many physicians are not aware of the prevalence of this disease, arriving at a correct diagnosis can be complicated. There are no specific laboratory tests for humans, and as such, an epidemiological history is of critical importance. Symptoms and clinical manifestations in association with a history of travel to or residence in endemic areas, especially during the season of prominent mosquito activity, should suggest the possibility of this infection [4]. The diagnosis is largely based on clinical manifestations, which are variable in subcutaneous dirofilariasis in humans, and associated with the localization of Dirofilaria in subcutaneous tissue. The cyclical nature of the symptoms is a striking characteristic, the most important of which is the constant movement of the parasite as well as the overall ineffectiveness of antiallergic and antiinflammatory therapies. In the absence of a visibly detectable helminth (as one would see with subconjunctival localization) or moving induration (associated with subcutaneous localization), an ultrasound scan or computed tomography may shed clarity on the diagnosis [12]. However, it is critical to recognize that the use of ultrasound can accelerate helminth migration, which can generate further difficulties with respect to its removal. For the same reason, physiotherapeutic procedures, such as heating with compresses or warming ointments, are also contraindicated. In some cases, the diagnosis is made when a live helminth emerges on its own, as a result of an incision made in a cyst wall, affected node, or granuloma, or upon direct surgical excision [11].

Treatment ultimately includes the removal of the helminth. Antiparasitic drugs are unnecessary given that one is typically infected by a single parasite, which in most cases is an immature female that does not generate larvae [7].

Currently, the incidence of dirofilariasis is growing both in endemic areas with warm and humid climate and in regions with a more temperate climate as well.

CLINICAL CASE NO. 1

The first case was a 30-year-old male who presented in January 2019 with a chief complaint of an unusual sensation under the upper eyelid of the right eye. He was a citizen of Congo; however, he had not left the Russian Federation for five years and was currently residing in the Leningrad region. He reported that five months prior to presentation, he visited a reservoir where there were many mosquitoes. In the ophthalmic trauma center, a helminth was discovered under the conjunctiva upon inversion of the upper eyelid which could not be removed due to its rapid migration. The patient was referred to the city multi-field hospital No. 2 in St. Petersburg. After one unsuccessful attempt to remove the parasite, it migrated to a position under the conjunctiva of the right eye; it was successfully removed through conjunctiva surgery (Fig. 1). A parasitological study identified the pathogen as a 7.6-cm immature D. repens female.

 

Fig. 1. Patient N., 30 years old. a – the parasite is visualized under the skin of the upper eyelid OD; b – helminth under the conjunctiva OD; c – helminth extraction

Рис. 1. Пациент Н., 30 лет. a — паразит визуализируется под кожей верхнего века OD; b — гельминт под конъюнктивой OD; c — извлечение гельминта

 

CLINICAL CASE NO. 2

The second patient was a 52-year-old female resident of St. Petersburg who presented to a primary health care facility in March 2019 with a chief complaint of a painful node in the right temporal region. The clinical presentation initially resulted in a diagnosis of allergic/inflammatory reaction to an insect bite. After 10 days, the node disappeared, but within two months it appeared periodically in the region of the right temple, right zygomatic arch, and upper eyelid of the right eye. One month later, she presented to the eye trauma center with sharp burning pains at the outer corner of the upper eyelid and pronounced edema of the eyelids and periorbital tissues. She also noted progressive weakness and fatigue. A tumor-like formation was identified under the skin of the upper eyelid of the right eye (Fig. 2) in association with edema of the eyelids, minor hyperemia, and chemosis; the parasite was visualized at that time. She was diagnosed with parasitic subcutaneous granuloma of the right eye. The skin of the upper eyelid was dissected along the path of the migrating parasite. An incision was made through a dense area of granulation tissue and a mobile 10-cm long helminth was removed, which was subsequently identified as an immature specimen of D. repens.

 

Fig. 2. Patient N., 52 years old. a – the parasite under the skin of the upper eyelid OD; b – Female D. repens extracted from under the skin of the upper eyelid

Рис. 2. Пациентка Н., 52 года. a — паразит под кожей верхнего века OD; b — Самка D. repens извлеченная из-под кожи верхнего века

 

CLINICAL CASE NO. 3

The third patient was an 88-year-old resident of St. Petersburg who presented with chief complains of severe acute pain and a sharp decrease in vision in his right eye. In October 2019 he was sent to hospital No. 2 from a primary care facility for emergency diagnosis and care. He was initially diagnosed with acute anterior iridocyclitis with posterior synechia; the examination was also notable for open-angle IIIa postoperative drug-controlled glaucoma and an immature cataract. The patient reported the recent onset of aching pains that were aggravated by pressure on the right eye. Findings at admission included pronounced, mixed injection of the eyeball; the cornea was smooth and slightly edematous with small-point precipitates on the endothelium and on the single folds of the Descemet’s membrane. The anterior chamber was of medium depth and contained fibrin fibers. At the 12 o’clock position, there was postoperative coloboma of the iris. The reflex from the fundus was pink-colored; the fundus could not be evaluated ophthalmoscopically due to diffuse opacities in all layers of the lens. A translucent helminth, approximately 1.5-cm long, was visualized in the meridian in the 5 o’clock position; the helminth was moving unusually fast and chaotically, while one of the ends of its body was fixed to the stroma of the iris (Fig. 3). Visual acuity was tested by hand movement in the face and intraocular pressure was 5 mmHg. A preliminary diagnosis was made of ophthalmic dirofilariasis of the right eye and anterior uveitis. The ultrasound examination revealed vascular detachment from the equator with moderate bubbles and small-point opacities in the vitreous body; no other pathology was detected. Surgery was performed to remove the helminth from the anterior chamber of the right eye. After instillation of an anesthetic agent and standard preparation of the surgical field at the 12 o’clock position, corneal paracentesis was performed. Viscoelastic gel was administered, and the helminth was removed from the anterior chamber with sterile forceps. The helminth was identified at the Department of Infectious Diseases of the S.M. Kirov Military Medical Academy an immature D. repens female.

 

Fig. 3. Patient H., 88 years old. a – helminth in the anterior chamber of the eye OD; b – helminth is fixed by the end portion of the body to the stroma of the iris OD

Рис. 3. Пациент Х., 88 лет. a — гельминт в передней камере глаза OD; b — гельминт фиксирован концевым участком тела к строме радужки OD

 

CLINICAL CASE NO. 4

The final patient was a 59-year-old resident of St. Petersburg who presented to a primary health care facility in October 2019 with a chief complaint of a swollen eyelid and burning pain at the bridge of her nose. Her past history was notably for a trip taken during the summer of 2019 to a cottage in the Leningrad region. She was sent to hospital No. 2 with suspected dirofilariasis. A helminth of 5.7 cm in length was discovered and removed from underneath the bulbar conjunctiva of the right eye in the lower external section. The helminth was later identified at the Department of Infectious Diseases of the S.M. Kirov Military Medical Academy as an immature D. repens female (Figs. 4–6).

 

Fig. 4. Patient T., 59 years old. a – subconjunctival localization of helminth OD; b – stage of surgical removal of the parasite

Рис. 4. Пациентка Т., 59 лет. a — субконъюнктивальная локализация гельминта OD; b — этап хирургического удаления паразита

 

Fig. 5. Photo of the end area of the extracted D. repens female executed with a stereomicroscope digital camera

Рис. 5. Фото концевого отдела извлеченной самки D. repens, выполненноe цифровой камерой стереoмикроскопа

 

Fig. 6. Photo of a helminth executed with a stereomicroscope digital camera

Рис. 6. Фото гельминта, выполненноe цифровой камерой стереoмикроскопа

 

The following two features were common to all four patients in this report, as well as the previous five cases of this infection reported from 2015–2018: (1) initial right-sided localization. A similar and yet unexplained tendency for infection in the right eye is observed in global practice for both the ocular and skin and visceral forms of human dirofilariasis; and (2) patients remained within the Russian Federation for more than two years until the diagnosis of dirofilariasis was established.

Given the history of the disease and the development cycle of the parasite, all cases of invasion are local infections. Likewise, many of the recent cases can be traced epidemiologically to territory within the Leningrad region. This finding is in accordance with the global trend of northward expansion of the regions endemic for dirofilariasis [11]; as such, ophthalmologists need to be especially alert to this disease.

About the authors

Nataliya G. Zumbulidze

North-Western State Medical University named after I.I. Mechnikov

Author for correspondence.
Email: guramovna@gmail.com
ORCID iD: 0000-0002-7729-097X
SPIN-code: 4439-8855

MD, PhD, Assistant Professor, Ophthalmology Department

Russian Federation, Saint Petersburg

Janina S. Konenkova

City Multi-Field Hospital No. 2

Email: Krocon@mail.ru

MD, Head of Department, Microsurgery Department No. 4

Russian Federation, Saint Petersburg

Alexandr V. Laskin

S.M. Kirov Military Medical Academy

Email: lar_vma@mail.ru

MD, PhD, Senior Lecturer, Department of Infectious Diseases (with a Course of Medical Parasitology and Tropical Diseases)

Russian Federation, Saint Petersburg

Olga M. Kasatkina

Diagnostic center No. 7 (ophthalmological) for adults and children

Email: kasatik-2101@mail.ru

Ophthalmic Surgeon

Russian Federation, Saint Petersburg

Dmitrij F. Belov

City Multi-Field Hospital No. 2

Email: belovd1990@gmail.com

Ophthalmic Surgeon

Russian Federation, Saint Petersburg

Dmitrij V. Vigonyuk

Regional clinical hospital of the Kaliningrad Region

Email: vigonyk@gmail.com

Ophthalmic Surgeon

Russian Federation, Kaliningrad

References

Supplementary files