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Year : 2021  |  Volume : 8  |  Issue : 2  |  Page : 83-86

Human dirofilariasis: An emerging zoonotic nematodal infection - A case series


Department of Otorhinolaryngology, Amala Institute of Medical Sciences, Thrissur, Kerala, India

Date of Submission19-Nov-2021
Date of Decision23-May-2021
Date of Acceptance03-Oct-2021
Date of Web Publication30-Dec-2021

Correspondence Address:
Dr. Nevil Varghese
Department of Otorhinolaryngology, Amala Institute of Medical Sciences, Thrissur - 680 555, Kerala
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijamr.ijamr_259_20

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  Abstract 

Dirofilariasis is an emerging parasitic infection caused by Dirofilaria spp., a parasite carried by domestic dogs, cats, and other wild animals. Humans become accidental dead end hosts when inoculated with microfilariae by blood sucking arthropods like mosquitoes. Subcutaneous dirofilariasis is an accidental human infection that presents as subcutaneous nodules in the body resulting from an inflammatory reaction in response to the infection. We report a case series of human dirofilariasis to highlight its increasing trend from a tertiary care hospital in Kerala, South India.

Keywords: Dirofilaria repens, granulomatous reaction, human dirofilariasis, zoonoses


How to cite this article:
Jacob L, Varghese N, Menon AG, Vinayakumar AR. Human dirofilariasis: An emerging zoonotic nematodal infection - A case series. Int J Adv Med Health Res 2021;8:83-6

How to cite this URL:
Jacob L, Varghese N, Menon AG, Vinayakumar AR. Human dirofilariasis: An emerging zoonotic nematodal infection - A case series. Int J Adv Med Health Res [serial online] 2021 [cited 2022 Jan 21];8:83-6. Available from: https://www.ijamhrjournal.org/text.asp?2021/8/2/83/334370




  Introduction Top


Dirofilariasis is a zoonotic nematode infection commonly found in mammals such as dogs, cats, wolves, foxes, and raccoons.[1] An accidental vector borne microfilariae inoculation during their blood meal causes human dirofilariasis by Dirofilaria species such as Dirofilaria repens, Dirofilaria immitis, Dirofilaria tenuis, Dirofilaria ursi, and Dirofilaria subdermata.[2] The human infection may present as pulmonary dirofilariasis, subcutaneous, and ocular dirofilariasis with a rare heart and blood vessel involvement.[1] Humans cardiac and vascular parasite is not known to produce microfilaria in the bloodstream.

Global warming with extended vector borne transmission cycles, enzoonotic distribution, and higher prevalence of canine microfilariae infections contributes to increased prevalence of animal and human dirofilariasis.[3] Failing chemoprophylaxis has also contributed to increased dirofilarial infections in domestic dogs and cats.[3] The prevalence of this emerging zoonosis is rising in various parts of India, particularly in the endemic states, including Kerala. Here, we report series of human dirofilariasis cases from a tertiary care hospital in Kerala, South India.


  Case Reports Top


Case 1

A 56-year-old male was referred from ophthalmology outpatient department with suspected cellulitis and left periorbital swelling for a duration of 1 month. Initial evaluation revealed normal vision with no remarkable findings on ocular assessment. On examination, there was a firm, nontender, non-fluctuant, palpable mass of 2 cm × 1 cm above the medial canthus of the left eye along with congestion and edematous changes [Figure 1]a. Radiographic evaluation and anterior rhinoscopy for the assessment of the paranasal sinuses showed no abnormality. Wide-bore needle aspiration of the presumed lid abscess revealed a 10 cm long slender threadlike dead worm with pus [Figure 1]b and [Figure 1]c. Further, on parasitology evaluation, the causative agent was confirmed as D. repens. He was discharged with a course of oral amoxicillin and clavulanic acid as per hospital protocol to prevent postsurgical infections. On follow-up, he was asymptomatic with complete recovery after the removal of the nematode. No other new subcutaneous nodules were identified.
Figure 1: (a) Clinical picture shows a subcutaneous swelling just superior to the medial canthus of the left eye (arrow), (b) the extracted nematode, and (c) a white to grayish, thread-like, cylindrical worm measuring 10 cm in length and 0.5 mm in diameter

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Case 2

A 50-year-old female presented with complaints of throat pain and swelling over right eye of 4 days duration. On examination, there was tenderness over frontal and ethmoid sinuses. With a provisional diagnosis of frontal sinusitis, the patient was given antibiotics and treated conservatively. Patient again attended outpatient department after 3 days with a localized tender swelling 1cm above and medial to right medial canthus of size 1.5 cm × 1 cm [Figure 2]a. Computed tomography of the paranasal sinuses revealed right nasolacrimal duct obstruction. Aspiration of the subcutaneous swelling with a wide bore needle revealed a thin slender thread-like worm, the same was sent for microbiological examination, and was found to be D. repens [Figure 2]b and [Figure 2]c. She was discharged with a course of oral amoxicillin and clavulanic acid as per hospital protocol to prevent postsurgical infections. On follow-up a week after the procedure, she recovered completely with no new symptoms or subcutaneous swelling.
Figure 2: (a) Clinical picture shows a subcutaneous swelling between the nasal bridge and the right medial canthus (Arrow), (b) a thin thread-like worm being extracted, and (c) the completely extracted whitish worm

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Case 3

A 34-year-old male presented with a left cheek swelling of 3-week duration. The swelling was insidious in onset, with no sudden increase in the size. Clinical examination showed a firm, mobile swelling of 1 cm × 1 cm, located inferior to the left medial canthus and lateral to the left nasofacial fold [Figure 3]a and [Figure 3]b. The swelling was non-tender, non-pulsatile and not adherent to the overlying skin with free infraorbital margin. Routine ENT and ophthalmological examination revealed no findings to suggest paranasal sinus and lacrimal apparatus involvement. He underwent complete excision and enucleation of the swelling. Gross specimen of the excised tissue specimen demonstrated the worm in the center encased within the tuft of fibrous tissue [Figure 3]c. Histopathological examination revealed D. repens with surrounding fibrosis and dense inflammatory infiltration [Figure 4]a and [Figure 4]b. He was treated with one course of intravenous antibiotics. He was discharged with a course of oral amoxicillin and clavulanic acid as per hospital protocol to prevent postsurgical infections. On follow-up, he was asymptomatic with complete recovery and showed no new subcutaneous nodules.
Figure 3: (a) Clinical picture shows a well-defined subcutaneous nodule just inferior to the medial aspect of the left eye (Arrow), (b) intraoperative image shows excision of the nodule into along with a cuff of surrounding tissue, and (c) cut section of the excised tissue specimen demonstrating the worm in the center

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Figure 4: Histopathological examination of the select operative samples. Hematoxylin and eosin staining. (a) Shows multiple vertical and transverse sections of dirofilaria repens surrounded by fibrosis and dense inflammatory tissue response (arrow heads) (×40) and (b) shows magnified (×400) transverse section of dirofilaria with thick eosinophilic cuticle (1), underlying external muscle layer (2) encasing the gravid uterus (3) and the intestinal tubes (4)

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Case 4

A 46-year-old female presented with left supraauricular swelling of an 1-week duration. She also complained of a similar lump in the left cheek with a spontaneous resolution a month ago. No history of purulent discharge associated with the left supraauricular swelling. Clinical examination revealed a nontender, ill-defined scalp swelling of 1 cm × 1 cm in the left supra auricular region. ENT examination was within normal limits. Ultrasound examination showed a hypoechoic lesion with linear mobile internal strands and soft tissue thickening, favored to represent in parasitic infection, likely dirofilariasis. She underwent excision under local anesthesia with dissection of a dirofilarial worm [Figure 5]a and [Figure 5]b. Further microbiological examination suggested D. repens. She was discharged with a course of oral amoxicillin and clavulanic acid as per hospital protocol to prevent postsurgical infections. On follow-up, a week after the procedure, she was asymptomatic with no other subcutaneous nodules.
Figure 5: (a) Intraoperative image shows removal of the worm from a left supraauricular swelling with an incision made over it (Arrow) and (b) the extracted thin, slender, whitish cylindrical worm (Arrow)

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  Discussion Top


Human dirofilariasis is an emerging zoonotic infection with significant increase in the reported subcutaneous and ocular manifestations in the last decade. Dirofilariasis commonly presents with subcutaneous and ocular involvement followed by pulmonary manifestations. Since its initial description in 1885, approximately 1782 cases of human dirofilariasis are reported.[1] They were commonly subcutaneous and ocular dirofilariasis (1410 cases), followed by pulmonary dirofilariasis (372 cases).[1] However, the reported cases may be the “tip of the iceberg,” owing to underreporting of unnoticed subcutaneous nodules and asymptomatic pulmonary dirofilariasis.

Human dirofilariasis have been reported from Southern and Eastern Europe, sub-Saharan Africa, Asia, particularly Sri Lanka, Malaysia, and India.[4],[5] Italy has the highest prevalence of human dirofilariasis (66%), followed by France (22%). The maximum reported cases in India are from Assam, Kerala, Tamil Nadu, and Karnataka.[6],[7],[8],[9],[10] Commonly associated Dirofilaria species with human infections are D. repens and D. immitis. D. repens is the major species associated with subcutaneous and ocular dirofilariasis in Asia and India.[7],[8],[11] D. tenuis and D. repens are the Dirofilaria species predominantly associated with ocular dirofilariasis.[12]

The dogs are a common definitive host for D. repens and D. immitis. However, other animals such as cats, wolves, and raccoons have also been reported as reservoirs.[3] The adult female worm releases microfilaria into the circulation, which are ingested by vectors such as mosquitoes, ticks, and fleas during their blood meal. An accidental human infection can happen as subcutaneous lesions in the body with a resultant inflammatory granulomatous reaction in response to the infection.[3] In humans, adult worms neither reach maturity, nor produce microfilaria.

Subcutaneous dirofilariasis presents as a subcutaneous nodule, caused by an adult D. repens worm in the subcutaneous tissues. It grows slowly over weeks to months and manifests as a firm or pliable nodule associated with erythematous changes. Although any age group can be involved, the reported incidence is higher in the fifth decade of life.[1] In a retrospective study, approximately one-third of reported cases were in children aged below 10 years. Subcutaneous dirofilariasis shows slight female preponderance (55.4% females vs. 44.6% males) with no gender predisposition in pulmonary dirofilariasis.[1] Although subcutaneous nodules are first detected by the patients, they seldom seek medical aid. Most of the subcutaneous nodules are benign unless situated near the lymph node or adjacent to major blood vessels. Only a few patients present with systemic manifestations. Blood eosinophilia is not usually present.

Timely diagnosis is essential for optimal management of human dirofilariasis. The patient detects the subcutaneous nodules, and ocular localization initially, followed by clinical examination and investigations. As pulmonary nodules are asymptomatic in most patients, only a few of the lung nodules are accidentally diagnosed on chest radiography performed for unrelated presentations.[13] However, when detected, both the subcutaneous and pulmonary nodules pose a diagnostic challenge as they mimic malignancy.[1],[14]

In the diagnostic evaluation, adequate sample collection and accurate identification may be challenging due to the absence of microfilaria in the blood and the need for diagnostic biopsy to elicit the presence of worms in the nodules. The diagnosis is established by biopsy and detailed evaluation of the entire tissue specimen to determine the parasite. The key morphological features of dirofilariasis include thick laminated cuticle, broad lateral ends, and large muscle cells. The length of female worms may vary from 8 to 13 cm and male worms from 4 to 4.8 cm.[12],[15] Although external longitudinal cuticular ridges are favored to represent D. repens, these may be present in other Dirofilaria species.[16],[17] However, the exact identification of species may be possible only after studying fully mature worm.[9] The absence of ridge enables differentiation of D. immitis from D. repens.[9] In our cases, histopathological examination revealed thick cuticle in the cut section of the worm favoring D. repens. The molecular and immunological techniques present diagnostic alternatives for morphology-based histopathological examination. To confirm the Dirofilaria species, DNA extraction followed by pan-filarial polymerase chain reaction may be performed after the extraction of the parasite and morphological evaluation to confirm the diagnosis.[18]

Chemotherapy is not recommended for human dirofilariasis as microfilaremia is extremely rare.[1],[8] The definitive choice for treatment is the surgical removal of the worm to rule out the malignant origin of the nodule. Complete resection of subcutaneous nodules or conjunctival filaria is a relatively simple procedure. However, complex surgical procedures may be needed for pulmonary, intraorbital, retro-orbital, or other deep locations.[3] In our cases, complete surgical removal of subcutaneous nodules along with the necrosed or entire live worm was done. The prognostic outcome is excellent in patients with subcutaneous dirofilariasis.


  Conclusion Top


Human dirofilariasis is an emerging zoonotic infection attributed to increased ecological niche for the breeding of vector species, global warming, and higher incidence of canine dirofilariasis. As most of the Dirofilaria infections are likely undiagnosed and unpublished, we emphasize the need for increased awareness of this nematodal infection, the diagnostic serological tests that aid in differentiating it from its mimics, including malignancy and avoid inadvertent surgical management.

Acknowledgment

We acknowledge the valuable help of Dr.Ajith T.A Professor, Department of Biochemistry, Amala Institute of Medical Sciences, Thrissur, Kerala, India, during the preparation of this manuscript.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Simón F, Siles-Lucas M, Morchón R, González-Miguel J, Mellado I, Carretón E, et al. Human and animal dirofilariasis: The emergence of a zoonotic mosaic. Clin Microbiol Rev 2012;25:507-44.  Back to cited text no. 1
    
2.
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3.
Diaz JH. Increasing risks of human dirofilariasis in travelers. J Travel Med 2015;22:116-23.  Back to cited text no. 3
    
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Pampiglione S, Canestri Trotti G, Rivasi F. Human dirofilariasis due to Dirofilaria (Nochtiella) repens: A review of world literature. Parassitologia 1995;37:149-93.  Back to cited text no. 4
    
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Megat Abd Rani PA, Irwin PJ, Gatne M, Coleman GT, Traub RJ. Canine vector-borne diseases in India: A review of the literature and identification of existing knowledge gaps. Parasit Vectors 2010;3:28.  Back to cited text no. 5
    
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Joseph E, Matthai A, Abraham LK, Thomas S. Subcutaneous human dirofilariasis. J Parasit Dis 2011;35:140-3.  Back to cited text no. 7
    
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Sathyan P, Manikandan P, Bhaskar M, Padma S, Singh G, Appalaraju B. Subtenons infection by Dirofilaria repens. Indian J Med Microbiol 2006;24:61-2.  Back to cited text no. 9
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Sekhar HS, Srinivasa H, Batru RR, Mathai E, Shariff S, Macaden RS. Human ocular dirofilariasis in Kerala Southern India. Indian J Pathol Microbiol 2000;43:77-9.  Back to cited text no. 10
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Khurana S, Singh G, Bhatti HS, Malla N. Human subcutaneous dirofilariasis in India: A report of three cases with brief review of literature. Indian J Med Microbiol 2010;28:394-6.  Back to cited text no. 11
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Nadgir S, Tallur SS, Mangoli V, Halesh LH, Krishna BV. Subconjunctival dirofilariasis in India. Southeast Asian J Trop Med Public Health 2001;32:244-6.  Back to cited text no. 12
    
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Cordero M, Muro A, Simón F, Tapia JI, Espinoza E. Are transient pulmonary solitary nodules a common event in human dirofilariosis? Clin Investig 1992;70:437-40.  Back to cited text no. 13
    
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Simón F, López-Belmonte J, Marcos-Atxutegi C, Morchón R, Martín-Pacho JR. What is happening outside North America regarding human dirofilariasis? Vet Parasitol 2005;133:181-9.  Back to cited text no. 14
    
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Joseph K, Vinayakumar AR, Criton S, Vishnu MS, Pariyaram SE. Periorbital mass with cellulitis caused by dirofilaria. Indian J Med Microbiol 2011;29:431-3.  Back to cited text no. 16
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Favia G, Tringali R, Cancrini G. Molecular diagnosis of human dirofilariasis. Ann Trop Med Parasitol 1997;91:961-2.  Back to cited text no. 18
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5]



 

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