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Onchocerca jakutensis filariasis in humans.
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MedLine Citation:
PMID:  18217562     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
We identified Onchocerca jakutensis as the causative agent of an unusual human filariasis in a patient with lupus erythematosus. To our knowledge, this is the first case of human infection with O. jakutensis and the first human case of zoonotic onchocercosis involving >1 worm.
Authors:
Martina Koehsler; Afschin Soleiman; Horst Aspöck; Herbert Auer; Julia Walochnik
Publication Detail:
Type:  Case Reports; Journal Article    
Journal Detail:
Title:  Emerging infectious diseases     Volume:  13     ISSN:  1080-6040     ISO Abbreviation:  Emerging Infect. Dis.     Publication Date:  2007 Nov 
Date Detail:
Created Date:  2008-01-25     Completed Date:  2008-03-25     Revised Date:  2012-09-18    
Medline Journal Info:
Nlm Unique ID:  9508155     Medline TA:  Emerg Infect Dis     Country:  United States    
Other Details:
Languages:  eng     Pagination:  1749-52     Citation Subset:  IM    
Affiliation:
Medical University of Vienna, Vienna, Austria.
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MeSH Terms
Descriptor/Qualifier:
Animals
Female
Humans
Immunocompromised Host
Lupus Erythematosus, Systemic / therapy
Middle Aged
Onchocerca / isolation & purification*
Onchocerciasis / drug therapy,  parasitology*,  surgery
Polymerase Chain Reaction / methods
Renal Dialysis
Zoonoses / parasitology
Comments/Corrections

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Journal Information
Journal ID (nlm-ta): Emerg Infect Dis
Journal ID (iso-abbrev): Emerging Infect. Dis
Journal ID (publisher-id): EID
ISSN: 1080-6040
ISSN: 1080-6059
Publisher: Centers for Disease Control and Prevention
Article Information
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Print publication date: Month: 11 Year: 2007
Volume: 13 Issue: 11
First Page: 1749 Last Page: 1752
ID: 3375810
PubMed Id: 18217562
Publisher Id: 07-0017
DOI: 10.3201/eid1311.070017

Onchocerca jakutensis Filariasis in Humans Alternate Title:Onchocerca jakutensis Filariasis in Humans
Martina Koehsler*
Afschin Soleiman*
Horst Aspöck*
Herbert Auer*
Julia Walochnik*
*Medical University of Vienna, Vienna, Austria
Correspondence: Address for correspondence: Julia Walochnik, Department of Medical Parasitology, Clinical Institute of Hygiene and Medical Microbiology, Medical University of Vienna, Kinderspitalgasse 15, 1095 Vienna, Austria; email: julia.walochnik@meduniwien.ac.at

Zoonotic filarial infestations occur worldwide, and in most reported cases the involved species are members of the genus Dirofilaria. However, zoonotic Onchocerca infections are rare and to date only 13 cases (originating from Europe, Russia, the United States, Canada, and Japan) have been described. In all of these cases only 1 immature worm was found, and the causative species was identified as O. gutturosa, O. cervicalis, O. reticulata, or O. dewittei japonica on the basis of morphologic and in some cases serologic parameters (14). O. cervicalis and O. reticulata are found in the ligaments of the neck and extremities of horses, O. gutturosa is typically found in the nuchal ligaments of cattle, and O. dewittei japonica is found in the distal parts of the limbs and adipose tissue of footpads of wild boars.

We identified the causative agent of a zoonotic Onchocerca infection with multiple nodules in a patient with systemic lupus erythematosus (SLE) who had been receiving hemodialysis. The parasite was identified in paraffin-embedded tissue samples by PCR and DNA sequence analysis.


The Study

The patient was a 59-year-old woman with SLE who had developed multiple nodules on the neck and face over several years. Because of major renal insufficiency, she also had been receiving hemodialysis 3 times per week (3.5 hours) for >10 years. The first clinical differential diagnoses were cutaneous SLE, nephrogenous dermatopathy, calciphylaxis, and calcinosis. The clinical picture was obscured by secondary inflammations and ulcerations caused by self-inflicted trauma. Multiple sampling attempts by cutaneous core biopsies resulted in histologic diagnosis of unspecific, secondary inflammatory changes. Deep surgical excision of 1 subcutaneous nodule on the scalp indicated subcutaneous helminthosis (Figure). The patient was treated with ivermectin and subjected to 2 plastic surgeries for facial reconstruction, after which she recovered.

At this point, species identification of the causative agent was still pending. A history of travel anamnesis and location of the nodules indicated a possible Dirofilaria infection, but a specific PCR showed negative results. Morphologic features of the few available sections suggested Onchocerca spp. To our knowledge, multiple nodules had never been reported in cases of infection with zoonotic Onchocerca. Because a definitive morphologic identification of the causative nematode was not possible, molecular identification from DNA isolated from the only available material (formalin-fixed and paraffin-embedded tissue) was conducted.

To evaluate the causative genus, universal filarial primers were constructed on the basis of filarial sequences available in GenBank (primer FILfw 5′-cggtgatattggttggtctc-3′ for the first internal transcribed spacer region and primer FILrev 5′-ctagctgcgttcttcatcgatc-3′ for the 5.8S rRNA gene). PCR and sequencing were performed and a similarity matrix was calculated after multiple sequence alignment (5).

The DNA fragment obtained was 226 bp and showed greatest similarities to Onchocerca sequences, ranging from 87% to 95%. Similarities to Wuchereria, Brugia, Mansonella, Dirofilaria, and Acanthocheilonema were lower, ranging from 75% to 80%. Assignment to the genus Onchocerca was obvious, but species identification still posed a problem because published O. volvulus sequences showed higher similarities among each other (98.8%–100%) than with our sequence. The only exception was a clinical O. volvulus strain (OvNod1–3) from Bolo, Cameroon, which showed 94.8% sequence similarity. However, the authors of that report indicated that their strain might be a zoonotic Onchocerca sp. (6).

An identical thymine mononucleotide repeat motif in our strain and strain OvNod1–3, which was shorter in all O. volvulus sequences, indicated that both strains were not O. volvulus because repeat motifs have been reported to occur in species-specific patterns. The negative results with an O. volvulus–specific PCR (6) corroborated this assumption. Therefore, 2 additional primer pairs for Onchocerca spp. identification were constructed, 1 for the mitochondrial NADH dehydrogenase subunit 5 gene (OND5fw 5′-ctcctgttagttgtttggttc-3′, OND5rev 5′-gcaaacccctaccaatagc-3′) and 1 for the 16S mitochondrial rRNA gene (O16fw 5′-gcgtgatggcataaaagtagc-3′, O16rev 5′-caaccctgttaactccggag-3′), on the basis of available Onchocerca spp. sequences (7,8). PCR products were sequenced and similarity matrices were calculated (Tables 1, 2). The NADH amplicon was 201 bp and the 16S rRNA amplicon was 225 bp. Both amplicons unambiguously identified our strain as O. jakutensis with 100% and 99.55% sequence similarities, respectively. Sequence data were deposited in GenBank and are available under the following accession nos.: EF202184, EF202185, and EF202186.


Conclusions

The limiting factor in identifying the causative agent in our patient was the nature of the sample material. Because only a few formalin-fixed and paraffin-embedded sections were available, morphologic identification was not possible. PCR-based identification was restricted because DNA has a tendency to degrade when stored in formalin, which limits the length of the target sequence to ≈300 bp and limits its discriminatory power (9). A different approach with 3 PCRs, 1 for genus identification and 2 for species identification, and primers for highly variable multicopy targets enabled us to accurately identify the causative agent as O. jakutensis.

To our knowledge, O. jakutensis has never been identified as an agent of human filariasis. It has been identified as a rare parasite of red deer in Germany, Poland, and Russia, and may also be found in other northern European countries (10). Our patient came from the United States and had traveled all over Europe. She could thus have acquired the infection in several different locations.

Two findings for this patient were particularly unusual and obscured the identification of the parasite. The first finding was that she had, in contrast to all previous human cases of zoonotic onchocercosis, multiple nodules. The second finding was that her face (periorbital and buccal), neck, and scalp were affected, although zoonotic filariae are typically found in similar or identical tissues as in their natural hosts (11). O. jakutensis is usually found in tissues of the outer thigh and caudal part of the back; >2 nodules per infected host are rare (12,13).

It is unlikely that these findings are associated with greater virulence of O. jakutensis than of other zoonotic Onchocerca spp. However, parasite virulence might be related to the patient having had autoimmune disease since childhood and as a result having received long-term immunosuppressive therapy. The immune status of the patient was further impaired by renal insufficiency for >10 years. However, no data exist on the immune status of patients in any of the previously reported cases of infection with zoonotic Onchocerca spp. For other nematodes, e.g., Strongyloides stercoralis, a correlation between immune status of the patient and severity of disease is well established. One report describes more severe skin manifestations caused by O. volvulus in HIV patients (14).

We have identified a zoonotic infestation with an Onchocerca sp. that can cause disease in humans. The combination of impaired immunity and unusually progressing infestation highlights a new aspect of zoonotic filariasis.


Notes

Suggested citation for this article: Koehsler M, Soleiman A, Aspöck H, Auer H, Walochnik J. Onchocerca jakutensis as a causative agent of human filariasis. Emerg Infect Dis [serial on the Internet]. 2007 Nov [date cited]. Available from http://www.cdc.gov/eid/content/13/11/1749.htm

Acknowledgments

We thank Odile Bain and Silvio Pampiglione for helpful comments.

Ms Koehsler is a research assistant and a doctoral student at the Department of Medical Parasitology of the Medical University of Vienna. Her research interests include the molecular biology of parasites.


References
1. . SiegenthalerR, GublerRParaarticulares Nematodengranulom (einheimische Onchocerca).Schweiz Med Wochenschr. Year: 1965;95:1102–45843203
2. . BeaverPC, HornerGS, BilosJZZoonotic onchocercosis in a resident of Illinois and observations on the identification of Onchocerca species.Am J Trop Med Hyg. Year: 1974;23:595–6074847039
3. . TakaokaH, BainO, UniS, KorenagaM, TadaK, IchikawaH, et al. Human infection with Onchocerca dewittei japonica, a parasite from wild boar in Oita, Japan.Parasite. Year: 2001;8:261–311584758
4. . PampiglioneS, VakalisN, LyssimachouA, KouppariG, OrihelTCSubconjunctival zoonotic Onchocerca in an Albanian man.Ann Trop Med Parasitol. Year: 2001;95:827–3210.1080/0003498012011116311784437
5. . KöhslerM, LeitnerB, BlaschitzM, MichelR, AspoeckH, WalochnikJITS1 sequence variabilities correlate with 18S rDNA sequence types in the genus Acanthamoeba (Protozoa: Amoebozoa).Parasitol Res. Year: 2006;98:86–9310.1007/s00436-005-0022-x16261355
6. . Morales-HojasR, PostRJ, ShelleyAJ, Maia-HerzogM, CoscaronS, ChekeRACharacterisation of nuclear ribosomal DNA sequences from Onchocerca volvulus and Mansonella ozzardi (Nematoda: Filarioidea) and development of a PCR-based method for their detection in skin biopsies.Int J Parasitol. Year: 2001;31:169–7710.1016/S0020-7519(00)00156-911239937
7. . Morales-HojasR, ChekeRA, PostRJMolecular systematics of five Onchocerca species (Nematoda: Filarioidea) including the human parasite, O. volvulus, suggest sympatric speciation.J Helminthol. Year: 2006;80:281–9016923273
8. . KruegerA, FischerP, Morales-HojasRMolecular phylogeny of the filaria genus Onchocerca with special emphasis on Afrotropical human and bovine parasites.Acta Trop. Year: 2007;101:1–1410.1016/j.actatropica.2006.11.00417174932
9. . AnSF, FlemingKARemoval of inhibitor(s) of the polymerase chain reaction from formalin fixed, paraffin wax embedded tissues.J Clin Pathol. Year: 1991;44:924–710.1136/jcp.44.11.9241752983
10. . BainO, Schulz-KeyHThe species of Onchocerca in the red deer: redescription of O. flexuosa (Wedl, 1856) and description of O. tubingensis n.sp. and O. tarsicola n.sp [in French]. Tropenmed Parasitol. Year: 1974;25:437–494446067
11. . DemiaszkiewiczAWRedescription of Onchocerca jakutensis (Gubanov, 1964) (Nematoda, Filaroideaea).Acta Parasitologica Polonica.Year: 1993;38:124–7
12. . Schulz-KeyHStudies on the Filariidae of Cervidae in southern Germany. 2. Filariidae of the red deer (Cervus elaphus) [in German]. Tropenmed Parasitol. Year: 1975;26:348–581189029
13. . Plenge-BonigA, KromerM, ButtnerDWLight and electron microscopy studies on Onchocerca jakutensis and O. flexuosa of red deer show different host-parasite interactions.Parasitol Res. Year: 1995;81:66–7310.1007/BF009324197724516
14. . KippW, BamuhiigaJ, RubaaleTSimulium neavei–transmitted onchocerciasis: HIV infection increases severity of onchocercal skin disease in a small sample of patients.Trans R Soc Trop Med Hyg. Year: 2003;97:310–110.1016/S0035-9203(03)90157-X15228250

Figures

[Figure ID: F1]
Figure 

Transverse section of a female worm and surrounding tissue isolated from the patient (hematoxylin and eosin stained). Scale bar = 100 μm.



Tables
[TableWrap ID: T1] Table 1  Sequence similarities in the NADH dehydrogenase subunit 5 gene in the Onchocerca sp. isolated in this study and other Onchocerca spp.*
Species % Sequence similarity
arm duk fas fle gib gut jak lie och ram vol This study
arm 100 94.03 91.54 91.54 92.04–92.53 86.07–92.54 92.04 91.54–92.54 89.55–93.03 81.59 93.03–94.03 92.04
duk 100 94.53 92.54 96.51–97.01 92.04–96.51 94.53 97.51–98.51 95.02–97.01 82.59 98.01–99.00 92.02
fas 100 89.05 92.04–92.53 88.56–94.03 94.53 95.02–96.02 92.04–95.52 82.59 93.53–94.53 94.53
fle 100 93.03–95.03 86.57–92.04 91.04 91.04–92.04 90.55–92.04 82.09 92.53–93.53 91.04
gib 99.5 90.05–95.02 92.04–92.54 94.03–95.52 94.03–95.52 84.08–84.58 95.52–97.01 92.04–93.54
gut 90.55–97.51 89.05–94.53 91.54–96.02 91.04–95.52 79.10–82.59 91.04–96.52 89.05–94.53
jak 100 94.53–95.52 92.54–95.02 82.09 94.03–95.02 100
lie 98.51–100 94.53–98.51 83.08–84.08 96.52–98.51 94.53–95.52
ochi 94.53–100 81.59–84.58 94.03–98.01 92.54–95.02
ram 100 83.58–84.08 82.09
vol 98.51–100 94.03–95.02
This study 100

*arm, armillata; duk, dukei; fas, fassiata; fle, flexuosa; gib, gibsoni; gut, gutturosa; jak, jakutensis; lie, lienalis; och, ochegni; ram, ramachandrini; vol, volvulus.


[TableWrap ID: T2] Table 2  Sequence similarities in the mitochondrial 16S rRNA gene in the Onchocera sp. isolated in this study and other Onchocherca spp.*
Species % Sequence similarity
arm duk fas fle gib gut jak lie och ram vol This study
arm 100 91.56 96.00 96.00 94.67 93.78–94.22 94.22 93.33-93.78 93.33–93.78 93.33 91.55–92.00 93.78
duki 100 95.56 92.00 95.56 94.67–95.11 94.67 95.11 96.89–97.33 91.11 96.89–97.33 91.11
fas 100 95.56 96.89 96.00–96.44 96.44 96.44–96.88 95.56–96.00 93.33 94.66–95.11 96.00
fle 100 94.22 94.22–94.66 95.56 93.78–94.22 92.40–92.88 93.78 92.44–92.89 95.11
gib 100 97.78–98.22 97.78 96.89–97.33 94.67 93.78 93.77–94.22 97.33
gut 99.10–100 96.89–97.33 96.00–96.89 93.33–93.77 91.56–92.00 93.33–93.78 96.89–97.33
jak 100 98.22–98.67 92.88–93.33 92.44 92.00–92.44 99.56
lie 99.56–100 93.33–93.78 92.44–92.88 92.44–92.88 97.78–98.22
och 99.56–100 91.11–91.55 97.33–98.22 93.33–93.78
ram 100 90.22–90.67 92.00
vol 99.56–100 92.44–92.89
This study 100

*arm, armillata; duk, dukei; fas, fassiata; fle, flexuosa; gib, gibsoni; gut, gutturosa; jak, jakutensis; lie, lienalis; och, ochegni; ram, ramachandrini; vol, volvulus.



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Keywords: Keywords: Onchocerca jakutensis, zoonosis, filariasis, PCR, paraffin-embedded tissue, lupus erythematosus, dispatch.

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