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Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

British Journal of Ophthalmology, 1986, 70, 536-542

Ophthalmia nodosa and the oculoglandular syndrome of Parinaud*

XAVIER MARTIN, SYLVIE UFFER, AND CLAUDE GAILLOUD From the University Eye Clinic, Lausanne, Switzerland

SUMMARY We present a case of ophthalmia nodosa and Parinaud's oculoglandular syndrome in a patient scratched by a cat six and a half months previously and who gave a positive result to an antigen test for cat scratch disease. In conjunctival swabs were also found urticarial hairs, tracheal fragments, processionary caterpillar oenocytes, and a grain of pollen. The pathogenic part played by each of these foreign bodies is discussed, as well as the possibility of the oculoglandular syndrome being due to the reactivation of a latent , the organism of cat scratch disease. So far as we know, this work provides the first description of the association of ophthalmia nodosa with the oculoglandular syndrome of Parinaud.

The hairs of certain or plants can penetrate had been scratched or had simply come into contact the conjunctiva and the cornea to produce an inflam- with cats, many other causes of the disease have been mation named ophthalmia nodosa. The severe ocular reported (Table 1). reaction is the combined effect of two separate The explanation for the unusual association in the components, one mechanical and the other toxic.' same patient of an ophthalmia nodosa and of an http://bjo.bmj.com/ The term 'ophthalmia nodosa' derives from the oculoglandular syndrome is suggested from histo- nodular conjunctival reaction.2 Depending on the pathological examination of the lesions. regions, the cause of the ophthalmia nodosa is mainly the needles of plants, such as the common burdock,'I I or urticarial hairs of some caterpillars.57 Table 1 Causes ofthe oculoglandular syndrome According to Watson and Sevel8 only six varieties of Diseases Responsible agents caterpillars are known to cause ophthalmia nodosa. on September 28, 2021 by guest. Protected copyright. and Arctia caja are found only in Frequent the British Isles, while Thaumetopoea pityocampa Cat scratch disease Unknown Schiff (pine processionary), Thaumetopoea jordana, Tularaemia Isia isabella, and Dendrolimus pini may be found in Sporotrichosis Sporothrix schenkii Occasional other countries. Two other species may be added to Tuberculosis Mycobacterium these, namely Thaumetopoea pinivora, another pine processionary, and Thaumetopoea processionnea L., Coccidioidomycosis Coccidioides immitis an oak processionary.' Furthermore, the oak pro- Rare septica Yersinia pseudo- cessionary is supposed to have a greater urticarial tuberculosis, y. enterocolitica impact than the pine caterpillar.'0 Equinia mallei The oculoglandular syndrome" is defined as a ducreyi unilateral granulo-conjunctivitis associated with one Venereal lymphogeanuloma trachomatis L, L2, L3 Listeria monocytogenes or several pretragal and/or submaxillary adeno- Actinomycosis Actinomyces israelii pathies. Although in several cases the patients either Blastomycosis Blastomyces dermatidis Mumps Paramyxovirus *A part of this work was presented as a poster at the SSO meeting, Infectious mononucleosis Epstein-Barr herpes virus Lausanne, 1984. Spotted Correspondence to Dr X Martin, Universitats-Augenklinik, Mittlere Strasse 91, 4056 Basel, Switzerland. Modified according to Chin and Hyndiuk.24 5536 Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

Ophthalmia nodosa and the oculoglandularsyndrome ofParinaud 537

Fig. 1 Characteristic aspect ofthe nodular lesions in ophthalmia nodosa. Fig. 2 Macroscopic, nodular conjunctival lesion. (H-E, scale=200 pmn). Fig. 3 Typical nodule in ophthalmia nodosa, centred by a caterpillar hair. Same slide as in Fig. 2. (H-E, scale=50 pn). http://bjo.bmj.com/ on September 28, 2021 by guest. Protected copyright.

Case report that six and a halfmonths earlier the patient had been scratched on the forehead and right eyelid by a cat. CASE HISTORY AND STATUS OF THE EYE Around mid February 1983, a few days before the A 56-year-old man, without a history of ocular beginning of the conjunctivitis of the right eye, the disease, came to our outpatient department on patient had pulled down a caterpillar nest from a pine 28 February 1983 suffering from unilateral con- in his garden without taking any precautions. junctivitis ofthe right eye since 21 February 1983. On On 18 March 1983, the right pretragal gland, examination, we observed conjunctival injection and palpable since the beginning of the disease, had marked inferior temporal chemosis but an unscathed become very enlarged and painful, measuring 5 by 7 cornea. The condition deteriorated in spite of an cm; the conjunctival lesion of the right eye remained initial treatment with neomycin and bacitracin, unchanged. Various investigations (general, ear, followed by neomycin, polymyxin B, and dexa- nose, and throat, blood tests) all gave normal results. methasone. Taking a second case history revealed The patient's condition did not improve in spite of Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

538 XavierMartin, Sylvie Uffer, and Claude Gailloud

* Fig. 4 Trachealfragments ofthe processionary caterpillarfound in the conjunctival lesion. (H-E, scale=55 pm). Fig. 5 Trachealfragments and eightoenocytes oftheprocessionary caterpillar. Sameslide as in Fig. 4. (H-E, scale=20 pm). Fig. 6 Grain ofpollenfound in the conjunctivallesion. (H-E, scale=30 pm). http://bjo.bmj.com/ on September 28, 2021 by guest. Protected copyright.

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local and general antibiotic therapy (Spiramycin 2 g lesion. On 20 June 1983 an antigen test for cat scratch daily). Consequently on 29 March 1983 we per- disease proved to be positive after 48 hours. formed an incision and drainage ofthe swollen gland. At follow-up on 25 June 1983 the patient was Examination (aerobic and anaerobiccultures) proved regarded as cured. negative, and histological examination led us to the conclusion of reticulo- lymphadenitis com- PATHOLOGY OF THE CONJUNCTIVAL LESION patible with cat scratch disease. On 1 June 1983 Macroscopically. Characteristic nodular lesion we excised the conjunctival lesion, which had not measuring 5 mm in length, 2 mm in width, and 1-5 regressed in spite of local treatment (Fig. 1). Histo- mm in height were observed. They were whitish pathological examination showed the presence of yellow in colour, firm in consistency, and not ad- granulomas containing foreign bodies, caterpillar herent below (Fig. 2). hairs, tracheal fragments, caterpillar oenocytes, and Microscopically. On light microscopy the conjunc- a grain of pollen. On 13 June 1983 a thorough tival stroma was highly infiltrated by lymphocytes in examination of the eye showed no other ocular which were found various badly delimited nodules Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

Ophthalmia nodosa and the oculoglandularsyndrome ofParinaud 539

Fig. 7 Granulomaphotographed within thepretragaladenopathy. (H-E, scale=127 pn).

made up of epithelioid cells and sometimes of giant found elsewhere on the caterpillar body were not multinucleated cells of the foreign body type. Serial urticarial and did not become detached spon- slides showed various structures-caterpillar hairs taneously. Experimental studies on the rabbit eye (Fig. 3), tracheal fragments, oenocytes (Figs. 4 and with hairs other than the urticarial ones of the 5), and a grain of pollen (Fig. 6). Although the eye did not provoke ophthalmia nodosa.'3 circumstances of the onset of this condition, the macroscopic appearance of the lesion, and its histo- TRACHEAL FRAGMENTS logical appearances were pathognomonic according The tracheal apparatus, highly developed in the to Malan,'2 we wanted to ascertain whether the caterpillar, is subdivided into a multitude of small foreign bodies found on the slides did in fact come tracheas, the smallest of which is intercellular.'4 http://bjo.bmj.com/ from processionary caterpillars. Discussion PATHOLOGY OF THE PRETRAGAL ADENOPATHY Histological examination showed a ganglionic stroma In Switzerland ophthalmia nodosa is mainly caused with micro- surrounded by histiocytes (Fig. by urticarial hairs of the pine processionary cater- 7). The histological image was compatible with cat pillar. Their urticarial hairs, constituent elements of scratch disease. the 'mirror', measure from 0-08 to 0*16 mm depend- on September 28, 2021 by guest. Protected copyright. ing on the age ofthe caterpillars. 15 Contrary to what is Morphology ofthe processionary caterpillar generally thought, the hairs surrounding the 'mirror' do not play any part in the releasing of the hairs. The caterpillars studied, Thaumetopoea pityocampa When a 'mirror' opens, the hairs are carried away by Schiff, were captured at the larval stage on a black the wind and break up at the slightest contact, thus pine (Pinus nigra) in mid November 1983. Scanning releasing an unknown urticarial substance.'6 When electron and light microscopic examination allowed the urticarial hairs penetrate the eye by an as us to compare and recognise the various foreign yet unknown means,'7 "' they cause various complica- bodies found in the conjunctival swab. tions, such as hypopyon ulceration, iritis, irido- cyclitis, cataract, and even retinal detachment.'9-2' THE INSECT EYE AND URTICARIAL HAIRS The eyelid and conjunctival lymphatic drainage is Urticarial hairs are implanted on the facets of the carried out by means of the pretragal glands for the insect 'mirror',* including two small posterior and external part and by the submaxillary glands for the two large anterior facets (Figs. 8 and 9). The hairs internal part.22 In this case the lesion situated in the conjunctival sac near the external angle is therefore *'Mirror' or group of papillae (Beille, 1896), cited by Pesce H, Delgado A. Poisoning from adult and caterpillars. In: related to the pretragal adenopathy, described as Bicherl W, Buckley EE, eds. Venomous and the venoms. Parinaud's oculoglandular syndrome. However, so New York: Academic Press, 1971; 3: 142. far as we know, ophthalmia nodosa has never been Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

540 Xavier Martin, Sylvie Uffer, and Claude Gailloud

Fig. 8 Open mirror ofthepine processionary caterpillar Thaumetopoea pityocampa Schiff (larvalstage L4). Scanning electron microscopy. (Electron Microscopy Center ofthe Medical Faculty, Lausanne University. Scale=J mm). Fig. 9 Urticarialhairs. Enlargement ofa bunch ofhairs on the left upperfacet ofthe mirror shown in Fig. 8. (Scale=100 pum). http://bjo.bmj.com/ on September 28, 2021 by guest. Protected copyright.

described in association with an oculoglandular syn- review of the entomological literature,'42"' and from drome,382"4 nor has the oculoglandular syndrome, a comparison between the conjunctival and cater- with cat scratch disease as its most frequent cause, pillar slides. Oenocytes are cells of ectodermal ever been described as appearing later than the sixth origin, usually found in chain formation on the week after the scratching.2"' Thus we realise that caterpillar walls3' in the vicinity of the trachea.'4 The pretragal adenopathy is related not only to caterpillar oenocytes produce lipoprotein, probably carried by hairs but also to some other pathogenic element, such oenocytoids. These lipoproteins are necessary for the as tracheal fragments, oenocytes, pollen, the cat formation of the caterpillar's cuticle.32 Are the scratch disease agent, or another. oenocytes and their lipoproteins the responsible antigens or co-antigens in causing the adenopathy? If TRACHEAL FRAGMENTS AND OENOCYTES this were so, the association would probably be It was possible to identify tracheal fragments and known, because when destroying a caterpillar nest oenocytes found in conjunctival tissue through a one is exposed to hairs as wells as to fragments. Br J Ophthalmol: first published as 10.1136/bjo.70.7.536 on 1 July 1986. Downloaded from

Ophthalmia nodosa andthe oculoglandularsyndrome ofParinaud 541

POLLEN sich bildenden tuberkelartigen Knotchen. In: Donders FC, Hess W, Zehender W, eds. Bericht uber die funfzehnte Ver- Even though the patient had several types ofallergy- sammiung der Ophthalmologischen Gesellschaft, Heidelberg. for example, to and -we Rostock: Universitats-Buchdrucherei von Adler's Erben, 1883: think it most improbable that a black-pine pollen 176-81. grain could be the cause of the oculoglandular 7 Lawford JB. Ophthalmic nodosa. Trans Ophthalmol Soc UK and tests 1895; 15: 210-29. syndrome. Clinical laboratory possibly 8 Watson PG, Sevel D. Ophthalmia nodosa. Br J Ophthalmol failed to reveal some other pathogenic agent, con- 1966; 50: 209-17. tracted by the patient at the same time or transmitted 9 Berman E. Un cas d'ophtalmia nodosa. These, Univ. de by the caterpillar fragments. Lausanne, Clinique Ophtalmologique, 1928. 10 Balachowsky AS. Famille des Notodantidae (=Ceruridae) In: Balachowsky AS, ed. Entomologie applique a l'agriculture, OTHER PATHOGENIC ELEMENTS Lgpidopteres 1972; 2: 1248-52. It is seldom that a second pathogenic agent is 11 Parinaud H. Conjonctivite infectieuse paraissant transmise a associated with the hairs of the processionary cater- l'homme par les animaux. Recueil Ophtal Soc d'Ophtal de Paris case was one described by 1889; 11:176. pillar. The only reported 12 Malan P. Lesions oculaires dues aux poils de chenille. Clin Rhoner and Huber,33 who, after having enucleated Ophtalmol 1981; 3: 229-33. an eye for aspergillosis, found a caterpillar hair in the 13 Haluska FG, Puliafito CA, Henriquez A, Albert DM. Experi- vitreous body. In the case we present here myco- mental gypsy (Lymantria dispar) ophthalmia nodosa. Arch tests to be negative. Ophthalmol 1983; 101: 799-801. logical proved 14 Snodgrass RE. The oenocytes. In: Snodgrass RE, ed. Prin- ciples of insect morphology. New York: McGraw-Hill, 1935: CAT SCRATCH DISEASE 410. The cause of cat scratch disease is unknown, but 15 Molin G de. Les 'miroirs' urticants de la processionnaire du pin. atypical ,' chlamydia, and a herpes-like Rev zool agric apple 1963; 10-12: 107-14. 16 Fischer-Cassiot A. Essai de synthese bibliographique sur la virus35are possible. The scratches on the homolateral processionnaire du pin: Thaumetopoea pityocampa Schiff. eyelid that the patient received six and a half months Technicum Horticole de Lullier-Genve 1979: 1-119. before the ophthalmia nodosa, the histological 17 Ascher K. Raupenhaarverletzungen des Auges. Uber den appearance of the adenopathy, and the presence of a Mechanismus der Haarwanderung. Med Klin 1937; 33: 297-300. 18 Ascher KW. Mechanism of locomotion observed on caterpillar positive antigen test to cat scratch disease all suggest hairs. BrJ Ophthalmol 1968; 52: 210. the presence of this disease, whose causal agent, as in 19 Gailloud CI, Rabinowicz Th, Dufresne JJ. Catamnese d'un cas herpes , remains latent. So far as we know d'ophtalmie nodulaire (par poils de chenilles). Ophthalmologica this report provides the first description of the 1964;147:244-7. 20 Damand F. Raupenhaar-Vreitis durch Raupenhaare des association of ophthalmic nodosa and the oculo- Brombeerspinners. Klin MonatsblAugenheilkd 1968; 153:643-8. http://bjo.bmj.com/ glandular syndrome of Parinaud. 21 Augebault J-Y, Mathieu M. Accidents oculaires par poils de chenille processionnaire du pin. Bull Soc Ophtalmol Fr 1974; 74: We are very grateful to Ms Anne Fischer-Cassiot, who allowed us to 373-9. consult her most interesting work on the processionary caterpillar, 22 Warwick R. Lymphatics, In: Warwick R, ed. Eugene Wolff 's and to Mr Max Hachler for his advice, both working at the Federal anatomy of the eye and orbit. 7th ed. London: Lewis, 1981: Centre of Agronomic Research at Changins, and to Mr Alexander 218. Cotty, of the Zoological Museum of Lausanne. We also thank Dr 23 Duke-Elder S. Irritant products In: System of ophthal- Robert Brun, lecturer at the Geneva Medical Faculty, for kindly mology. London: Kimpton, 1972:14(2):1196-202. on September 28, 2021 by guest. Protected copyright. giving us the cat scratch disease antigen, Ms Madeleine Martin for 24 Chin GN, Hyndiuk RA. Parinaud oculoglandular conjunctivitis. typing the article. Ms Franqoise Sallaz for bibliographic research, In: Duane TD, Jaeger EA, eds. New York: Harper and Row, Ms Letitia van der Linden for the English translation, and Dr Phillip 1983; 4: 1-8. Hendrickson, University Eye Hospital, Basle, for proof reading the 25 Margileth AM. Cat-scratch disease as a cause of the oculo- text. glandular syndrome of Parinaud. Pediatrics 1957; 20: 1000-5. References 26 Margileth AM. Cat-scratch disease: nonbacterial regional lymphadenitis. Pediatrics 1968; 42: 803-18. 1 Havener WH, Falls HF, McReynolds WU. Burdock bur 27 Warwick WJ. The cat-scratch syndrome, many diseases or one ophthalmia. Arch Ophthalmol 1955; 53: 260-3. disease? Progr Med Virol 1967; 9: 256-301. 2 Saemisch Th. Die Krankheiten der Conjunctiva, Cornea und 28 Dewitz H. II. Wissenschaftlische Mitteilungen 1. Einige Sklera. In: Graefe-Saemisch, Handbuch der gesamten Augen- Beobachtungen, betreffend das geschlossene Tracheen-system heilkunde. Ed. 2. 1904; 5(1): 548. bei Insectlarven. ZoolAnz 1890; 13: 500-31. 3 Gredsted A. Beitrag zur Kenntnis der Verletzungen des Auges 29 Gonin J. Recherches sur la metamorphose des Lepidopteres (De durch Klettenstacheln. Z Augenheilkd 1928; 64: 357-65. la formation des appendices imaginaux dans la chenille du Pieris 4 Bruhn AM. Klinische und experimentelle Untersuchungen uber brassicae). Bull Soc Vaud Sci Nat 1894; 31: 89-139. Augenschadigungen durch Klettenhaare. Klin Monatsbl Augen- 30 Weidner H. Beitrage zu einer Monographie der Raupen mit heilkd 1938; 101: 730-41. Gifthaaren. Zangewandete Entomologie 1936; 3: 432-84. 5 Schon JMA. 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niques. London: Cambridge University Press, 1979: 312-4. 35 Corey L. Cat-scratch disease. In: Petersdorf RG, Adams RD, 33 Rhoner M, Huber 0. Aspergillus als Ursache von Erblindung. Braunwald E, Isselbacher KJ, Martin JB, Wilson JD, eds. Schweiz Med Wochenschr 1933; 63: 181-3. Harrisson's principles of internal medicine. 10th ed. New York: 34 Wear DJ, Margileth AM, Hadfield TL, Fischer GW, Schlager McGraw-Hill, 1983: 1176-7. CJ, King FM. Cat-scratch disease. A bacterial infection. Science 1983; 221: 1403-5. Acceptedforpublication 31 October 1985. http://bjo.bmj.com/ on September 28, 2021 by guest. Protected copyright.