UNUSUAL MYCOTIC INFECTION O F T H E LACRIMAL CANALICULI AND CONJUNCTIVA* H U G H C. DONAHUE,
M.D.
Boston, Massachusetts The lacrimal gland and its drainage apparatus may be subject to various pathologic abnormalities, among which are: (1) Inflammation; (2) neoplasm, largely mixed tumors involving both epithelial and connective-tissue cells; (3) cystoid dilatation of the ducts of the gland, a condition called dacryops ; and (4) atrophy of the gland as in xerophthalmia. The most common of these varying types of pathologic conditions which affect the drainage apparatus is inflammation, often times involving the lacrimal duct and sac and usually due to processes set up by pathogenic bacteria following a period of stagnation of the flow of tears resulting from partial or complete occlusion of the duct. This abnormal entity has long been recognized and the more common organisms involved in such inflammations of the tear sac are Staphylococcus albus and aureus, Streptococcus, Pneumococcus, and various diphtheroid bacilli. In addition to these agents, however, there occur somewhat infrequently infections of the lacrimal apparatus which may be attributable to certain types of fungi. It is to this group that I desire to add a most unusual example of infection of the palpebral conjunctiva, canaliculi, and lower punctum due to Aspergillus niger. REPORTS I N THE LITERATURE
Various infections of the lacrimal apparatus due to fungi have been reported in the literature since the original description by von Graefe, in 1854. The most common type of abnormality described has been concretion * Presented before a meeting of the New England Ophthalmological Society and the Massachusetts Eye and Ear Infirmary Alumni Association at Boston, November 16, 1948.
of the canaliculi due to fungus infection, the most frequently observed being Streptothrix and Leptothrix. This type of disease involving the canaliculi solely has been widely discussed in the literature ; whereas, mycotic involvement of the lacrimal sac and duct are infrequently mentioned. Reese,1 McLanahan, 2 Carsten,3 de SaintMartin, 4 Elliot,5 A. Fazakas, 6 and ValiereVialeix,9 have reported cases demonstrating mycotic concretions in the canaliculi. Talice10 and Brinkerhofr11 have also described such cases, while Fine and Waring 8 have reported two cases of obstruction of the nasolacrimal duct due to mycotic infection. Obstruction of the canaliculi and sac due to involvement by Aspergillus niger has not been previously described in the literature. In 1934, S. Fazakas 7 reported the results of a study to determine the flora which occur in normal and diseased eyes from the point of view of the incidence of fungi ; he found that, from cultures taken from the conjunctiva, cornea, lid margins, and lacrimal passages, the most frequently recovered fungi were Pénicillium, Torula, Alternaria, Schizosacchromyces hominis, Haplographium, and Aspergillus in that order. In examining case reports, however, one cannot always conclude that the sole cause of lacrimal-duct obstruction was entirely mycotic in nature; very probably bacterial infection also played a part in producing many of these conditions. In the case herein described, it seems to me that, from both clinical examination of the lacrimal apparatus prior to treatment and from laboratory studies of the material obtained after surgical removal of the obstructing tissue, the etiologic factor in this case was completely mycotic in character. Abnormalities of the eye due to fungus
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infections occur in this climate infrequently, although the occurrence and distribution of fungi is enormous. Everywhere that there is organic material, earth, or plant life, there may exist fungus growth and their nomenclature, it seems to me, is in a chaotic state. There are more than 600 various types of penicillin alone with correspondingly variegated titles ! DESCRIPTION OF ASPEEGILLUS
The fungus mold, Aspergillus, is a similar agent of infection to the mold penicillin. It is composed of 66 different types which may be differentiated from one another by means of morphology and growth characteristics in ordinary media. It is found in all parts of the world, especially in France, Germany, Italy, Australia, and North and South America; it is extremely prevalent in soil, dried vegetable matter, hay, and grain and it thrives on a small amount of moisture. In contrast to penicillin, it must have a high optimum temperature and accordingly predominates in the tropics, whereas penicillin predominates in the northern climates. This fungus is an important cause of spoilage of preserves, jellies, bread, and meats; there are only one or two species which are pathogenic to man, although many species are pathogenic to birds, insects, domestic animals, and plants. Aspergillus fumigatus is pathogenic especially to birds, and is found commonly in chickens, pigeons, and ducks, where it is a cause of some diseases which are of economic importance. It produces the so-called "brooder pneumonia" in epidemic form in chicks which can be traced to the ingestion of moldy grain and to moldy nesting material. Cattle, sheep, and horses may also develop aspergillosis of the lungs, the spores being inhaled from contaminated hay or grain. Aspergillus fumigatus and Aspergillus niger are pathogenic to man, producing inflammatory granulomatous lesions of the skin, external ear, nasal sinuses, orbit,
bronchi, lungs, and occasionally in the bones and méninges. In the tropics, man is also a victim of a form of infection which produces splenomegaly. Adults are affected more commonly than children, males more frequently than females. Infection occurs most often in those exposed to fungus spores as: (1) Bird feeders who place grain in the mouth to moisten it and incidentally inhale clouds of spores; (2) fur cleaners who use rye flour containing spores; and (3) agricultural workers exposed to dust from threshing machines. ASPERGILLUS NIGER
One of the more common species of the Aspergillus family is Aspergillus niger, which is easily recognized morphologically by high and widely spaced conidiophores terminating in high, black globular sporeheads. From these sporeheads lie radially disposed primary sterigmas, each of which bears secondary sterigmas; the conidia are black or dark brown and spiny. This species is of some importance in the spoilage of foodstuffs and grows by preference in substances rich in sugar and of an acid reaction. In regard to its effect upon the eye, the literature reveals that abnormalities may be produced in the lid margins, conjunctiva, cornea, iris, and vitreous. What happens pathologically has been most widely studied in the cornea, although entire eyes have been examined by Schirmer, Nobbe, Buchanan, and others. The usual infection of the cornea by the Aspergillus produces a rather typical clinical picture characterized by the development of a gray ulcerative necrotic area with a dull, dry surface surrounded by a yellow line of demarcation, running a very slow course and associated with hypopyon. This rare infection is carried to the eye by foreign bodies associated with earth and portions of plants to which are attached the spores of the fungus. The first case of this
MYCOTIC INFECTION OF EYE
type was reported by Leber, in 1879, who reproduced the condition experimentally in a rabbit's cornea. DESCRIPTION OF EYE INFECTION
Following the injury to the epithelium by a foreign body, a gray cloudiness develops with a dull, dry, crumbly surface around which develops a very sharply defined line of demarcation, usually yellowish in color. Very slowly, this line deepens into a gutter and finally the infiltrated areas are sloughed off, revealing an infiltrated ulcer. The active stage is associated with iritis and the formation of an hypopyon but, after the sequestrum is thrown off, healing tends to follow. Perforation is rare, but can occur. The entire process is very slow and gradual and usually symptoms are slight, although occasionally there may be considerable pain. Usually the lesion is as described but rarely it takes on a less serious form and is not central but near the' limbus. Pathologic examination shows advanced necrosis with a lesion permeated by a densely felted mycelium which forms a network of fibers. The area around the slough is densely infiltrated by a typical infiltration ring of leukocytes surrounding the lesion, while the iris and ciliary body are infiltrated with round cells. It would appear that the toxins of the fungus, when concentrated locally, cause complete necrosis, and, diffusing outward, cause chemotactically a widespread migration of cells from the entire anterior segment of the globe. One result is sufficient concentration of leukocytes around the lesion to cause a complete and sharp line of demarcation by their histolytic ferments; another, the formation of hypopyon. Only rarely does the fungus penetrate into the inner eye and invade the vitreous. Previous incidence of an infection of the conjunctiva and canaliculi due to Aspergillus niger was not discovered in the available literature, although Rosenvold,13 in 1942, reported two cases of dacryocystitis and bleph-
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aritis which he states were caused by this fungus. In one case, the source of infection was in the nose ; the other was attributed to the ear. REPORT OF CASE
This is the case of a 12-year-old white schoolgirl who consulted me because of epiphora and discoloration of the inner aspect of the lower lid of the left eye which had been present for several weeks. This child had always been in good health, and general physical examination revealed nothing abnormal. Examination of the ears, nose, and sinuses by an otolaryngologist showed no evidence of disease. Vision in the right eye was 20/20, and this eye was entirely normal. Vision in the left eye was 20/20. The upper lid was normal. Upon the lower lid in the region of the punctum, there was a discoid slightly elevated area, about 1 cm. in diameter, of brown-black color which was situated underneath the palpebral conjunctiva and which could be completely seen only by eversion of the lid. The upper punctum was normal. The lower punctum was completely occluded with a black substance which resembled the tip of a lead pencil. Pressure upon the lacrimal sac produced no discharge. There was no preauricular glandular swelling. Irrigation through the upper punctum was attempted but no fluid passed into the nose. This lesion was unique and perplexing in appearance and melanoma or angioma of the conjunctiva were considered possibilities. A very tiny incision was made under local anesthesia in the black substance located in the lower punctum and following this procedure, pressure was exerted in the tear-sac region. A sticky, tenacious, molasseslike fluid was expressed, with complete disappearance of the brownish-black discoloration of the conjunctiva. Fluid was then easily irrigated through the canaliculi and passed easily into the nose. The material expressed and the nasal washings were cultured following this
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procedure. The patient has been completely relieved of epiphora and no further symptoms have occurred. LABORATORY STUDIES
The black viscid material together with the nasal washings were submitted to Miss A. Mangiaricine, bacteriologist at the Massachusetts Eye and Ear Infirmary, and a portion was inoculated upon two Petri dishes of Sabouraud's dextrose agar. Following a period of incubation, the Sabouraud's agar plate revealed a growth of typical Aspergillus niger fungi whose morphologic characteristics were completely demonstrated. These colonies are fast growing and first appear as white filamentous growths upon the surface of the medium, but quickly become dark green and black in color as spores are produced. The diagnosis is based upon finding mycelian fragments and numerous spores upon direct examination and upon obtaining a culture showing the typical morphology of Aspergillus Niger, with conidiophores and
spore changes characteristic of this fungus. I believe that this very unusual brownishblack lesion involving the lower punctum, canaliculi, and conjunctiva was caused by the formation of a cast resulting from infection by the Aspergillus niger fungus. This fungus produced mechanical formation of the cast which in turn produced occlusion of the lower punctum ; extension of the infection to the palpebral conjunctiva occurred secondarily. SUMMARY
A case of mycotic obstruction of the lacrimal canaliculi with involvement of the palpebral conjunctiva is described with identification of the fungus Aspergillus niger as the etiologic agent. Recovery from symptoms was immediate following extrusion of a tenacious, black, viscid substance after incision of the lower punctum and pressure upon the tear sac. Prior incidence of such fungus infection has not been described in the available literature. 520 Commonwealth Avenue (15).
REFERENCES
1. Reese, W. S. : Concretions of the lacrimal canaliculus. Pennsylvania M. J., 38:772, 1945. 2. McLanahan, A. : Fungus infection of the lacrimal canaliculi. Am. J. Ophth., 19:418, 1936. 3. Carsten, P. : Fungus concretions in the lacrimal canaliculi. Ztschr. f. Augenh., 62:2S, 1927. 4. de Saint-Martin : Mycosis of the lacrimal passages. Médecine, 17 :32, 1936. 5. Elliot, A. J. : Streptothricosis of the lacrimal canaliculi. Am. J. Ophth., 24:382, 1941. 6. Fazakas, A. : Fungi found in the lacrimal canaliculi on the eyelids and in the margins of the lids. Klin. Monatsbl. f. Augenh., 104:59, 1940. 7. Fazakas, S. : Study of fungi cultured from conjunctiva, cornea, lid margin and lacrimal passages. Arch. f. Ophth., 133 :461, 1934. 8. Fine, M. and Waring, W. S. : Mycotic obstruction of the nasolacrimal duct. Arch. Ophth., 38 :39, 1947. 9. Valiere-Vialeix : Chronic conjunctivitis produced by undetected mycelian concretions of the lacrimal canaliculi : Report of Cases. Bull. Soc. d'opht. de Paris. 49:298, 1937. 10. Talice, R. V. : Primary mycotic concretions of the lacrimal canaliculi : Report of a case. Ann. de parasitol., 14:164, 1936. 11. Brinkerhoff, A. J.: Actinomycosis of the inferior canaliculus. Am. J. Ophth., 25 :978, 1942. 12. Henrici, A. T.: Molds, yeasts, and actinomycetes. New York, Wiley, 1930, p. 97. 13. Rosenvold, L. R. : Dacryocystitis and blepharitis due to infection by Aspergillus niger. Am. J. Ophth., 25 :S, 1942. 14. Adams, N. F. : Infection involving sinuses and orbit due to Aspergillus fumigatus. Arch. Surgery, 26:999, 1933. 15. Favorolo, G. : Ann. di ottal. e clin ocul., 55 :86-109, 1927. 16. Rohner, M. and Huber, C. : Aspergillus als Ursache von Erblindung., Schweiz, med. Wchnschr., 63 :181, 1933. 17. Duke-Elder, W. S. : Textbook of Ophthalmology. St. Louis, Mosby, 1938, v. 2, pp. 1941-1943.