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Special Article |

The Ocular Complications of Smallpox and Smallpox Immunization FREE

Richard D. Semba, MD, MPH
[+] Author Affiliations

From the Wilmer Eye Institute, The Johns Hopkins University School of Medicine, Baltimore, Md. The author has no relevant financial interest in this article.


Arch Ophthalmol. 2003;121(5):715-719. doi:10.1001/archopht.121.5.715.
Text Size: A A A
Published online

Although smallpox was eradicated worldwide, concerns have been raised about the use of smallpox as a biological weapon. Plans are being considered for smallpox immunization in the United States. Variola virus, the cause of smallpox, and vaccinia virus, used in smallpox immunization, are both orthopoxviruses that are associated with serious ocular complications, including eyelid and conjunctival infection, corneal ulceration, disciform keratitis, iritis, optic neuritis, and blindness. About 5% to 9% of patients with smallpox develop ocular complications, and case-fatality rates reach 20% to 35% among unvaccinated individuals. About 10 to 20 patients develop ocular complications per 1 million smallpox immunizations, usually through autoinoculation, in which the patient transfers vaccinia from the immunization site to the eye. The risk of ocular vaccinia infection may be reduced by instructing patients and individuals in close contact with the vaccinee to wash their hands often and avoid touching the immunization site and their eyes. Topical antiviral therapy, topical steroids, and topical and oral antibiotics have been used to reduce the ocular complications of smallpox immunization. In contrast, there has been little experience with the use of these therapies for the ocular complications of smallpox.

Figures in this Article

In 1980, the World Health Assembly declared that smallpox had been eradicated worldwide.1 However, there is recent concern that smallpox might be used as a biological weapon.2 Plans are being considered for immunization against smallpox in the United States. Variola, the virus that causes smallpox, and vaccinia, the virus used in the smallpox vaccine, are both orthopoxviruses that can cause serious eye disease and blindness. The specific aims of this article are to review the epidemiology, diagnosis, and treatment of theocular complications of smallpox and smallpox immunization.

Smallpox was known nearly worldwide by the late 18th century, 3 when Edward Jenner discovered smallpox immunization.4 In the United States, smallpox immunization became compulsory in 1855, 5 and by 1948, there were no further deaths reported from smallpox.6 Between 1948 and 1965, there were 200 to 300 deaths from smallpox immunization.6 Routine smallpox immunization for children was discontinued in the United States in 1971. The World Health Organization intensified efforts to eliminate smallpox in 1967, 1 and the last naturally occurring case was found in Somalia in 1977.1 Remaining stocks of variola virus were reportedly destroyed or sent to either Atlanta, Georgia, or Moscow, Russia.7

Variola and vaccinia are closely related members of Orthopoxvirus, a genus of viruses within the family Poxviridae.8 Poxviruses are large and complex brick-shaped viruses consisting of a core of viral DNA, lateral bodies, an outer membrane containing tubular-shaped lipoprotein subunits, and an envelope.9 Poxviruses use their own set of enzymes to replicatein the cytoplasm, and these sites of replication can be seen in histologic preparations as characteristic inclusions, or "Guarnieri bodies."1 The host cell undergoes necrosis and ruptures, releasing infectious virions.

Smallpox

Smallpox is spread from person to person through aerosolized droplets from respiratory discharges, direct skin contact, and through fomites. The incubation period is 10 to 14 days, and infected individuals can communicate the disease from 1 to 2 days prior to the onset of symptoms until the rash has resolved and all scabs and crusts have been shed. The case-fatality rates are about 20% to 35% among those who have not been vaccinated.1013 Infants, pregnant women, and older adults are at higher risk of mortality from smallpox, 1012 and there is a lower risk of death among immunized individuals.10

Smallpox reportedly caused more than one third of the blindness in Europe prior to immunization, 14 and even as late as the 1960s, smallpox remained a significant cause of blindness in Africa.15 Ocular complications have been reported in about 5% to 9% of patients with smallpox. During smallpox epidemics in Vienna, 16 Italy, 17 and France, 18 the proportion of people with ocular complications was 9%, 7.2%, and 5.1%, respectively. During a smallpox epidemic in Cleveland in 1902, 1.8% of cases developed corneal ulcers.13 In a large series of smallpox cases in India, corneal ulceration developed in 1%, primarily in children younger than 14 years.10

Vaccinia

The rate of ocular complications following smallpox immunization is about 10 to 20 patients per 1 million primary immunizations. In the United States in 1963, there were 115 accidental infections (85 after primary vaccination, 8 after revaccination, and 22 in contacts), of which 103 were caused by autoinoculation of the eye.19 Most cases occurred in children aged 1 to 4 years. The rate of accidental infections was 13.6 per 1 million primary vaccinations, and eye infections comprised nearly all of the cases of accidental infection. Further surveillance in 1968 showed a rate of accidental infection of 25.1 per 1 million primary vaccinations, and ocular infections again comprised most of the accidental infections.20 Higher complication rates occur with primary immunization compared with reimmunization.19,20 The rates of ocular complications with smallpox immunization in the United States are similar to that reported in Marseille, France (23.8 per 1 million immunizations), 21 but higher than South Wales (10 per 1 million immunizations).22 Of 348 patients with ocular complications from immunization detected by the American Red Cross from 1963 to 1968, most were preschool children.23 Most had vaccinia of the eyelid or conjunctiva, and corneal involvement occurred in 6.3%.23

The eyelids are usually involved in the generalized pustular rash, and the edema, discharges, and dried secretions may be severe enough to prevent the eyelids from opening for a few days. Conjunctival pustules can occur and are accompanied by pain, photophobia, and lacrimation.16 Conjunctival phlyctenules are occasionally reported.16,24 The smallpox virus is actively secreted in tears during conjunctivitis.25 Corneal involvement usually occurs through contiguous spread of a pustule at the limbus.26 Prior to the onset of the rash, corneal infiltrates may appear that do not stain with fluorescein.27,28 Corneal ulceration is the most common serious complication of smallpox and may involve any part of the cornea13,16,2833 and result in perforation, 13,34 iris prolapse, 3436 hypopyon, 13 staphyloma, 13,24,37 and/or endophthalmitis.37 Bacterial superinfection may occur with the corneal ulceration, leading to widespread destruction of the cornea.3739 Disciform keratitis can occur late in the rash or 1 to 2 weeks after the patient has been released from quarantine, 28,33,4042 and may last for months.41,42 A corneal leukoma may follow corneal ulceration or disciform keratitis, 26,31,32 as shown in Figure 1.26

Place holder to copy figure label and caption
Figure 1.

Unilateral corneal leucoma in an adult who survived smallpox. The patient has hyperpigmented skin lesions, a common sequela of smallpox. Reprinted from reference 26, with permission from Elsevier Science.

Graphic Jump Location

Iritis, 27,33,37,38,43,44 iridocyclitis, 16 and secondary glaucoma39 may occur with smallpox. There are isolated case reports of retinitis, 45 chorioretinitis, 45 optic neuritis, 46 paralysis of accommodation, 45 paralysis of extraocular muscles, 45 retrobulbar hemorrhage with proptosis, 18,47 suppurative dacryocystitis, 16 lagophthalmos with exposure keratitis, 39 and ankyloblepharon48 associated with smallpox. There are relatively few published data on the use of topical antivirals, topical steroids, or topical and oral antibiotics for variola infection of the eye.

Clinical Findings

Ocular vaccinia is an infection of the eye or ocular adnexa that results from accidental inoculation with vaccinia virus. Accidental infection usually occurs through autoinoculation, when the patient touches the site of immunization and then rubs the eye. It can also occur among individuals who are in close contact with the vaccinee, when the virus is transferred from the site of immunization to the eye of the contact. Those who share a bed or are in close contact with a vaccinee are at higher risk of accidental infection, and the risk is also higher among individuals who have not been immunized or who have waning immunity from a previous immunization.

The most common ocular complication of smallpox immunization is vaccinia of the eyelids, often occurring 7 to 10 days after immunization.23 Eyelid vaccinia is characterized by raised, white, umbilicated pustules with a necrotic center surrounded by local erythema. Typically, a few pustules appear on the upper or lower eyelids, eyelid margins, or inner canthus (Figure 2).49 The medical literature contains at least 200 case reports of eyelid vaccinia.5058 Atypical herpes simplex infection can be confused with vaccinia pustules.59

Place holder to copy figure label and caption
Figure 2.

Vaccinia infection of the eyelids in a young boy. The umbilicated vesicles on the skin are typical of vaccinia. The clinical appearance of eyelid vaccinia can resemble orbital cellulitis. Reprinted from reference 49, with permission from Elsevier Science.

Graphic Jump Location

Vaccinia pustules may occur on the conjunctiva, either through direct inoculation or spread from an eyelid lesion.52,53,55,60 Corneal ulceration may arise in a clear cornea or adjacent to a conjunctival pustule51,6168 and can result in perforation61,63 and hypopyon.61 Disciform keratitis may occur as late as 2 to 3 months after immunization.67,6973 Other complications include interstitial keratitis with vestibuloauditory symptoms, 74 iritis, 23,75 central retinal artery occlusion, 76 pigmentary retinopathy, 77,78 chorioretinitis, 74,79 central serous retinopathy, 74 exudative retinitis, 80 optic neuritis, 79,8183 retrobulbar neuritis with encephalomyelitis, 84 transient strabismus, 85 and orbital involvement with proptosis, reduced ocular motility, and optic atrophy.86 Entropion, symblepharon, eyelid margin defects, and loss of eyelashes are some long-term sequelae of eyelid involvement.63

Diagnosis

The diagnosis of ocular vaccinia is made on the basis of a history of smallpox immunization or recent close contact with a vaccinee and the clinical appearance of pustules on the eyelid or conjunctiva. Laboratory confirmation is seldom needed, but scrapings of lesions may demonstrate the virus in chick chorioallantoic membrane cultures1 or show Guarnieri bodies on staining.87 The differential diagnosis of vaccinia of the eyelids includes hordeolum, preseptal and orbital cellulitis, atypical herpes simplex, and acute dacryocystitis.87 Vaccinia keratitis may sometimes resemble herpes simplex keratitis.

Treatment

Topical antivirals, such as idoxuridine, trifluridine, and vidarabine, are used to treat vaccinia of the cornea and conjunctiva or to prevent corneal and conjunctival involvement in patients with eyelid lesions.20,49,68,8891 Topical antiviral drops or ointments are given every 4 hours for 7 to 10 days.91 Vaccinia immune globulin is recommended for ocular vaccinia23 at doses of 0.3 to 0.5 mL/kg of body weight and repeated in 48 hours if there is no improvement.91 Topical vaccinia immune globulin (100 mg/mL) may be used every 4 hours but is contraindicated if the corneal epithelium is not intact, 91 as it may worsen corneal clouding and edema, presumably through precipitation of antigen-antibody complexes in the cornea.91,92

Topical steroid therapy may be combined with antiviral therapy for treatment of disciform keratitis if the cornea is intact and the active infection has cleared. Topical and/or oral antibiotics have been used as treatment against bacterial superinfection of the conjunctiva or cornea or as prophylactic therapy against preseptal cellulitis in patients with severe eyelid involvement.

Prevention

The risk of ocular complications may be reduced by instructing patients and individuals in close contact with the vaccinee to wash their hands often and to avoid touching the immunization site and their eyes. Individuals who have been immunized against smallpox should probably avoid contact lens use until the scab on their immunization site has resolved. Relative ophthalmologic contraindications to smallpox immunization include allergic conjunctivitis, eyelid eczema, and other pruritic eye diseases in which there may be a greater likelihood of autoinoculation or altered immunity.

Smallpox is characterized by frequent and severe ocular complications. The ocular complications of smallpox vaccination are relatively rare, but in a hypothetical situation involving mass vaccination of 100 million individuals, about 1000 to 2000 cases of ocular vaccinia might be anticipated. The risks of ocular vaccinia may be reduced by careful patient education and appropriate prophylactic therapy. Although there are few published data on newer therapies for the ocular complications of smallpox, antiviral agents used to treat ocular vaccinia may prove beneficial should smallpox become an emerging medical problem.

Submitted for publication December 4, 2002; accepted January 22, 2003.

This research was supported in part by grants RO1 HD30042 and RO1 AI45441 from the National Institutes of Health, Bethesda, Md.

Corresponding author and reprints: Richard D. Semba, MD, MPH, 550 N Broadway, Suite 700, Baltimore, MD 21205 (e-mail: rdsemba@jhmi.edu).

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Figures

Place holder to copy figure label and caption
Figure 1.

Unilateral corneal leucoma in an adult who survived smallpox. The patient has hyperpigmented skin lesions, a common sequela of smallpox. Reprinted from reference 26, with permission from Elsevier Science.

Graphic Jump Location
Place holder to copy figure label and caption
Figure 2.

Vaccinia infection of the eyelids in a young boy. The umbilicated vesicles on the skin are typical of vaccinia. The clinical appearance of eyelid vaccinia can resemble orbital cellulitis. Reprinted from reference 49, with permission from Elsevier Science.

Graphic Jump Location

Tables

References

Fenner  FHenderson  DAArita  LJezek  ZLadnyi  ID Smallpox and Its Eradication.  Geneva, Switzerland World Health Organization1988;
Shalala  D Bioterrorism: how prepared are we? Emerg Infect Dis. 1999;5492- 493
Link to Article
Hopkins  DR Princes and Peasants: Smallpox in History.  Chicago, Ill University of Chicago Press1983;
Jenner  E An Inquiry Into the Causes and Effects of the Variolæ Vaccinæ, a Disease Discovered in Some of the Western Counties of England, Particularly Gloucestershire, and Known by the Name of Cow Pox.  London, England E Jenner1798;
Parish  HJ A History of Immunization.  Edinburgh, Scotland E & S Livingstone1965;
Kempe  CH An evaluation of the risks of smallpox vaccination in the United States. J Pediatr. 1965;671017- 1022
Link to Article
Benenson  AS Smallpox: the end of the story? In:Evans  ASKaslow  RAeds.Viral Infections of Humans: Epidemiology and Control. 4th New York, NY Plenum Medical Book Co1997;
Buller  RMLPalumbo  GJ Poxvirus pathogenesis. Microbiol Rev. 1991;5580- 112
Pogo  BGTDales  S Two deoxyribonuclease activities within purified vaccinia virus. Proc Natl Acad Sci U S A. 1969;63820- 827
Link to Article
Rao  AR Smallpox.  Bombay, India Kothari Book Depot1972;
Basu  RNJezek  ZWard  NA The Eradication of Smallpox From India.  New Delhi, India World Health Organization, Southeast Asia Regional Office1979;
Foege  WHMillar  JDHenderson  DA Smallpox eradication in West and Central Africa. Bull World Health Organ. 1975;52209- 222
Baker  AR The eye complications of smallpox: some observations during the recent epidemic in Cleveland. JAMA. 1903;41645- 648
Link to Article
du Villards  JF Carron Guide Pratique Pour L'étude et le Traitement des Maladies Des Yeux.  Paris, France Société Encyclographique des Sciences Médicales1838;
McGlashan  ND Measles, malnutrition and blindness in Luapula province, Zambia. Trop Geogr Med. 1969;21157- 162
Gambarotto  G Fenomeni oculari nel vaiuolo. Ann Ottal. 1896;25312- 315
Del Monte  A Contributo allo studio delle complicanze oculari del vaiuolo. Ann Ottal. 1911;40852- 913
Painblan  Not AvailableTaconnet  G Complications oculaires de la variole. Écho Méd Nord. 1904;8361- 371
Neff  JMLane  JMPert  JHMoore  RMillar  JDHenderson  DA Complications of smallpox vaccination, I: national survey in the United States, 1963. N Engl J Med. 1967;276125- 132
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