ocular manifestations ofonchocerciasis forest area of west ... ·...

British7ournal ofOphthalmology, 1991,75, 163-169

Ocular manifestations of onchocerciasis in a rainforest area ofWest Africa

Henry S Newland, Albert T White, Bruce M Greene, Robert P Murphy, Hugh R Taylor

AbstractThe epidemiology and natural history ofonchocerciasis and its ocular complications inrain forest areas are poorly understood. Thepresent study was conducted on a rubberplantation-in a hyperendemic area in the rainforest of Liberia, West Africa, where 800persons were examined. The prevalence ofinfection was 84% overall 29% had intraocularmicrofilariae, and 2-4% were blind in one orboth eyes. Onchocerciasis was the cause of allbinocular blindness and one-third of all visualimpairment. Over halfofthe visual impairmentcaused by onchocerciasis was due to posteriorsegment diseases. Chorioretinal changes werepresent in 75% of people, and included intra-retinal pigment clumping in 52% and retinalpigment epithelium atrophy in 32%. Atrophy ofthe retinal pigment epithelium was associatedwith increasing age and severity of infection.Intraretinal pigment was strongly associatedwith anterior uveitis. There was a strongcorrelation between uveitis and the inflam-matory chorioretinal sequelae: retinitis,intraretinal pigment, subretinal fibrosis, andoptic neuropathy. These findings indicate thatconsiderable visual impairment associatedwith rain forest onchocerciasis is common andis due largely to chorioretinal disease.

Dana Center forPreventiveOphthalmology, WilmerInstitute, Johns HopkinsUniversity, Baltimore,Maryland, USAH S NewlandR P MurphyH R Taylor

Division of GeorgraphicMedicine, University ofAlabama at Birmingham,Birmingham, Alabama,USAA T WhiteB M GreeneCorrespondence to:H S Newland, MD,Flinders Medical Centre,Bedford Park,South Australia 5042,Australia.Accepted for publication16 August 1990

Onchocerciasis is a major public health problemin equatorial West Africa.' Furthermore,mortality in blind adults is, on average, three tofour times greater than of people of the same agewho can see.2 Although much has been learnedabout the systemic manifestations of the diseaseand the ocular changes in the anterior segment,especially in savanna areas,34 relatively little isknown about the epidemiology and naturalhistory of the ocular complications in rainforest areas ofWest Africa.While onchocerciasis has been known to exist

in Liberia since 1926,5 the importance of itsocular sequelae was not initially appreciated. Asmall study in 19556 found little evidence forsevere ocular disease and reported a prevalenceof infection of 40%, with 10% of patients havingocular involvement. Another report in 1958found a prevalence of infection of 69%, but nocases of blindness or obvious lesions due toonchocerciasis were found despite slit-lampexamination.7 Another study reported that 49%of adults infected with Onchocerca volvulus hadmicrofilariae in the lateral canthus of the eye, anindicator of ocular involvement.8 Subsequentstudies, however, have indicated that oncho-cerciasis is an important blinding disease inLiberia. In 1973, Frentzel-Beyme found signifi-cant ocular onchocerciasis and a blindness rate of

1 2% in the Bong Range.9 This was double therate found in areas of Liberia free of oncho-cerciasis. In 1978 Connorandcoworkersreportedchorioretinitis in 22% and a blindness prevalenceof approximately 1% in northern Liberia.'0Chorioretinitis has also been reported in a highproportion of patients studied in clinical trials inLiberia."We undertook a more detailed ocular survey of

a population in a hyperendemic area of Liberia toprovide further information on the epidemiologyand natural history of anterior and posteriorsegment ocular disease in Liberia and on riskfactors associated with those chorioretinalchanges.

Materials and methods

CENSUS AND SAMPLINGEmployees and their dependents on the LiberianAgricultural Company (LAC) Rubber Plantationin Grand Bassa County, Liberia, were chosen asthe study population. A house-by-house censusof 1997 people in 18 camps was taken, and theoffer of participation in a clinical trial was made.A census card recording name, house, camp,age, sex, tribe, and occupation was completedfor each person aged 12 years or more. Partici-pants generally, lived within walking distance ofthe examination clinic, though transport wasavailable when needed.

EXAMINATION PROCEDUREUncorrected and corrected visual acuity wastested by illiterate E chart at 6 m. If either acuitywas <6/12, it was assessed with a pinhole. Thevisual fields were tested with a clear dome Good-lite perimeter with fibre optic target. Fieldswere recorded as normal, 40-20°, 20-10O, <100residual field, or absent.

Before anterior segment examination with aTopcon SL5D slit-lamp the patient waspositioned in the head-down position for at leasttwo minutes. Then the number of live micro-filariae in the anterior chamber was counted(MfAC).On the basis of presence and extent of flare

and cells in the anterior chamber, uveitiswas graded as absent, mild, moderate, orsevere. The numbers and locations of live anddead microfilariae and punctate opacities in thecornea were recorded. Limbitis was diagnosedby the presence oflimbal vessel dilatation, limbaloedema, or white globular opacities. The severityoflimbitis was graded as absent, mild, moderate,or severe. Sclerosing keratitis was graded asabsent, limbal haze, stroma opacified, orvascularised in the nasal or temporal meridian,

163

on 26 May 2019 by guest. P

rotected by copyright.http://bjo.bm

j.com/

Br J O

phthalmol: first published as 10.1136/bjo.75.3.163 on 1 M

arch 1991. Dow

nloaded from

http://bjo.bmj.com/

Newland, White, Greene, Murphy, Taylor

with or without confluence inferiorly, or com-pletely covering the pupil. Intraocular pressurewas measured on all patients over 30 years oldwith a Goldmann applanation tonometer. Theremainder of the anterior segment structureswere examined by the slit-lamp, and any otherabnormalities were recorded.

After pupil dilatation with 1% tropicamideand 10% phenylephrine, direct and indirectophthalmoscopy was performed, and fundalabnormalities were recorded. Colour photo-graphs were taken of the Diabetic ResearchStudy fields 1, 2, 3, and 8 (nasal to disc) with aTopcon FE fundus camera.' Subsequently thephotographs were evaluated in a masked fashionwith patient identity obscured. The chorioretinalchanges were graded according to the presenceand extent ofretinal pigment epithelium atrophy,intraretinal pigment clumping, shiny and whiteintraretinal deposits, retinitis, subretinalfibrosis,and optic neuropathy (neuritis or atrophy); anyother abnormalities were also noted.A medical history was taken, and it included a

review of the dermatological, cardiovascular,nervous, and lymphatic systems. A thoroughphysical examination was also performed withparticular reference to the general appearance,location of nodules, lymphadenopathy, der-matological findings, and weight.

Skin biopsies were taken bilaterally with aHolth-type corneoscleral punch from thescapulae, upper buttocks, and calves. Thesewere individually weighed and placed in a flat-bottom microtitre plate well containing 0-1 ml oftissue culture medium (Roswell Park MemorialInstitute: RPMI) with penicillin (100 U/ml) andstreptomycin (100 ttg/mg.) Microfilariae werecounted after overnight incubation, and thedensity ofinfection was expressed as number permg of skin (MfS).

DATA ANALYSISThe analyses included: (1) simple frequencydistribution for descriptive analysis; (2) Student'st test for comparison between means; (3) X2 orFisher's exact test for comparison ofproportions;(4) Pearson's correlation for the computation ofbivariate correlation; and (5) multiple regressionfor computation of the adjusted correlationcoefficient.

Results

STUDY POPULATIONA total of 800 persons aged 12 years or morevoluntarily reported for detailed physical,parasitological, and ocular examination. Themean camp size was 111, and the mean responserate was 40%. The age and sex distribution ofthose who were examined was the same as thatfor the general population, and no obvioussources of selection bias were seen (Table 1).

PREVALENCE AND INTENSITY OF INFECTIONThe overall prevalence of infection was 84-3%(Table 2). The prevalence was uniformly high inall age groups and was similar for each sex. It was

Tdble I Age and sex distribution ofcensus and studypopulations

Age (Years) Male Female Total

Census Population12-19 280 (24-5%) 253 (29 6%) 553 (26-7%)20-29 337 (29 5) 357 (41-8%) 694 (34 8%)30-39 281 (24 6%) 185 (21-6%) 466 (23-3%)40-49 161 (14-1%) 44 (5-1%) 205(10-2%)50+ 83(7 3%) 16(1-9%) 99(5 0%)Total 1142 (100%) 855 (100%) 1997 (100%)Study population12-19 146 (28 6%) 95 (32 9%) 241 (30 1%)20-29 139 (27-2%) 96 (33 2%) 235 (29 4%)30-39 111(21-7%) 70(24-2%) 181 (22 6%)40-49 84(16-4%) 20(6 9%) 104(13-0%)50+ 31 (6-1%) 8(2 8%) 39(4*9%)Total 511 (100%) 289(100%) 800(100%)

Table 2 Prevalence and density ofinfection by age, sex, andoccupation

Number Density PrevalenceTotal tested positive MF/mg skin (%)

Total 776* 654 5-3 84-3Age12-19 229 184 4 0 80-420-29 231 199 5 1 86-230-39 175 145 55 82-940-49 103 92 8-1 89-350+ 38 34 8-8 89-5SexMale 449 424 6-5 85-0Female 277 230 3-5 83-0OccupationTapper 215 192 8-6 89-3Housewife 186 161 4-4 86-6Student 221 174 3 9 78-7Othert 154 127 5 0 82-5

*Skin snips from 24 patients were mislaid. other occupationsincluded factory workers, drivers, teachers, and nurses.

Table 3 Proportion with monocular or binocular visualimpairment by age, sex, and occupation

Total Number Blind* Low Visionteach group 793;t 19(2-4%) 10(1 3%)

Age12-19 241 2(088%) 4(1 7%)20-29 233 6(2-6%) 2 (0 9%)30-39 178 1 (0-6%) 2(1-1%)40+ 141 10(7-1%) 2(1 4%)SexMales 509 8(166%) 7(1-4%)Females 284 11(3-9%) 3(1-1%)OccupationTapper 215 4 (1-9%) 3 (1-4%)Other 578 15(2-6%) 7(1-2%)(Combined)

*Blind: vision less than 3/60 in one or both eyes. tLow vision: lessthan 6/18 to 3/60 in one or both eyes. ftSeven subjects were unableto comprehend the visual acuity test.

significantly higher in those who worked asrubber tappers (89 3%) than in those with anyother occupation (<0 02).

Density of infection increased with age, and inmales (6-5 microfilariae/mg) it was almost twicethat in females (3-5 microfilariae/mg) (Table 2).Tappers were also the most heavily infectedoccupational group (8-6 microfilariae/mg) withstudents having the lowest density (3 9 micro-filariae/mg).

BLINDNESS AND VISUAL IMPAIRMENTThe rates of blindness and visual impairmentincreased with age, with the highest ratesoccurring in people over 40 (Table 3). Therewere fewer blind males (1 6%) than blind females(3 9%). Although there was less blindness amongthe tappers (1-9%) than in other occupations(2 6%), more (1-4%) had low vision than didthose with other occupations (1 2%).

164



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/

Ocular manifestations ofonchocerciasis in a rainforest area ofWest Africa

Table 4 Prevalence ofmonocular and binocular visual impairment by cause among studypopulation

Binocular (better eye) Monocular

Blind* Low vision Blind Low visionCause Number (%) Number(%) Number (%) Number (%)

Onchocerciasis 3(04) 1(0-1) 5(06) 1(0-1)Glaucoma 0 (0 0) 1 (0-1) 2 (0-3) 0 (0 0)Cataract 0(0-0) 1(0-1) 2(0-3) 1(0-1)Toxoplasmosis 0(00) 0(00) 1(0-1) 1(0-1)Trauma 0 (0 0) 0 (0 0) 4(0 5) 0 (0 0)Amblyopia 0 (0 0) 0 (0 0) 0 (0 0) 2 (0 3)Refractive error 0 (0 0) I (0-1) 0 (0 0) 0 (0 0)Other 0(00) 1(0-1) 2(03) 0(00)Total 3 (0 4) 5 (0-6) 16 (2-0) 5 (0 6)

*Blind: vision less than 3/60. tLow vision: less than 6/18 to 3/60. tOther causes include measles, bushmedicine, and corneal scarring.

Blindness is the most serious sequel of oncho-cerciasis, and the three people who werebilaterally blind (vision <3/60 in each eye) allhad lesions attributable to onchocerciasis (Table4). In addition, there were 16 people who weremonocularly blind (vision <3/60 in the worsteye), and five of these were blind from oncho-cerciasis. Seven of those with monocularblindness had some visual impairment (vision<6/18) in the fellow eye. In four of these thevisual impairment was due to onchocerciasislesions. Five subjects (0 6%) had binocular lowvision and five (0 6%) had monocular low vision.Thus 29 subjects had visual impairment in one orboth eyes. In 9 (31 0%) this was attributed toonchocerciasis, and of those in whom blindnessor low vision was due to onchocerciasis it was dueto anterior segment disease in four (40 0%) andto posterior segment disease in six (60 0%).

ANTERIOR SEGMENT FINDINGSMfAC were present in 191 (23-9%). The pre-valence of microfilariae in the anterior chamberincreased with age for both males and females(Fig 1). Live and dead microfilariae (MfC) werepresent in 13-6% of the population overall, but,except for an apparent increase in elderlywomen,there was less ofan increase with age (Fig 2). Theproportion of those with punctate cornealopacities was 19*1% overall, with no clear age orsex dependency, but again there was an increase

0,0

0

0.u

E760F00

0'

aO-

100

90

80

70

60

50

40

30

20

10

0

- Women

12-19 20-29 30-39 40-49 50+Age

Figure 2 Proportion and 95% confidence limits ofthose withmicrofllariae in the cornea.

in prevalence in the older women (Fig 3).Sclerosing keratitis had an overall prevalence of5% and was more common in the older subjects(Fig 4).

POSTERIOR SEGMENT FINDINGSChorioretinal changes were present in 596(76 2%) of 782 subjects with readable fundusphotographs (Fig 5-11). The commonest changewas intraretinal pigment (IRP), which occurredin 405 patients (51 8%), while retinal pigmentepithelium atrophy was found in 251 (32-1%).Less common were white intraretinal deposits in168 (21-4%) and shiny intraretinal deposits in 79(10*1%) of the patients (Table 5). On univariateanalysis atrophy of retinal pigment epitheliumwas correlated with age, MfC, punctate cornealopacities, total number of nodules, MfS,sclerosing keratitis, and being a tapper. Age andMfC remained significantly correlated in multi-variate analysis after controlling for other riskfactors (p<0 05). Subretinal fibrosis and opticneuropathy were both associated with increasingage. Subretinal fibrosis, optic neuropathy, IRP,and retinitis were all associated with uveitis, andthe correlation persisted for IRP and retinitisafter multivariate analysis. IRP was also found inthose with MfAC and a skin rash. Retinitis was

00 r

90

80

l00 r

lI

70 _

60

50

40

30

20

10

0I I I

12-19 20-29 30-39 40-49 50+

AgeFigure I Proportion and 95% confidence limits ofthose withmicrofilariae in the anterior chamber.

90to0.

.-80

700,

° 60L)

C 50-C

3 40

30c

I. 200.

10

~~IMn

_

_

u * * ..12-19 20-29 30-39 40-49 50+

AgeFigure 3 Proportion and 95% confidence limits ofthose withpunctate opacities in the cornea.

.0E0

0

c0.c0

0

0

0U.

.E

._.

-

0,0

._-

c

050.

165



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/


100

Un 90 _ I m//en I. ~ I -a- womenIo90

a, 70._

0 60

X 50- 3j 40_

2010

0 -

12-19 20-29 30-39 40-49 50+Age

Figure 4 Proportion and 95% confidence limits ofthose withsclerosing keratitis.

associated with prior treatment with diethyl-carbamazine and with limbitis. White and shinyintraretinal deposits were weakly correlated withpunctate opacities in the cornea.

All the people were classified on clinical andparasitological findings as to the overalllikelihood oftheir actually having onchocerciasis.It should be remembered that they lived in anendemic area and were highly likely to have beenexposed, if not infected. Those who had micro-filariae in either the skin or the eye were classifiedas having definite onchocerciasis; those withoutskin or ocular microfilariae but who hadpunctate corneal opacities, sclerosing keratitis,charactersitic nodules, a history of previoustreatment, or who had skin lesions consistentwith onchodermatitis were classified as havingprobable onchocerciasis. People in whom all ofthe above criteria were negative were considerednot to have onchocerciasis. Subretinal fibrosisand optic neuropathy were found only in thosewith definite onchocerciasis; retinitis, limbitis,and uveitis were found in those in the definite orprobable groups (Table 6). Interestingly, atrophy

Figure 5 Montage offundus showing discrete areas of retinal pigment epithelium atrophy(RPEA) and areas ofRPE hypertrophy in a 19-year-old male with a mean skin snip count of17 Mfilmg.

Figure 6 Severe chorioretinitis and intraretinal pigmentclumping in a 19-year-old male with a mean skin snip count of15 Mflmg.

of retinal pigment epithelium was common ineach group but more prevalent in those patientswith definite or probable onchocerciasis.There was no correlation between oncho-

cerciasis status and either age or sex, though ahigher proportion of rubber tappers hadonchocerciasis.

DiscussionOnchocerciasis was the main cause of bilateralblindness in this population. We found a highprevalence of ocular involvement and in par-ticular a high prevalence of posterior segmentchanges. The examinations were in part carriedout as a preliminary screen for clinical trial.'314This may have introduced some bias, as it ispossible that those who considered themselveshealthy might see litttle purpose in participating.Indeed, we ascertained by interview that therequisite blood samples and skin biopsies weredeterrents to participation for at least somepeople.We found a prevalence of infection of 84%.

This is higher than in a previous study in the areain 1975, which reported a prevalence of infectionof only 63%,'5 but they took fewer skin snips.During the past 10 years there have been import-ant changes in this area associated with theprogressive development of the plantation,

F r 7 A...yw.hd

Figure 7 A shiny white deposit (arrow).

166



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/

Ocular manifestations ofonchocerciasis in a rainforest area ofWestAfrica

Figure 8 Multiple white intraretinal deposits temporal to themacula in a 19-year-old male with a mean skin snip count of17 Mflmg.

which requires the recruitment of new workers,many of whom came from other hyperendemicareas.The density of infection was especially high in

males and tappers, who were also at higher riskofinfection than other occupations. The tappers,who are mostly male, work among the rubbertrees near the breeding sites and are moreexposed to the biting black flies that transmitonchocerciasis. Their clothing, often minimal,offers little protection from the flies. It isinteresting that there was not a correspondinglyhigh proportion of blind tappers. Almost para-doxically, it was the elderly females who had thehighest rate of blindness. This may be becausetappers leave the plantation when their vision isso badly affected that they are no longer able towork. On the other hand the wives or femalerelatives ofsighted male employees would remainfor as long as their husbands worked, and thiswould artificially increase the numbers ofvisuallyimpaired females.The prevalence of bilateral blindness was also

relatively low (0-4%) but it was all attributable toonchocerciasis. This rate is still twice that ofmost developed countries.16 In other studies inrain forest areas, Anderson et al reported a 2-0%blindness rate from all causes in the Cameroonrain forest, three-fourths of which was due toonchocerciasis.'7 In Liberia, Frentzel-Beyme

Figure 10 Area ofsubretinalfibrosis with overlying pigmentin a 17-year-old male patient with a mean skin snip count of6Mflmg.

reported a 1 -2% blindness rateamong 285 personsin a rural area,9 with the majority of blindnessdue to onchocerciasis. From a larger survey helater reported a 1-9% prevalence of blindness,with one-fourth attributable to onchocerciasis. 18The presence of microfilariae in the anterior

chamber (MfAC) is often taken as a measure ofocular disease in onchocerciasis, but the validityof this as an indicator is limited by the relativedifficulty in obtaining reproducible data unlessthe examination technique is standardised.19Prevalence figures for MfAC from various studiesin Liberia show considerable differences for thedata we report. Connor and coworkers foundmicrofilariae in the anterior chamber in about41% of their subjects,'" while Frentzel-Beymereported a prevalence of only 8-7%.9 This lowerfigure is almost certainly due in part to the factthat the patients were examined without previouspositioning with the head down.

In the present study, as in the Cameroon rainforest,10 older women had a higher prevalence ofcorneal microfilariae and punctate opacities.Perhaps this is because the older women remainin the population longer, but hormonal factorshave also been implicated. Anderson andcoworkers suggest that a protective role is playedby hormonal factors in females during theirreproductive years.20The prevalence of sclerosing keratitis was

higher in our Liberian study (5%) than the 1 6%

Figure 9 Advanced retinitis, IRP, RPEA, and otpicatrophy in a 30-year-oldfemale with a mean skin snip countof Figure 11 Large area ofacute retinitis in a 14-year-old111 Mflmg. patient with a mean skin snip count of9 Mflmg.

167



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/


Table S Univariate and multivariate analysis offundus abnormalities

Subretinal Optic White ShinyRPEAt fibrosis neuropathy IRPL Retinitis deposits deposits

(251)§ (8) (8) (405) (34) (168) (79)Age ( * **MfC (**) - * **Punctate ** - - - - * *

opacitiesNodule total ** - - - - **MfS * - - - - - -Sclerosing * - - - _ _ _

keratitisOccupation **

tapperUveitis - *** *** (**) (**)MfAC - - -

Skin rash - - - *Prior - - - - *

treatmentLimbitis - - - - *

*p=0.09 to 0-05. **p=0.04 to 0-01. *p<O1. ( ) Significant after multivariate analysis,controlling for other risk factors. tRetinal pigment epithelium atrophy. t:Intraretinal pigment.SNumbers in parentheses are numbers of people with fundus abnormality in one or both eyes.

prevalence found in the Cameroon rain forest.20Although the early stage of limbal haze was notclassified as sclerosing keratitis in the Cameroonstudy, when Liberian subjects with limbal hazealone were excluded the overall prevalence stillremained at 4-2%. Sclerosing keratitis was oftenseen in a milder form in the Liberian rain forestpopulation than in the savanna, and in thispopulation of largely able-bodied men it wasassociated with relatively little visual impair-ment. It was the cause of bilateral blindness inone patient, while secondary glaucoma causedblindness in another.The advanced chorioretinal abnormalities

associated with onchocerciasis have been des-cribed in detail,2' but little is known about theearlier stages of ocular involvement. A highnumber of vitreoretinal changes were reported ina study of 30 Liberian men" who were examinedin great detail with direct and indirect ophthal-moscopy, fundus photography, fluoresceinangiography, and triple-mirror contact lensexamination. Even in the present study, with asomewhat less detailed examination includingonly indirect ophthalmoscopy and fundus photo-graphy, the prevalence of chorioretinal changeswas high.The pathogenesis of the chorioretinal changes

in onchocerciasis is not clear, and many theorieshave been advanced. In 1935 Bryant suggestedthat the adult worms secrete a systemic toxinwhich affects the fundus and optic nerve.22 This

Table 6 Percentage prevalence offundus abnormalities,ocularfindings, and demographic characteristics byonchocerciasis status

Onchocerciasis status*Totalnumber Definite Probable None

Subretinal fibrosis 8 1% 0 0Optic neuropathy 7 1% 0 0Retinitis 34 5% 5% 0Limbitis/uveitis 20 3% 2% 0RPEA 248 34% 32% 22%White deposits 158 21% 20% 22%Shiny deposits 75 9% 18% 10%IRP 395 52% 52% 53%Mean age (years) 28-2 28-7 24-1Males 66% 66% 59%Rubber tapperst 21% 9% 3%Total 7564 641 44 71

*See text for grounds for classification. 4Twenty four people hadmissing MfS values and 20 had unreadable photographs. tXI test,p=0 001.

type of process would be consistent with thebilateral symmetrical nature of the disease.Bryant also suggested that microfilariae invadethe optic tract producing perivascular infiltrationand bilateral symptoms.

In 1945 Ridley concluded from his own, andother, observations that dead microfilariae in thechoroid cause occlusion of the smaller bloodvessels and atrophy of the retina.23 He alsoimplicated perivascular infiltration and endo-thelial proliferation of the short ciliary vessels inthe production of a diffuse choroidoretinaldegeneration. In 1955 Budden echoed Bryant'ssuggestion that posterior segment damage mightbe due to the effects of toxins released by adultworms.24 A combined effect of these toxins andavitaminosis A was postulated by Rodger,2"whereas Choyce suggested that onchocercalchorioretinitis was only a genetic condition.26Neumann and Gunders suggested that thechorioretinal lesion was either due to an inflam-matory reaction caused by the death of micro-flariae in situ in the posterior segment ordiffusion of toxic products from disintegratingmicrofilariae into the choroid and retina.27 Garnersuggested that the marked retinal and chorio-capillaris atrophy was attributable to a precedingchoroiditis.2"

Although the precise mechanism is unknown,the role of systemic immune processes in patho-genesis of some of the complications of oncho-cerciasis has been established.2>3' An associationbetween circulating immune complexes and theoccurrence of major ocular complications,including chorioretinitis, was reported.32Furthermore, circulating antibodies againstvarious retinal antigens, including retinal S-antigen have been demonstrated in patients withretinopathy due to onchocerciasis.33135

Donnelly and coworkers have demonstratedthat chorioretinal changes similar to those in thehuman onchocerciasis occur in a monkey modelafter the vitreal injection of 0 volvulus micro-filariae.36 They suggested that the changes couldbe directly related to the presence of micro-filariae in the retina. Microfilariae were found inthe retina adjacent to the areas of retinal pigmentepithelial changes, but with no surroundinginflammation. This would point to either apurely mechanical effect resulting from thepassage of microfilariae through the retina or tothe effect of toxins released by microfilariae. Intheir studies there was massive death of micro-filariae and possibly an accumulation ofmicrofilarial antigens, producing a change in thehost immune status. This in turn could befollowed by severe inflammation causing thetissue damage in the retina. Punctate cornealopacities, which are acute inflammatory focienveloping dead microfilariae, demonstrate asimilar chain of events in the anterior segment.We conducted a risk factor analysis to gain

further insight into the pathogenesis of some ofthe chorioretinal changes. We found a strongcorrelation between both anterior segmentdisease (live and dead microfilariae punctateopacities, and sclerosing keratitis) and systemicmarkers of cumulative disease (age, numbers ofskin microfilariae, occupation, and total numberof nodules). This suggests that similar

168



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/

169Ocular manifestations ofonchocerciasis in a rainforest area ofWest Africa

mechanisms are likely to cause both atrophy ofretinal pigment epithelium and the anteriorsegment changes. The significance of the shiny,white intraretinal deposits seen in patients withonchocerciasis in unclear. These lesions were

correlated with punctate opacities and may pointto an inflammatory aetiology. It is possible thatthey represent the retinal equivalent of thecorneal lesions and are small focal areas ofinflammation surrounding dead or dying micro-filariae; it may not be possible to determine theirexact nature until further histopathologicalmaterial is available.The impact of onchocerciasis in rain forest

areas in terms of visual impairment has oftenbeen underestimated, but our results suggest it isof considerable importance. Most posterior seg-

ment changes in onchocerciasis threaten sightand may cause irreversible damage. Furtherstudies are needed to identify risk factors forchorioretinitis in hyperendemic areas and totreat as early as possible so that some visual lossmay be prevented.

We are grateful to the following persons for their support andassistance: Dr P Noel William, Mr Ken Gerhart, and their staff ofthe Liberian Agriculture Company; Mrs Theo Greene, CaseWestern Reserve University and University Hospitals ofCleveland; and Dr E Keyvan-Larijani, Mr Sam D'Anna and MrsInga Jackman, Johns Hopkins University.

This study was supported in part by the OnchocerciasisChemotherapy Project of the FAOIUNDP/World Bank/WHOOnchocerciasis Control Programme in the Volta River Basin Area.

1 Prost A. The burden of blindness in adult males in thesavannah villages of West Africa exposed to onchocerciasis.Trans R Soc Trop Med Hyg 1986; 80: 525-7.

2 Prost A, Vaugelade J. La surmortailit6 des aveugles en zone desavaneOuest-Africaine. Bull WHO 1981; 59: 773-6.

3 Anderson J, Fait RL. Ocular onchocerciasis. In: Bulford CH,Connor DH, eds. Pathology of tropical and extraordinarydiseases. Washington: Armed Forces Institute of Parasitoi-ogy, 1976; 373-81.

4 Anderson J, Fuglsang H. Ocular onchocerciasis. TropicalDiseases Bulletin 1977; 74: 257-72.

5 Strong RP. The African Republic of Liberia and the BelgianCongo.Boston: Harvard University Press, 1930.

6 Burch TA, Qualls DM, Greenville HJ. Onchcerciasis inLiberia.Am]i TropMedHyg 1955; 4:923-9.

7 Miller MJ, Franz KN. Some clinical aspects of onchocerciasisin Liberia. Am] Trop MedHyg 1958; 7: 558-60.

8 Miller MJ, Gunders AE. Studies on onchocerciasis in Liberia.Proceedings of the Smith International Congress of TropicalMedicine and Malaria. Instituto de Medecina Tropical,Lisbon, 1958.

9 Frentzel-Beyme R. The prevalence of onchocerciasis andblindness in the population of the Bong Range, Liberia. TropMed Parasitol 1973; 24: 339-57.

10 Connor DH, Cupp EW, Ganley JP, Gibson DW, Schiller EL.Report ofstudies on onchocerciasis in Northern Liberia, includingtopical treatment with diethylcarbamazine: pathology, ophthal-mology, parasitology, and entomology; and recommendation forcontrol of the disease. American Public Health Association:1978.

11 Taylor HR, Murphy RP, Newland HS, et al. Treatment ofonchocerciasis; the ocular effects of ivermectin and diethyl-carbamazine. Arch Ophthalmol 1986; 104:863-70.

12 Diabetic Retinopathy Study Research Group. Report No. 6:Design, methods, and baseline results. Invest OphthalmolVisSci 1981; 21: 212.

13 White AT, Newland HS, Taylor HR, et al. Controlled trial anddose-finding study of ivermectin for treatment of oncho-cerciasis. 7 InfectDis 1987; 156: 463-70.

14 Newland HS, White AT, Greene BM, et al. The effect of singledose ivermectin therapy on human Onchocerca volvulusinfection and onchocercal ocular involvement. Br]7 Ophthal-mol1988;72:561-9.

15 Frentzel-Beyme R. The geographical distribution of0 volvulusinfection in Liberia. TropMed Parasitol 1975; 26: 70-87.

16 World Health Organisation. Methods of assessment of avoidableblindness. WHO Offset Publication No. 54. Geneva: WorldHealth Organisation, 1980.

17 Anderson J, Fuglsang H, Hamilton PJS, Marshall TFdeC.Studies on onchocerciasis in the United Cameroon RepublicII. Comparison of onchocerciasis in rain-forest and Sudan-Savannah. Trans R Soc Trop Med Hyg 1974; 68: 209-21.

18 Frentzel-Beyme RR. Visual impairment and incidence ofblindness in Liberia and their relation to onchocerciasis.Trop Med Parasitol 1975; 26: 469-88.

19 Thylefors B, Brinkmann UK. The microfilarial load in theanterior segment of the eye. A parameter of intensity ofonchocerciasis. Bull WHO 1977; 55: 731-7.

20 Anderson J, Fuglsang H, Hamilton PJS, Marshall TFdeC.Studies on onchocerciasis in the United Cameroon RepublicI. Comparison of populations with and without Onchocercavolvulus. Trans R Soc Trop MedHyg 1974; 68: 190-208.

21 Bird AC, Anderson J, Fuglsang H. Morphology of posteriorsegment lesions of the eye in patients with onchocerciasis. BrJ Ophthalmol 1976; 60: 2-20.

22 Bryant J. Endemic retino-choroiditis in the Anglo-Egyptianand its possible relationship to Onchocerca volvulus. Trans RSoc TropMedHyg 1935; 28: 523-32.

23 Ridley H. Ocular onchocerciasis, including an investigation inthe Gold Coast. Br] Ophthalmol 1945; suppl10.

24 Budden FH. Incidence of human infection with onchocerciasisin different communities in relation to the incidence andtype of the ocular lesions. Br] Ophthalmol 1955; 39: 321-32.

25 Rodger FC. Posterior degenerative lesion of onchocerciasis. Br_XOphthalmol 1958; 42: 21.

26 Choyce DP. IV. Some observations on the ocular complicationsof onchocerciasis and their relationship to blindness. TransRSocTropMedHyg1958;52: 112-21.

27 Neumann E, Gunders AE. The posterior segment lesion ofocular onchocerciasis. Histological aspects. Isr J Med Sci1972;8:8-9.

28 Garner A. Pathology of ocular onchocerciasis: human andexperimental. Trans R Soc Trop Med Hyg 1976; 70: 374-7.

29 Greene BM, Taylor HR, Humphrey RL. Proteinuria associatedwith diethylcarbamazine treatment of onchocerciasis. Lancet1980; i: 254-5.

30 Paghandi R, Ngu JL, Levinsky RJ. Circulating immunecomplexes in onchocerciasis. Clin Exp Immunol 1980; 39:570-5.

31 Steward MW, Sisley B, Mackenzie CD, El Sheikh H.Circulating antigen-antibody complexes in onchocerciasis.Clin Exp Immunol 1982; 48: 17-24.

32 Greene BM, Taylor HR, Brown EJ, Humphrey RL, LawleyTJ. Ocular and systemic complications of diethyl-carbamazine therapy for onchocerciasis: association withcirculating immune complexes.]_ Infect Dis 1983; 147: 890-7.

33 Newsome DA, Hewitt TA, Quinn TC, et al. Immune statusalteration in onchocerciasis, with and without retinopathy.XXV International Congress ofOphthalmology. 1986: 4.

34 Vintain P, Thillaye B, LeHoang P, Sanite-Landy J,Chanderver J, Faure JP. Sensitivity of patients with ocularonchocerciasis to filarial antigen and retinal autoantigen.Fourth International Symposium on Immunology and Immuno-pathology of the Eye 1986: 51.

35 Chan C, Nussenblatt RB, Kim MY, Palestine AG, Awadzi K,Ottesen EA. Immunopathology of ocular onchocerciasis 2:anti-retinal autoantibodies in serum and ocular fluids.Ophthalmology 1987; 94: 439-43.

36 Donnelly JJ, Taylor HR, KhatamiM, etal. Immunopathologyof onchocerciasis: ocular disease in monkeys. Invest Ophhal-mol Vis Sci 1984; 25 (suppl): 188-4.



j.com/

Br J O


arch 1991. Dow

nloaded from

http://bjo.bmj.com/

ocular manifestations ofonchocerciasis forest area of west ... ·...

Documents