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Epidemiology |

An Epidemiological and Clinical Study of Ocular Manifestations of CongenitalRubella Syndrome in Omani Children FREE

Rajiv Khandekar, MS (Ophth) PGDip Epi; Salah Al Awaidy, PGDip Epi; Anuradha Ganesh, MRCOphth; Shyam Bawikar, MD, MPH
[+] Author Affiliations

From the Eye and Ear Health Care Programme, Ministry of Health (DrKhandekar); Department of Disease Surveillance and Disease Control, Ministryof Health (Dr Al Awaidy); Department of Ophthalmology, Sultan Qaboos UniversityHospital (Dr Ganesh); and Department of Disease Surveillance and Disease Control,Ministry of Health (Dr Bawikar), Muscat, Oman. The authors have no relevantfinancial interest in this article.


Arch Ophthalmol. 2004;122(4):541-545. doi:10.1001/archopht.122.4.541.
Text Size: A A A
Published online

Objective  To conduct a follow-up study in patients with congenital rubella syndrome(CRS) in Oman and analyze the prevalence of ophthalmic disorders and associatedsystemic problems.

Methods  This historical prospective cohort study included review of 32 survivingpatients with CRS reported by the surveillance system in Oman from 1987 through2002. All patients underwent a complete ophthalmic examination that includedvisual acuity estimation, refraction and anterior and posterior segment evaluation,and intraocular pressure measurement. Pediatric and otorhinolaryngologic consultationswere also performed.

Results  The age-adjusted prevalence of CRS in Oman was 73.2 per million in theOmani population younger than 20 years, and the incidence was 0.6 per 1000live births. Cataract, retinitis, microphthalmos, and glaucoma were observedin 11, 16, 6, and 4 patients, respectively. Keratoconus, corneal hydrops,and spontaneous resorption of lens were found in 1 patient each. Vision testingwas possible in 16 children; 4 were bilaterally blind. Patients who had undergoneeye surgery had significantly lower visual acuity, as compared with thosewho had not undergone surgery (relative risk 2.53; 95% confidence interval,1.07-6.13). Among the 11 patients with CRS with cataract, we found hearingloss, cardiac anomalies, and neuropsychologic anomalies in 7, 4, and 6 children,respectively.

Conclusions  Congenital rubella syndrome has a wide variety of severe ophthalmicand systemic complications. High clinical vigilance for signs of CRS and regularobservation of surviving patients with CRS is desirable. In patients withcataract, the functional results of surgery, despite state-of-the-art ophthalmiccare, continue to be poor. Because of a high prevalence of visual, audiologic,and neurologic disabilities, surviving patients with CRS pose a burden onthe medical and social communities. Emphasis in management ought to be preventionof CRS through effective immunization programs.

Figures in this Article

Congenital rubella syndrome (CRS) was first described by an ophthalmologistwho linked congenital cataract to German measles infection in mothers duringpregnancy.1 Although rubella is a mild diseasein adults, when a woman contracts rubella during pregnancy, there is a riskfor transplacental transmission of the virus and development of serious complicationsin the fetus. The consequences of rubella infection in utero are the manifestationsof CRS.2 Congenital cataract, glaucoma, andpigmentary retinopathy are considered cardinal features of the syndrome, anda diagnosis of CRS can be made in their presence despite lack of laboratoryevidence.3

Patients with CRS exhibit progressive disease; patients without cataractor glaucoma in infancy might manifest them later, and patients with littleor no hearing loss initially may later become deaf. Therefore, all reportedand surviving patients with CRS need to be carefully observed for early detectionand management of new disease manifestations.4

The World Health Organization encourages its member countries to strengthentheir surveillance system for CRS to achieve global elimination of CRS by2010.5 New cases of CRS have been rare sincethe development of an attenuated vaccine in 1969 and the effective implementationof immunization programs.6 However, epidemicsof rubella continue to occur. De Owens et al7 reportedthe birth of 54 neonates with CRS in Panama in 1986. Lee et al8 reporteda resurgence of CRS in the United States in the 1990s.

The Sultanate of Oman is a member country in the Eastern MediterraneanRegion of the World Health Organization, with a high-quality surveillanceand disease control system for communicable diseases9 andaims to eliminate CRS by 2005.10 In Oman, therewas an outbreak of rubella in 1992 and 1993, and many infants born in thatyear exhibited features of CRS. Since 1994, important milestones in the controlof rubella in Oman have been achieved, notably mass vaccination of children;introduction of measles, mumps, and rubella vaccination in an immunizationschedule; and rubella immunization for all mothers after childbirth. A high-qualitysurveillance and disease control system for communicable diseases has beenestablished, and strategies have been reorganized to make surveillance ofCRS more sensitive.10

The ocular profile pertaining to congenital cataract during the 1992epidemic of rubella in Oman has been reported.11 However,limited information is available about the entire spectrum of ocular manifestationsof CRS in this cohort. We reviewed the magnitude of CRS and the ocular profilein children with CRS in Oman.

This was a historical prospective cohort study. All patients with CRSreported through the national surveillance system from January 1, 1987, throughDecember 31, 2002, formed the study population. Patients had CRS diagnosedon the basis of criteria provided by the World Health Organization.12,13

At nearly 165 primary health institutions, physicians examine the newlyborn and children at the time of their vaccination visits to assess the presenceof white pupil, nystagmus, and abnormal eyeball size. Clinically suspectedCRS cases are referred to ophthalmologists for confirmation. A newborn withany congenital anomaly is screened by a pediatrician to rule out toxoplasmosis,other agents, rubella, cytomegalovirus, and herpes simplex infection in themother and the possibility of CRS in the child. On the basis of the criteriaset by the World Health Organization, all health institutions (governmentaland private clinics) notify the Department of Disease Surveillance and DiseaseControl, Muscat, Oman, by fax of any child with CRS. This information includesthe parents' telephone number and health institution and the criteria observedfor clinically suspected CRS. The child is immediately referred to a pediatricianfor detailed examination and laboratory confirmation.

The patient is examined by a senior ophthalmologist, otorhinolaryngologicsurgeon, cardiologist, neurologist, and endocrinologist. All physicians andstaff in the specialist clinic are aware of mandatory notification of a clinicallysuspected CRS case in Oman. The cases that fulfill the CRS definition areevaluated annually for the presence of newer manifestations. Patients withCRS who cannot be offered treatment at facilities available within Oman aresent abroad for treatment at the government's expense. The tertiary childhealth care units maintain details of such cases. The information of all CRScases reported through the surveillance system and case records at secondaryand tertiary hospitals were reviewed to ensure complete enlisting of all CRScases.

For the present study, so we could determine their present status, allchildren with CRS underwent a detailed ophthalmic examination that includedevaluation of best-corrected visual acuity, slitlamp examination of the anteriorsegment, measurement of intraocular pressure, and examination of the posteriorsegment by means of indirect ophthalmoscopy through dilated pupils. B-scanultrasonography was performed for posterior segment evaluation in cases ofmedia opacities. Axial length was evaluated by means of A-scan ultrasonography.Presence of strabismus was established by performing the Hirschberg test.Children older than 6 years were tested by means of the Snellen chart. Youngerchildren were evaluated by means of the Snellen chart and Kolt test. Whenformal visual acuity testing was not possible, counting fingers or identificationof items used on a daily basis was tested at a distance of 1 m.

QUALITY ENSURANCE PROCEDURES

A national seminar was conducted by the Department of Disease Surveillanceand Disease Control to explain the revised surveillance and reporting systemfor CRS. Uniform pretested data collection forms were used. Multiple sourceswere used to ensure enrollment of all CRS cases.

DATA MANAGEMENT SYSTEM

Data were collected from regional hospitals and computed by using apretested format (Epi Info 6.0; Centers for Disease Control and Prevention,Atlanta, Ga). Predetermined checks ensured a high standard of data entry.The frequencies, percentage, and proportion of different ocular manifestationswere calculated (SPSS 9.0; SPSS Inc, Chicago, Ill), and a univariate methodof analysis was adopted for the study. The prevalence of CRS in the Omanipopulation younger than 20 years was adjusted by using an indirect standardizationmethod, for which the proportion of the global population was used.14

ETHICAL ISSUES

The permission of national and regional health administrators was obtainedto conduct this study. Patient identity was kept confidential. The resultsof the study were shared with the regional health administrators, and recommendationsto further improve the care of patients with CRS were discussed.

Thirty-two patients had clinical manifestations compatible with CRS;28 (88%) had ocular manifestations. Their sex, age group, and regional distributionare shown in Table 1. The distributionof cases of CRS in Oman according to year of birth is shown in Figure 1. More than 50% of children with CRS were born during theepidemic of 1992 and 1993. The number of boys was greater than the numberof girls, with 22 boys (69%) and 10 girls (31%) affected. The mean age ofpatients with CRS was 10.4 years (range, 3.2 to 16.4 years; SD, 3.3 years).More than one fourth of the patients resided in the mountainous southern regionof Dhofar, Oman.

Table Graphic Jump LocationTable 1. Profile of the 32 Patients With Congenital Rubella Syndromein Oman
Place holder to copy figure label and caption

Number of patients with congenital rubella syndrome (CRS) in Omanaccording to year of birth. In view of the limited study sample, nearly halfof the patients were born in 1992. From 1994, after introduction of the vaccineagainst rubella in Oman, the number of patients with CRS decreased, so ourcohort has only 3 patients born after 1995.

Graphic Jump Location

The prevalence of CRS was estimated to be 37.3 per million in the Omanipopulation younger than 20 years, and the age-specific prevalence was 73.2per million in this population. The incidence of CRS in 2002 was estimatedto be 0.6 per 1000 live births.

Systemic manifestations of CRS in Omani children are shown in Table 2. Ocular complications (28 of 32),hearing loss (23 of 32), and neurologic deficits (24 of 32) were the chiefmanifestations. Of 30 children who could be tested, 12 (38%) had cardiac anomalies.All except 1 child had undergone cardiac surgery to treat the congenital anomalies.

Table Graphic Jump LocationTable 2. Systemic Manifestations of Congenital Rubella Syndrome

The most common ocular finding was retinitis, seen in 16 patients (50%)and present in most patients in both eyes (14 of 16). Cataracts followed retinopathyin frequency (11 patients [34%]). Fifty-five percent of children with cataractshad bilateral involvement. Microphthalmos (axial length <17 mm) was notedin 6 patients (19%), and glaucoma was noted in 4 patients (12%). One caseeach of keratoconus, corneal hydrops, and spontaneous lens resorption (aphakiain the absence of surgery) were detected. No case of disciform maculopathywas found. Because of limited subgroup sample sizes, the statistical significanceof each ocular manifestation in terms of sex and other variables was not calculated.

Systemic complications among patients with congenital cataract and retinitisare shown in Table 3. Sensoryhearing loss was common among those with retinitis.

Table Graphic Jump LocationTable 3. Ocular Manifestations and Systemic Complications in CongenitalRubella Syndrome

Of the 64 eyes in the 32 patients with CRS, 18 eyes (28.1%) had undergonesurgery; their visual acuity was compared with that in the eyes that had notundergone surgery (Table 4). In30 eyes, vision testing was not possible because of poor cooperation or thechild being mentally challenged. Among those undergoing routine vision tests,visual acuity was normal in 10 eyes (16%). Five eyes (8%) had visual acuityless than 3/60, and 18 eyes (28%) had visual acuity less than 6/18 but greaterthan or equal to 3/60. The eyes that had undergone surgery had a significantlyhigher risk of visual impairment than did those that had not (relative risk,2.53; 95% confidence interval, 1.07-6.13). Observation of children who didnot cooperate for vision testing revealed that 20 eyes had some residual vision:light perception, identification of familiar objects, counting fingers closeto the face.

Table Graphic Jump LocationTable 4. Visual Acuity in Surviving Patients With Congenital RubellaSyndrome

Acquired rubella is mild and self-limiting, and infection usually produceslifelong immunity.15 Mass vaccination of childreninduces immunity in 80% to 90% of the population. In countries with effectiveimmunization programs, new cases of CRS are therefore rare.9 Unfortunately,outbreaks continue to occur, and investigation results suggest that failureto vaccinate susceptible individuals, rather than failure of the vaccine,is the major factor underlying resurgence.16 Toeliminate CRS, it is crucial to monitor the magnitude of the disease and toobserve surviving cases to manage newer complications and offer rehabilitativeservices. A study in Oman is crucial because it aims to achieve this goalby 2005.

Loss of the sample in a cohort study is always a matter of concern.17 However, the present study is unlikely to be affectedby this bias because a historical cohort was studied by using data from ahighly sensitive surveillance system. Hospitals with easy and affordable accessto child health care in Oman also ensured reporting of all cases of CRS.

The prevalence of CRS in our study is much lower than that reportedin the past in Oman and in other developing countries. During the rubellaepidemic of 1992 and 1993, the incidence of clinical CRS was 0.7 per 1000live births.11,12 The serologicallyconfirmed CRS rate in Saudi Arabia was 2.2% among children aged 1 to 14 years.18,19 The rate of CRS was 1.7 per 1000births in Jamaica and Israel, 0.9 in Sri Lanka, and 1.5 in Singapore.2 The absence of new CRS cases in Oman in the past 3years and the deaths of some patients with CRS during the epidemic in 1992could be responsible for this observation. A high rate of immunization ofchildren aged 15 months, the mass vaccination campaign in 1994 for childrenaged 15 months to 18 years, and the vaccination of mothers postpartum hasresulted in a marked decrease in CRS cases in Oman.

Ocular disease accounts for much of the effect that CRS has on the medicaland social communities,2 a finding also observedin our cohort. Among the Omani population with CRS, retinitis was the mostcommon ocular complication; however, congenital cataract and glaucoma accountedfor the most cases of visual disability. Inability to obtain fundus detailsin a number of patients may have resulted in underestimation of this complication.Congenital cataract and glaucoma were also the main reported ocular manifestationsin the past in Omani children.11 In comparisonwith the high prevalence (85%-95%) of cataract due to CRS reported in otherstudies,19,20 only 11 cases (34%)were detected in our cohort, which is difficult to explain. Isolation of virusfrom lens material might enable us to determine the strain of virus and itsaffinity for retinal tissue rather than lens tissue. We detected 1 case eachof spontaneous lens resorption, keratoconus, and corneal hydrops. These changesare reported as rare and delayed ones.19 Long-termfollow-up of CRS cases is thus justified.

The 8% (5 of 64 eyes) bilateral blindness in patients with CRS in ourstudy is much higher than the childhood blindness rate of 0.07% reported in1997.21 This finding supports the need forspecial care and periodic evaluation in this high-risk population.

Visual impairment was significantly greater in eyes that had undergoneocular surgery, mainly for cataract, as compared with those that had not undergonesurgery. Poor outcomes after cataract surgery in patients with rubella aredocumented in the literature.22,23 Inflammationand incidence of pupillary membrane, posterior synechiae, and secondary glaucomaare increased in patients with CRS. These findings have been attributed torelease of virus from the lens at the time of surgery and initiation of animmune reaction after cataract surgery.5 Thelevel of visual impairment in our patients, despite quality care free of cost,favors the argument that even though surgical and medical treatment of complicationsof CRS are available, the emphasis ought to be on prevention.12

Most patients with CRS with congenital cataract had additional nonoculardisabilities, such as hearing loss and cardiac and mental or behavioral anomalies,that compounded visual disability. Many patients with retinitis had associatedsensorineural hearing loss. Further studies are needed to confirm this association.

Few patients with CRS died during follow-up, which could be becauseof prompt management of cardiac anomalies in our cohort. Late ocular manifestationsof CRS thus can be observed, provided cardiac complication in a CRS case ismanaged effectively to increase the patient's chances of survival.

In conclusion, the prevalence of CRS is lower in Oman since 1994. Althoughocular complications were a major complication of CRS, congenital cataractwas less common than that observed in other studies. A high proportion ofvisual disability in eyes that underwent surgery, as compared with those thatdid not, needs further investigation. Effective immunization programs canprevent CRS and childhood blindness from its ocular manifestations.

Corresponding author: Rajiv Khandekar, MS (Ophth), PGDip Epi, Eyeand Ear Health Care Programme, Noncommunicable Disease Control Department,Directorate General of Health Affairs, Ministry of Health, PO Box 393, Pin113, Muscat, Oman (e-mail: rajshpp@omantel.net.om).

Submitted for publication June 19, 2003; final revision received January6, 2004; accepted January 15, 2004.

We thank the staff of the Department of Disease Surveillance and DiseaseControl, Muscat, Oman, for providing CRS case data. We also appreciate theefforts of the pediatricians, ophthalmologists, and otorhinolaryngologistswho helped in evaluating these cases. We thank the authorities in the Ministryof Health, Muscat, Oman, for their support of this study. A. Raju's assistancein data entry and Mohammed Hosammudin's sincere efforts to trace these caseswere crucial.

Gregg  NM Congenital cataract following German measles in the mother. Trans Ophthalmol Soc Aust. 1941;335- 46
Cutts  FTRobertson  SEDiaz-Ortega  JLSamuel  R Control of rubella and congenital rubella syndrome (CRS) in developingcountries, part 1: burden of disease from CRS. Bull World Health Organ. 1997;7555- 68
PubMed
Armstrong  NT The ocular manifestations of congenital rubella syndrome. Insight. 1992;1714- 16
PubMed
Sever  JLSouth  MAShaver  KA Delayed manifestations of congenital rubella. Rev Infect Dis. 1985;7 ((suppl 1)) S164- 169
PubMed Link to Article
Robertson  SEFeatherstone  DAMarta  GDGacic-Dobo  MHersh  BS Rubella and congenital rubella syndrome: global update. Rev Panam Salud Publica. 2003;14306- 315
PubMed Link to Article
Resnikoff  SParajasegaram  R Blindness prevention programmes: past, present and future. Bull World Health Organ. 2001;79222- 226
PubMed
De Owens  CSDe Espino  RT Rubella in Panama: still a problem. Pediatr Infect Dis J. 1989;8110- 115
PubMed
Lee  SHEwert  DPFredrick  PDMascola  L Resurgence of congenital rubella syndrome in the 1990s: report on missedopportunities and failed prevention policies among women of childbearing age. JAMA. 1992;2672616- 2620
PubMed Link to Article
 World Health Report Health Systems: Improving Performance.  Geneva, Switzerland World Health Organization2000;200
World Health Organization, Expanded programme on immunization: rubella outbreak, Oman. Wkly Epidemiol Rec. 1994;69333- 336
PubMed
Ministry of Health, Oman, Elimination of rubella and CRS in Oman by 2005. Community Health Dis Surveill Newsl. 2000;91- 3
Juma  AH Infantile rubella cataract in Oman. Med Newslett (Oman). 1989;627- 28
Cutts  FTBest  JSiqueira  MMRobertson  SE Guidelines for surveillance of congenital rubella syndrome and rubella. Surveillance of CRS. Available at:http://www.who.int/vaccines-documents/DocsPDF99/www9934.pdf Accessed February 4, 2004.
 The Sex and Age Distribution of the World Populations: The 1994Revision.  New York, NY United Nations1994;
Chin  J Control of Communicable Diseases Manual. 17 Washington, DC American Public Health Association Rubella2000;435- 440
Lindegren  MLFehrs  LJHadler  SCHinman  AR Update: rubella and congenital rubella syndrome, 1980-1990. Epidemiol Rev. 1991;13341- 348
PubMed
Mayrent  SedDoll  Sed Epidemiology in Medicine.  Boston, Mass Little Brown & Co1987;170- 171
Abdulla  MAJamjoom  GKarrar  ZABadreldine  AAl Jishi  NTaha  SA Sero-epidemiology of rubella in Saudi Arabia: an adapted vaccine policy. J Epidemiol Community Health. 1984;38236- 239
PubMed Link to Article
O'Neill  JF The ocular manifestations of congenital infection: a study of the earlyeffect and long-term outcome of maternally transmitted rubella and toxoplasmosis. Trans Am Ophthalmol Soc. 1998;96813- 879
PubMed
Vijayalakshmi  PKakkar  GSamprathi  ABanushree  R Ocular manifestations of congenital rubella syndrome in a developingcountry. Indian J Ophthalmol. 2002;50307- 311
PubMed
Khandekar  RMohammed  AJNegrel  ADRiyami  AA The prevalence and causes of blindness in the Sultanate of Oman: theOman Eye Study (OES). Br J Ophthalmol. 2002;86957- 962
PubMed Link to Article
Givens  KTLee  DAJones  TIlstrup  DM Congenital rubella syndrome: ophthalmic manifestations and associatedsystemic disorders. Br J Ophthalmol. 1993;77358- 363
PubMed Link to Article
Boniuk  VBoniuk  M The incidence of phthisis bulbas: a complication of cataract surgeryin the congenital rubella syndrome. Trans Am Acad Ophthalmol Otolaryngol. 1970;74360- 368
PubMed

Figures

Place holder to copy figure label and caption

Number of patients with congenital rubella syndrome (CRS) in Omanaccording to year of birth. In view of the limited study sample, nearly halfof the patients were born in 1992. From 1994, after introduction of the vaccineagainst rubella in Oman, the number of patients with CRS decreased, so ourcohort has only 3 patients born after 1995.

Graphic Jump Location

Tables

Table Graphic Jump LocationTable 1. Profile of the 32 Patients With Congenital Rubella Syndromein Oman
Table Graphic Jump LocationTable 2. Systemic Manifestations of Congenital Rubella Syndrome
Table Graphic Jump LocationTable 3. Ocular Manifestations and Systemic Complications in CongenitalRubella Syndrome
Table Graphic Jump LocationTable 4. Visual Acuity in Surviving Patients With Congenital RubellaSyndrome

References

Gregg  NM Congenital cataract following German measles in the mother. Trans Ophthalmol Soc Aust. 1941;335- 46
Cutts  FTRobertson  SEDiaz-Ortega  JLSamuel  R Control of rubella and congenital rubella syndrome (CRS) in developingcountries, part 1: burden of disease from CRS. Bull World Health Organ. 1997;7555- 68
PubMed
Armstrong  NT The ocular manifestations of congenital rubella syndrome. Insight. 1992;1714- 16
PubMed
Sever  JLSouth  MAShaver  KA Delayed manifestations of congenital rubella. Rev Infect Dis. 1985;7 ((suppl 1)) S164- 169
PubMed Link to Article
Robertson  SEFeatherstone  DAMarta  GDGacic-Dobo  MHersh  BS Rubella and congenital rubella syndrome: global update. Rev Panam Salud Publica. 2003;14306- 315
PubMed Link to Article
Resnikoff  SParajasegaram  R Blindness prevention programmes: past, present and future. Bull World Health Organ. 2001;79222- 226
PubMed
De Owens  CSDe Espino  RT Rubella in Panama: still a problem. Pediatr Infect Dis J. 1989;8110- 115
PubMed
Lee  SHEwert  DPFredrick  PDMascola  L Resurgence of congenital rubella syndrome in the 1990s: report on missedopportunities and failed prevention policies among women of childbearing age. JAMA. 1992;2672616- 2620
PubMed Link to Article
 World Health Report Health Systems: Improving Performance.  Geneva, Switzerland World Health Organization2000;200
World Health Organization, Expanded programme on immunization: rubella outbreak, Oman. Wkly Epidemiol Rec. 1994;69333- 336
PubMed
Ministry of Health, Oman, Elimination of rubella and CRS in Oman by 2005. Community Health Dis Surveill Newsl. 2000;91- 3
Juma  AH Infantile rubella cataract in Oman. Med Newslett (Oman). 1989;627- 28
Cutts  FTBest  JSiqueira  MMRobertson  SE Guidelines for surveillance of congenital rubella syndrome and rubella. Surveillance of CRS. Available at:http://www.who.int/vaccines-documents/DocsPDF99/www9934.pdf Accessed February 4, 2004.
 The Sex and Age Distribution of the World Populations: The 1994Revision.  New York, NY United Nations1994;
Chin  J Control of Communicable Diseases Manual. 17 Washington, DC American Public Health Association Rubella2000;435- 440
Lindegren  MLFehrs  LJHadler  SCHinman  AR Update: rubella and congenital rubella syndrome, 1980-1990. Epidemiol Rev. 1991;13341- 348
PubMed
Mayrent  SedDoll  Sed Epidemiology in Medicine.  Boston, Mass Little Brown & Co1987;170- 171
Abdulla  MAJamjoom  GKarrar  ZABadreldine  AAl Jishi  NTaha  SA Sero-epidemiology of rubella in Saudi Arabia: an adapted vaccine policy. J Epidemiol Community Health. 1984;38236- 239
PubMed Link to Article
O'Neill  JF The ocular manifestations of congenital infection: a study of the earlyeffect and long-term outcome of maternally transmitted rubella and toxoplasmosis. Trans Am Ophthalmol Soc. 1998;96813- 879
PubMed
Vijayalakshmi  PKakkar  GSamprathi  ABanushree  R Ocular manifestations of congenital rubella syndrome in a developingcountry. Indian J Ophthalmol. 2002;50307- 311
PubMed
Khandekar  RMohammed  AJNegrel  ADRiyami  AA The prevalence and causes of blindness in the Sultanate of Oman: theOman Eye Study (OES). Br J Ophthalmol. 2002;86957- 962
PubMed Link to Article
Givens  KTLee  DAJones  TIlstrup  DM Congenital rubella syndrome: ophthalmic manifestations and associatedsystemic disorders. Br J Ophthalmol. 1993;77358- 363
PubMed Link to Article
Boniuk  VBoniuk  M The incidence of phthisis bulbas: a complication of cataract surgeryin the congenital rubella syndrome. Trans Am Acad Ophthalmol Otolaryngol. 1970;74360- 368
PubMed

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