This Article Extract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Narula, J. Articles by Rahimtoola, S. Search for Related Content PubMed PubMed Citation Articles by Narula, J. Articles by Rahimtoola, S. Pubmed/NCBI databases Medline Plus Health Information Cardiomyopathy Related Collections Valvular heart disease Echocardiography

(Circulation. 1999;100:1576-1581.)
© 1999 American Heart Association, Inc.

Current Perspective

Diagnosis of Active Rheumatic Carditis

The Echoes of Change

Jagat Narula, MD, PhD; Y. Chandrasekhar, MD; Shahbudin Rahimtoola, MB, FRCP

From the Division of Cardiovascular Diseases (J.N.), Hahnemann University School of Medicine, Philadelphia, Pa; University of Minnesota School of Medicine (Y.C.), Minneapolis, Minn; and University of Southern California (S.R.), Los Angeles, Calif.

Correspondence to Jagat Narula, MD, PhD, Heart Failure/Transplant Center, Hahnemann University Hospital, Broad & Vine, Mail Stop 115, Philadelphia, PA 19102. E-mail Narula{at}auhs.edu

Key Words: rheumatic heart disease • endocarditis • mitral regurgitation • arthritis • streptococcal infections

Top References

 
Not everything that counts can be counted, and not everything that can be counted counts. Albert Einstein

Acute rheumatic fever (RF) continues to be a major health problem at the dawn of the new millennium in many parts of the world.^{1 2 3} Rheumatic heart disease (RHD), the sequel of RF, is a very common cause of cardiovascular mortality and morbidity,^{1 2 3 4 5} accounts for 35% to 40% of cardiovascular disease-related hospital admissions, and is the predominant indication for cardiac surgery in developing countries.^{1 6} Although traditionally considered to be a disease associated with poverty and overcrowding, RF continues to persist, even among the prosperous middle-class population in developed countries.^{7 8 9}

Although RF is a systemic disease with multiorgan involvement, none of its manifestations, except for carditis, lead to permanent damage. Clinical cardiac involvement has been reported in nearly one-third to almost all patients with RF in various series and in up to 50% of patients in prospective studies.¹⁰ Detection of active rheumatic carditis is of great prognostic and therapeutic importance and is currently based on the Jones criteria. Not infrequently, the diagnosis of carditis by the Jones criteria becomes difficult, especially when carditis is the isolated manifestation of the disease or when the rheumatic activity occurs on preexisting RHD.^{11 12 13} It is important to develop a diagnostic strategy that will improve our ability to diagnose rheumatic carditis and allow us to apply existing criteria more efficiently.^{13 14} The advent of modern, highly sensitive cardiac imaging modalities, predominantly echocardiography/Doppler ultrasound (echo-Doppler), has raised the question whether the Jones criteria should be modified to incorporate these techniques.

Clinical Diagnosis of RF and Carditis
The Jones criteria were introduced in 1944 as a set of clinical guidelines for the diagnosis of RF.¹⁵ The manifestations of RF in the Jones criteria were divided into major and minor categories (Figure). Suggested major manifestations were least likely to lead to an improper diagnosis and included carditis, joint symptoms, subcutaneous nodules, and chorea. Historical evidence of RF or RHD also constituted a major manifestation. Minor manifestations were considered suggestive of RF but were not sufficient for the diagnosis and included clinical signs such as fever and erythema marginatum, and laboratory markers of inflammation. Presence of 2 major or 1 major and 2 minor manifestations provided reasonable evidence of rheumatic activity. However, because a previous history of definite RF or RHD was considered a major criterion, presence of minor manifestations was sufficient to establish the diagnosis of RF recurrence.

View larger version (44K): [in this window] [in a new window]   Figure 1. Evolution of Jones Criteria. The manifestations of RF are categorized into major and minor groups. Two major or 1 major and 2 minor manifestations provide reasonable evidence of rheumatic activity. Major manifestations of RF include carditis, arthritis, subcutaneous nodules, erythema marginatum, and chorea. Previous history of RF or rheumatic heart disease (RHD) was considered a major manifestation in the original criteria, and the diagnosis of recurrence required just 2 minor manifestations. The historical evidence of RF and RHD was subsequently downgraded and has recently been completely withdrawn. Joint symptoms were considered major criterion in the original version but were divided into arthralgias (subjective) and arthritis (objective); arthritis continued as a major manifestation and arthralgia was placed into minor category. The erythema marginatum was initially considered minor evidence because of low incidence but was subsequently upgraded owing to high specificity. Most importantly, preceding evidence of streptococcal infection was added to original list initially as minor criterion, but it was subsequently recommended as a prerequisite for the diagnosis of RF. Some minor, less relevant features have been dropped.

To improve specificity, these guidelines have been periodically modified.^{16 17 18 19} In the first modification,¹⁶ objectively identifiable arthritis replaced joint symptoms as a major manifestation and arthralgia was assigned to the minor category. The history of previous RF or RHD was downgraded to the minor category and therefore documentation of a major manifestation became necessary for the diagnosis of recurrence of RF. On the other hand, erythema marginatum was recommended as a major criterion. Most importantly, the evidence of preceding group A ß-hemolytic streptococcal pharyngitis was added to the list of minor manifestations in the modified Jones criteria.¹⁶ The evidence of a prior streptococcal infection was considered essential for the diagnosis of RF in the 1965 revision of the Jones Criteria, and it was suggested that exclusion of clinical syndromes of nonstreptococcal origin will further increase the accuracy of the criteria.¹⁷ The increase in specificity adversely affected the sensitivity,²⁰ and 25% of the RF cases diagnosed by modified criteria¹⁶ could not be diagnosed by revised Jones criteria.¹⁷ Such cases usually presented in the relatively late phase of the disease or with delayed manifestations of RF, when antistreptococcal antibody titers suggestive of preceding streptococcal infection had already normalized. Therefore, the late manifestations of RF were subsequently exempted from the requirement of elevated antistreptococcal antibody titers.¹⁸

In the setting of RF, diagnosis of a primary episode of carditis is based on presence of a significant apical systolic and/or basal diastolic murmur(s), clinical presence of pericarditis, or unexplained congestive heart failure. Pericarditis and congestive heart failure almost never occur in the absence of valvular involvement.¹⁰ In a recurrence of RF, rheumatic cardiac involvement almost invariably occurs if the initial episode of RF involved the heart. The term mimetic carditis was introduced to explain this phenomenon.^{21 22} For the diagnosis of carditis in a recurrence of RF, the revised Jones criteria recommended demonstration of evidence either of pericarditis or an obvious change in previous clinical cardiac findings.¹⁸ Changes in the cardiac findings included appearance of a new murmur and change in the previous murmurs or an obvious increase in cardiac size in the clinical context of RF. The diagnosis of rheumatic carditis by Jones criteria becomes difficult when carditis is the isolated manifestation of RF. This is true especially when carditis is subclinical, when it is apparent but supportive noncarditic criteria for diagnosis of RF are not fulfilled, or when the previous cardiac findings are not known for documentation of interval change in cardiac findings during the recurrence of disease.¹³ These difficulties led to a major change in the 1992 update of Jones criteria wherein the previous history of RF or RHD was excluded from the list of minor manifestations, limiting the applicability of the Jones criteria only to primary episodes of RF.¹⁹ This change represented a return to the intent of the original proposal of Jones, which did not require strict application of the criteria for the diagnosis of a recurrence of RF.¹⁵

The diagnosis of carditis therefore remains a problem, and the solution is obviously not the formulation of yet another set of clinical criteria. The development of laboratory aids of incremental diagnostic use is desirable. Because valvulitis constitutes the sine qua non of rheumatic carditis, echocardiographic documentation of valvular regurgitant lesions should, theoretically, be of significant help.

Does Echocardiography Perform Better than Clinical Examination in the Detection of Carditis?
Clinically manifest mitral regurgitation (MR) and aortic regurgitation (AR) are diagnostic of acute rheumatic carditis. The rheumatic carditis is rarely diagnosed in the absence of valve regurgitation and precordial auscultation has been the usual modality for the diagnosis of MR and AR. However, studies done even in the golden era of cardiac auscultation have shown that valvular regurgitation may not always be detected by routine clinical auscultation.^{23 24} Recent studies have shown that clinical auscultation may be a dying art,^{25 26} especially in countries where RF is declining. Not more than one third of the Internal Medicine Residency programs in the United States teach cardiac auscultation in a structured way. The residents detect significant mitral regurgitation in less than half of the cases.^{25 26} Skill levels do not significantly improve with increasing periods of clinical training;^{25 26} even cardiology fellows have not demonstrated superior diagnostic ability for the identification of cardiac murmurs.²⁶ Fifty percent of the chiefs of cardiology responded to a survey conducted in the United States in 1993; 79% agreed that after 3 years of training, many cardiology fellows are still deficient in bedside clinical skills.²⁷ The auscultatory skills have declined compared with those reported in the 1960s.²⁸ All this suggests that the clinical diagnosis of rheumatic carditis may not be made with sufficient confidence. Echo-Doppler examination identifies valvular regurgitation not detectable with clinical examination,^{7 29 30 31 32 33} allows visualization of valve structure, and allows detection of unrelated causes of valve dysfunction, such as mitral valve prolapse. It is important to note that the incremental utility of echo-Doppler would be inversely proportional to the clinical skills. In the Irvington House reports, a number of patients with no clinical evidence of cardiac involvement in the first attack of RF developed cardiac involvement on follow-up.^{23 24} A concerted effort by experienced clinicians in subsequent enrollments led to better recognition of carditis in the index attack and thus better predicted the development of residual heart disease.

In the Utah outbreak of RF, whereas carditis was confirmed by auscultation in 53 of the 74 patients (72%) with RF, Doppler evidence of MR was demonstrated in an additional 14 patients (19%) who were clinically considered to have isolated arthritis or pure chorea.⁷ In another report from the same group,³³ asymptomatic cardiac involvement was detected in 47% of RF patients presenting with polyarthritis. Folger et al, from a middle-eastern country, also demonstrated significant valvular involvement with color flow Doppler examination in the patients with RF, polyarthritis, and no clinical evidence of carditis.^{29 32} On the other hand, a large prospective study of RF from India did not find evidence of Doppler regurgitation in the patients without clinical evidence of carditis.³⁴ The discrepancy in the diagnostic utility of echo-Doppler among these studies can be best explained by the presumption that patients in developing countries seek medical attention in relatively late phase of disease, when clinical valvular involvement is well manifested. This contention is supported by a recent study from New Zealand in which Doppler evidence of valvular involvement was observed in 100% of patients with RF compared with 79% on clinical auscultation.³⁰ However, all patients with only echo-Doppler evidence of valvular regurgitation demonstrated audible murmurs in the next 2 weeks. Echo-Doppler, therefore, may allow earlier diagnosis but ultimately may not prove to be superior. In addition, the ability of echo-Doppler to detect subclinical recurrence of carditis in the presence of preexisting rheumatic heart disease remains obscure, unless there is an obvious interval change in echo-Doppler findings. This presupposes that a previous echocardiogram is available for comparison, probably an unreasonable expectation in the developing countries which bear the brunt of disease.

Can Echocardiography Reliably Differentiate Echocardiographic Valve Regurgitation (Physiological) from Minor Degrees of Pathologic Valvular Regurgitation?
Echo-Doppler evidence of trivial-to-mild valvular regurgitation is commonly observed in the normal population.³⁵ The prevalence of MR in normal people may range from 38% to 45% and that of tricuspid regurgitation from 15% to 77%.³⁶ Importantly, echo-Doppler aortic regurgitation has also been reported in normal people.³⁷ The prevalence of regurgitation in normal people may be exaggerated on color-Doppler examination. The likelihood of transient valvular regurgitation may further increase in populations suspected to have RF, such as in clinical setting of patients with polyarthralgia, who may be febrile and thus have hyperdynamic circulation. A number of studies have described the characteristics of and differences between benign valvular regurgitation and organic rheumatic valvular dysfunction.^{38 39} A holosystolic jet of MR is tacitly accepted as pathologic if it is visible in 2 echo planes and extends beyond the plane of valve leaflets.^{30 31} In the absence of a gold standard for the diagnosis of carditis, the sensitivity and specificity of these echo-Doppler findings cannot be prospectively evaluated. In the New Zealand study, although all controls who were febrile had normal echo-Doppler studies, valvular regurgitation was also seen in 2 of the 3 patients (leading to the diagnosis of carditis) who were eventually not confirmed even to have RF.³⁰ Furthermore, Doppler evidence of pulmonary and tricuspid regurgitation, reported in some studies, cannot be used to diagnose carditis because these findings are not uncommon on echo-Doppler in normal subjects^{29 32 36} and isolated involvement of these valves is unlikely in RF. Thus, although echo-Doppler is a powerful tool for diagnosing pathologic valvular regurgitation in RF, a fair amount of overlap with regurgitation in normal people (physiological) cannot be avoided.

Use of serial echocardiographic studies has been proposed to facilitate identification of organic valvular involvement.²⁹ Although documentation of persistent abnormalities, involvement of multiple valves, and disease progression may improve the specificity of abnormal echocardiographic findings, they may cause a delay in the diagnostic process. More recently, nodular structures on inflamed valves have been observed on transthoracic echocardiographic examination,³⁴ which appear to be the ultrasonic counterparts of pathologic valvular vegetations seen at autopsy and have been suggested as an evidence of carditis in RF. The utility of diagnosis of valvular nodules needs to be validated prospectively. Transesophageal echocardiography, particularly multiplane echocardiography, can be expected to demonstrate these nodules more clearly, but there is no data to support this assumption at the present time.

Can the Detection of Echo-Detectable Carditis Translate into Clinical Benefit?
An important contribution of echo-Doppler could reside in the identification of the group of patients who do not show clinical cardiac involvement during an attack of RF. In a large echocardiographic prospective study, patients without echocardiographic evidence of valvular regurgitation did not develop valve dysfunction on 6-month follow-up.³⁴ The follow-up time was short and raises the question of whether one can reassure such patients of a benign prognosis that may allow early discontinuation of secondary prophylaxis.

Although exclusion of the diagnosis of carditis can be significantly facilitated by employing echo-Doppler as a primary diagnostic modality, use of echo-Doppler for uncovering the diagnosis of subclinical carditis needs evaluation of the following issues:

1. Would the detection of subclinical carditis alter the management strategy?

Echocardiography is unlikely to modify acute management of RF regardless of whether mild carditis is present or absent. The use of corticosteroids is not indicated in patients with mild carditis and the management is limited to symptomatic treatment.

2. If management is not altered, should the finding of echocardiographic subclinical carditis help in better assessment of prognosis?

All the data of benign prognosis in patients without carditis have essentially come from clinical studies.^{23 24 40 41 42 43 44 45 46 47} If the incremental utility of echo-Doppler is indeed limited to the detection of subclinical carditis,³⁴ then a large proportion of patients with echo-detectable carditis must have been included in the low risk noncarditis group in previous clinical studies. The good prognosis in the so-called noncarditis group suggests that the included group of echo-detectable carditis probably did not suffer adversely by the misclassification. It is likely that the majority of patients with the milder forms of rheumatic carditis would resolve with adequate prophylaxis,^{23 24 40 41 42 46 47 48} and it is not certain if the additional detection of nonclinical echocardiographic carditis will be of prognostic significance. However, Folger et al found that 4 of the 6 patients with Doppler-only evidence of valve involvement continued to show valvular regurgitation 18 to 36 months later.²⁹ One of these had a normal valve on follow-up and then redeveloped an abnormality suggesting a recurrence of RF possibly related to inadequate penicillin prophylaxis.

3. If echocardiography is not likely to significantly alter either acute management or prognostication, then should it influence the long-term prophylaxis strategy?

Some of the patients without clinical carditis in an index attack do develop carditis and cardiac damage in the subsequent recurrences.²³ It is possible that these patients had suffered from subclinical carditis in the index attack which was too mild to be detected clinically. Echo-Doppler is likely to identify this subset, which would support a somewhat longer duration of secondary prophylaxis. There is no clear evidence for this scenario, however, and the American Heart Association (AHA) expert group does not presently favor the diagnosis of carditis based on Doppler echocardiography in absence of clinical criteria to support the diagnosis.^{12 49}

4. Finally, if echocardiography is used as a primary diagnostic modality, will the epidemiological face of RF be completely altered?

Unlike a 50% prevalence of carditis by clinical auscultation in patients with RF, echo-Doppler demonstrates carditis in a much larger population. How useful is a test that identifies a test characteristic in a very large proportion of the whole population? Should we just accept that carditis is a universal phenomenon in RF and dispense with routine echocardiography? Since the echo-detectable subgroup has not yet been characterized prognostically and does not radically affect the therapeutic measures, one might, with equal facility, assume that a patient has carditis unless proven otherwise instead of undertaking an echocardiogram (with its added cost) and (probably) ending up with the same long-term clinical outcome as in those identified with echocardiography. There is little evidence at present that we need to incur the cost and effort to identify subclinical disease of unclear significance notwithstanding the intellectual purity of diagnosis allowed by the use of echo-Doppler. Thus, if echo-Doppler is to be used to diagnose carditis, then fairly strict criteria must be developed (and used) that reasonably excludes valve regurgitation which can be seen in normal people.

Should Echo-Carditis Be Accepted as a Major Manifestation in the Jones Criteria in the Absence of Clinical Evidence of Carditis?
Although echo-Doppler has paramount importance in the diagnosis and management of most valvular disorders, its incorporation in the Jones criteria for the diagnosis of RF will need some caveats and can be best considered on the basis of epidemiological burden of disease and socio-economic status of various countries.

Developed Countries
Since echocardiographic is currently the best modality to identify valvular involvement, it will have a role in countries with widespread access to health care and with low burden of RF (eg, the United States). Less than 115 cases of RF were seen in the United States in 1994 and RF no longer remains a reportable disease.⁵⁰ The incidence may be higher among immigrants from developing countries who are living in lower socio-economic conditions in the United States. In this situation, the patients are almost always seen during first attacks of RF and the additional cost and workload imposed by routine echocardiograms is small and should be outweighed by its advantages. There is a significant prognostic implication of finding a normal heart or finding unrelated causes of cardiac murmurs in this population. In addition, with suboptimal auscultation skills,^{25 26} an echo-Doppler study will quickly resolve the question of whether absence of a clinically detectable murmur is truly so. This will protect patients with clinical carditis from being misclassified as patients with a more benign prognostic class and protect them from inadequate secondary prophylaxis regimens. Even if echocardiography overestimates subclinical carditis, given the good medical follow-up in these countries, serial echocardiographic studies should resolve the significance of such valve dysfunction and optimize secondary prophylaxis program. Although there is a trend toward abbreviated periods of prophylaxis in developed countries, the minimum recommended period is sufficiently long to protect patients while the significance of subclinical carditis is being resolved. Therefore, detecting subclinical carditis and even mislabeling a minority of patients with RF as having carditis for a short period of time until their clinical situation is resolved would not seem to inconvenience or overtreat the RF patients.

Developing Countries
On the other hand, the clinical scenario is strikingly different in developing countries.^{2 3 6 51} The incidence of RF and prevalence of RHD is very high, whereas access to medical care and echocardiography are limited, and the disease is more aggressive which merits prolonged prophylaxis. First attacks are rarely witnessed; many patients present with recurrences and are likely to have established heart disease. Nonrheumatic causes of valvular murmur are proportionally less common, given a wide prevalence of RHD. Physical examination is the most commonly used modality of diagnosis; clinicians encounter a large burden of valvular heart disease and are likely to keep up their auscultation skills (although this has not been tested). In the prospective echocardiographic study reported from India, clinical examination accurately triaged patients with and without cardiac involvement and echocardiography did not provide incremental diagnostic utility in a large medical center.³⁴ This diagnostic facility is not widely available in developing nations and centers equipped with such facilities are far away from majority of the rural population. Furthermore, the cost and additional workload imposed on tertiary care centers with the universal use of echocardiography in RF episodes will need to be resolved. Detecting echo-detectable rheumatic carditis is costly and probably will not change the management strategy significantly because prophylaxis is initiated in both groups, that is, in those with or without carditis. An echocardiogram could be better utilized at the time of discontinuation of prophylaxis. The AHA and World Health Organization recommend a finite period of prophylaxis,^{2 52} which is longer in patients with clinical RHD. A number of recent studies have shown that RF can recur in adults not on prophylaxis;⁵³ recurrences are higher in patients with RHD and each recurrence further damages the heart. Thus, echocardiography might have a role in the detection of RHD before discontinuation of secondary prophylaxis (because the presence of RHD at this time will constitute an indication for life-long prophylaxis).^{2 52} Echocardiography during acute attack therefore cannot be recommended as a routine modality for investigating RF in developing countries at present. It is needless to emphasize that the role of echocardiography in the diagnosis and management of established RHD remains unquestioned in any population. The AHA 1995 recommendations for duration of secondary prophylaxis indeed includes clinical or echocardiographic evidence of valvular disease.⁵⁴

Conclusions
Echocardiography/Doppler ultrasound may have a place as a major criterion in the Jones Criteria in the United States, and possibly in the other developed countries, provided strict criteria are established and are used for the diagnosis of pathological valve involvement. Jones criteria are universally used and any major alterations in their application should strongly consider that most of the patients with RF live in developing countries. Any modification in the Jones criteria that renders their implementation difficult in these countries is likely to be intellectually satisfying but practically not possible. Prospective, well-controlled studies are needed in developing countries, possibly under the sponsorship of the World Health Organization. Echo-Doppler can always be given a progressively greater role if these prospective studies demonstrate distinctly superior prognostic value of echo-detectable carditis. Dr Jones' major contribution was to create a set of criteria that was easy to use, diagnostically accurate, and applicable worldwide. There is a major need for more objective evidence of the value of echocardiography/Doppler ultrasound in this clinical situation.

	References

Top References

 
1. WHO Study Group. Rheumatic Fever and Rheumatic Heart Disease. WHO Technical Report Series No. 764. Geneva: World Health Organization; 1988.

2. Vijaykumar M, Narula J, Reddy KS, Kaplan EL. Incidence of rheumatic fever and prevalence of rheumatic heart disease in India. Int J Cardiol. 1994;43:221–228.[Medline] [Order article via Infotrieve]

3. Murray CJ, Lopez AD, eds. Global Health Statistics: A Compendium of Incidence, Prevalence and Mortality Estimates for Over 200 Conditions. Global Burden of Disease and Injury Series. Vol 2. Cambridge, Mass: Harvard School of Public Health; 1996:132–140.

4. Markowitz M. Observations on the epidemiology and preventability of rheumatic fever in developing countries. Clin Ther. 1981;4:240–251.[Medline] [Order article via Infotrieve]

5. Padmavati S. Rheumatic fever and rheumatic heart disease in developing countries. Bull World Health Organ. 1978;56:543–550.[Medline] [Order article via Infotrieve]

6. Krishnaswami S, Joseph G, Richard J. Demands on tertiary care for cardiovascular diseases in India. Analysis of data for 1960–89. Bull World Health Organ. 1991;69:325–330.[Medline] [Order article via Infotrieve]

7. Veasy LG, Wiedmeier SE, Orsmond GS, Ruttenberg HD, Boucek MM, Roth SJ, Tait VF, Thompson JA, Daly JA, Kaplan EL, Hill HR. Resurgence of acute rheumatic fever in the intermountain area of the United States. N Engl J Med. 1987;316:421–427.[Abstract]

8. Stollerman GH. Rheumatogenic group A streptococci and the return of rheumatic fever. Adv Intern Med. 1990;35:1–25.[Medline] [Order article via Infotrieve]

9. Markowitz M. Pioneers and modern ideas. Rheumatic fever—a half-century perspective. Pediatrics. 1998;102:272–274.[Free Full Text]

10. Kothari SS, Chandrashekhar Y, Tandon RK. Rheumatic carditis. In: Narula J, Virmani R, Reddy KS, Tandon R, eds. Rheumatic Fever. Washington, DC: American Registry of Pathology Publication; 1999:257–270.

11. Markowitz M. Evolution and critique of changes in the Jones criteria for the diagnosis of rheumatic fever. N Z Med J. 1988;101:392–394.[Medline] [Order article via Infotrieve]

12. Narula J, Reddy KS, Khaw BA. Can antimyosin scintigraphy supplement the Jones Criteria in the diagnosis of active rheumatic carditis? In: Khaw BA, Narula J, Strauss HW, eds. Monoclonal Antibodies in Cardiovascular Diseases. Philadelphia, Pa: Lea & Febiger; 1994.

13. Narula J, Chopra P, Talwar KK, Vasan RS, Reddy KS, Tandon R, Bhatia ML, Southern JF. Endomyocardial biopsies in acute rheumatic fever. Circulation. 1993;88:2198–2205.[Abstract/Free Full Text]

14. Bhatnagar A, Calegaro JUM, Narula J. Radionuclide imaging in acute rheumatic fever. In: Narula J, Virmani R, Reddy KS, Tandon R, eds. Rheumatic Fever. Washington, DC: American Registry of Pathology Publication; 1999:329–338.

15. Jones TD. Diagnosis of rheumatic fever. JAMA. 1944;126:481–484.[Abstract/Free Full Text]

16. Rutstein DD, Bauer W, Dorfman A, Gross RE, Lichty JA, Taussig HB, Whittemore R. Report of the Committee on Standards and Criteria for Programs of Care of the Council of Rheumatic Fever and Congenital Heart Disease of American Heart Association. Jones Criteria (Modified) for guidance in the diagnosis of rheumatic fever. Circulation. 1956;13:617–620.[Medline] [Order article via Infotrieve]

17. Stollerman GH, Markowitz M, Taranta A, Wannamaker LW, Whittemore R. Report of the Adhoc Committee on Rheumatic Fever and Congenital Heart Disease of American Heart Association: Jones Criteria (Revised) for guidance in the diagnosis of rheumatic fever. Circulation. 1965;32:664–668.[Free Full Text]

18. Shulman ST, Kaplan EL, Bisno AL, Millard HD, Amren DP, Houser H, Sanders WE Jr, Durack DT, Watanakunakorn C. Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease of the American Heart Association. Jones Criteria (Revised) for guidance in the diagnosis of rheumatic fever. Circulation. 1984;70:204A–208A.

19. Dajani AS, Ayoub E, Bierman FZ, Bisno AL, Denny FW, Durack DT, Ferreri P, Freed M, Gerber M, Kaplan EL, Karchmer AW, Markowitz M, Rahimtoola SH, Schulman ST, Taranta A, Taubert KA, Wilson W, Special writing group of the Committee on Rheumatic fever, Endocarditis and Kawasaki disease of the Council of Cardiovascular disease in the young of the American Heart Association. Guidelines for the diagnosis of rheumatic fever: Jones criteria: 1992 update. JAMA. 1992;268:2069–2073.[Abstract/Free Full Text]

20. Okuni M. Problems in clinical application of revised Jones' diagnostic criteria for rheumatic fever. Jpn Heart J. 1971;12:436–441.[Medline] [Order article via Infotrieve]

21. Feinstein AR, Spagnuolo M. Mimetic features of rheumatic fever recurrences. N Engl J Med. 1960;262:533–540.

22. Markowitz M. Evolution and critique of changes in Jones' criteria for diagnosis of acute rheumatic fever. N Z Med J. 1988;101:392–394.

23. Taranta A, Kleinberg E, Feinstein AR, Wood HF, Tursky E, Simpson R. Rheumatic fever in children and adolescents: a long-term epidemiologic study of subsequent prophylaxis, streptococcal infections, and clinical sequelae, V: relation of the rheumatic fever recurrence rate per streptococcal infection to preexisting clinical features of the patients. Ann Intern Med. 1964;60(suppl 5):58–67.

24. Feinstein AR, Stern EK, Spagnuolo M. The prognosis of acute rheumatic fever. Am Heart J. 1964;68:817–834.[Medline] [Order article via Infotrieve]

25. St. Clair EW, Oddone EZ, Waugh RA, Corey GR, Feussner JR. Assessing housestaff diagnostic skills using a cardiology patient simulator. Ann Intern Med. 1992;117:751–756.

26. Mangione S, Nieman L, Gracely E, Kaye D. The teaching and practice of cardiac auscultation during internal medicine and cardiology training. Ann Intern Med. 1993;119:47–54.[Abstract/Free Full Text]

27. Shaver JA. Cardiac auscultation: a cost-effective diagnostic skill. Curr Probl Cardiol. 1995;20:441–532.[Medline] [Order article via Infotrieve]

28. Butterworth JS, Reppert EH. Auscultatory acumen in the general medical population. JAMA. 1960;174:32–34.[Abstract/Free Full Text]

29. Folger GM, Hajar R, Robida A, Hajjar HS. Occurrence of valvar heart disease in acute rheumatic fever without evident carditis: color-flow Doppler identification. Br Heart J. 1992;67:434–439.[Abstract/Free Full Text]

30. Abernathy M, Bass N, Sharpe N, Grant C, Neutze J, Clarkson P, Greaves S, Lennon D, Snow S, Whally G. Doppler echocardiography and the early diagnosis of carditis in acute rheumatic fever. Aust N Z J Med. 1994;24:530–535.[Medline] [Order article via Infotrieve]

31. Wilson NJ, Neutze JM. Echocardiographic diagnosis of subclinical carditis in acute rheumatic fever. Int J Cardiol. 1995;50:1–6.[Medline] [Order article via Infotrieve]

32. Folger GM Jr, Hajar R. Doppler echocardiographic findings of mitral and aortic valvular regurgitation in children manifesting only rheumatic arthritis. Am J Cardiol. 1989;63:1278–1280.[Medline] [Order article via Infotrieve]

33. Veasy LG, Tani LY, Hill HR. Persistence of acute rheumatic fever in the intermountain area of the United States. J Pediatr. 1994;125:673–674.[Medline] [Order article via Infotrieve]

34. Vasan R, Shrivastava S, Vijaya Kumar K, Narang R, Lister BC, Narula J. Echocardiographic evaluation of patients with acute rheumatic fever and rheumatic carditis. Circulation. 1996;94:73–82.[Abstract/Free Full Text]

35. Brand A, Dollberg S, Keren A. The prevalence of valvular regurgitation in children with structurally normal hearts: a color Doppler echocardiographic study. Am Heart J. 1992;123:177–180.[Medline] [Order article via Infotrieve]

36. Yoshida K, Yoshikawa J, Shakuro M, Akasaka T, Jyo Y, Takao S, Shiratori K, Koizumi K, Okumachi F, Kato H, Fukaya T. Color Doppler evaluation of valvular regurgitation in normals. Circulation. 1988;78:840–847.[Abstract/Free Full Text]

37. Choong CY, Abascal VM, Weyman J, Levine RA, Gentile F, Thomas JD, Weyman AE. Prevalence of valvular regurgitation by Doppler echocardiography in patients with structurally normal hearts by two-dimensional echocardiography. Am Heart J. 1989;117:636–642.[Medline] [Order article via Infotrieve]

38. Berger M, Hecht SR, Van Tosh A, Lingam U. Pulsed and continuos wave Doppler echocardiographic assessment of valvular regurgitation in normal subjects. J Am Coll Cardiol. 1989;13:1540–1545.[Abstract]

39. Sahn DJ, Maciel BC. Physiological valvular regurgitation: Doppler echocardiography and potential for iatrogenic heart disease. Circulation. 1988;78:1075–1077.[Free Full Text]

40. United Kingdom and United States Joint Report on Rheumatic Heart Disease. The natural history of rheumatic fever and rheumatic heart disease. Ten-year report of a cooperative clinical trial of ACTH, cortisone, and aspirin. Circulation. 1965;32:457–476.[Abstract/Free Full Text]

41. Sanyal SL, Berry AM, Duggal S, Hooja V, Ghosh S. Sequelae of the initial attack of acute rheumatic fever in children from North India: a prospective 5-year follow-up study. Circulation. 1982;65:375–379.[Abstract/Free Full Text]

42. Majeed HA, Bhatnagar S, Yousof AM, Khuffash F, Yusuf AR. Acute rheumatic fever and the evolution of rheumatic heart disease: a prospective 12 year follow up report. J Clin Epidemiol. 1992;45:871–875.[Medline] [Order article via Infotrieve]

43. Feinstein AR, Stern EK. Clinical effects of recurrent attacks of acute rheumatic fever: a prospective epidemiologic study of 105 episodes. J Chronic Dis. 1967;20:13–27.[Medline] [Order article via Infotrieve]

44. Feinstein AR, Wood HF, Spagnuolo M. Rheumatic fever in children and adolescents. VII. Cardiac changes and sequelae. Ann Intern Med. 1964;60(suppl 5):87–123.

45. Majeed HA, Shaltout A, Yousof AM. Recurrences of acute rheumatic fever: a prospective study of 79 episodes. Am J Dis Child. 1984;138:341–345.[Abstract/Free Full Text]

46. Tompkins DG, Boxerbaum B, Liebman J. Long-term prognosis of rheumatic fever patients receiving regular intramuscular benzathine penicillin. Circulation. 1972;45:543–551.[Abstract/Free Full Text]

47. Majeed HA, Yousof AM, Khuffash FA, Yusuf AR, Farwana S, Khan N. The natural history of acute rheumatic fever in Kuwait: a prospective six year follow-up report. J Chronic Dis. 1986;39:361–369.[Medline] [Order article via Infotrieve]

48. Stollerman GH. Rheumatic carditis. Lancet. 1995;346:390–391.

49. Dajani A, Allen AD, Taubert KA. Echocardiography for the diagnosis and management of rheumatic fever. JAMA. 1993;269:2084–2093.

50. Summary of notifiable diseases, United States 1994. MMWR Morb Mortal Wkly Rep. 1993;43:1–80.

51. Roy SB, Bhatia ML, Lazaro EJ, Ramalingaswami V. Juvenile mitral stenosis in India. Lancet. 1963;2:1193–1196.[Medline] [Order article via Infotrieve]

52. Dajani AS, Bisno AL, Chung KJ, Durack DT, Gerber MA, Kaplan EL, Millard HD, Randolph MF, Shulman ST, Watanakunakorn C. Prevention of rheumatic fever: a statement for health professionals by the Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease of the Council on Cardiovascular Disease in the Young, the American Heart Association. Circulation. 1988;78:1082–1086.[Free Full Text]

53. Mason T, Fisher M, Kujala G. Acute rheumatic fever in West Virginia: not just a disease of children. Arch Intern Med. 1991;151:133–136.[Abstract/Free Full Text]

54. Dajani A, Taubert K, Ferrieri P, Peter G, Shulman S. Treatment of acute streptococcal pharyngitis and prevention of rheumatic fever: a statement for health professionals. Pediatrics. 1995;96:758–764.[Abstract/Free Full Text]

This article has been cited by other articles:

				F. Antonini-Canterin, E. Leiballi, R. Enache, B. A. Popescu, M. Rosca, E. Cervesato, R. Piazza, C. Ginghina, and G. L. Nicolosi Hydroxymethylglutaryl Coenzyme-A Reductase Inhibitors Delay the Progression of Rheumatic Aortic Valve Stenosis: A Long-Term Echocardiographic Study J. Am. Coll. Cardiol., May 19, 2009; 53(20): 1874 - 1879. [Abstract] [Full Text] [PDF]

				I. Korn-Lubetzki, A. Brand, and I. Steiner Recurrence of Sydenham Chorea: Implications for Pathogenesis Arch Neurol, August 1, 2004; 61(8): 1261 - 1264. [Abstract] [Full Text] [PDF]

				L. Y. Tani, L. G. Veasy, L. L. Minich, and R. E. Shaddy Rheumatic Fever in Children Younger Than 5 Years: Is the Presentation Different? Pediatrics, November 1, 2003; 112(5): 1065 - 1068. [Abstract] [Full Text] [PDF]

				J. Kamblock, L. Payot, B. Iung, P. Costes, T. Gillet, C. Le Goanvic, P. Lionet, B. Pagis, J. Pasche, C. Roy, et al. Does rheumatic myocarditis really exists? Systematic study with echocardiography and cardiac troponin I blood levels Eur. Heart J., May 1, 2003; 24(9): 855 - 862. [Abstract] [Full Text] [PDF]

				P. Ferrieri and for the Jones Criteria Working Group Proceedings of the Jones Criteria Workshop Circulation, November 5, 2002; 106(19): 2521 - 2523. [Full Text] [PDF]

				F E Figueroa, M S. Fernández, P Valdés, C Wilson, F Lanas, F Carrión, X Berríos, and F Valdés Prospective comparison of clinical and echocardiographic diagnosis of rheumatic carditis: long term follow up of patients with subclinical disease Heart, April 1, 2001; 85(4): 407 - 410. [Abstract] [Full Text]

This Article Extract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Narula, J. Articles by Rahimtoola, S. Search for Related Content PubMed PubMed Citation Articles by Narula, J. Articles by Rahimtoola, S. Pubmed/NCBI databases Medline Plus Health Information Cardiomyopathy Related Collections Valvular heart disease Echocardiography