25

Original Article

Jones Criteria and Underdiagnosis of Rheumatic Fever

Breno A. F. Pereira, Nlzio Antonio da Silva, Lus E. C. Andrade, Flvio S. Lima, Fernanda C. Gurian
and Joaquim Caetano de Almeida Netto
Projeto PRONUCLEAR, Brazilian Society of Rheumatology and Hospital das Clnicas, Federal University of
Gois, Brazil

ABSTRACT
Objective. The authors attempt to determine whether typical clinical and laboratory manifestations of acute rheumatic fever
(ARF) are in accordance to what has been traditionally described and how useful the Jones criteria are for diagnosis.
Methods. Data from 81 cases of ARF were retrospectively collected. Inclusion criteria: 5 to 15 years of age and diagnosis of
ARF confirmed by 2 or more rheumatologists, sustained for at least 6 months and two or more visits.
Results. Girls had more chorea (23/50.0% vs. 5/14.3%)(p<0.0001). Cardiovascular (65/80.2%) and joint involvements (63 /
77.8%) were the most frequent manifestations. Fever was noted in roughly half of the patients. Arthritis was more frequent than
arthralgia (47/58.0% vs. 16/19.8%, respectively) (p<0.0001); however, no specific pattern of joint involvement was found to
be more prevalent. Mitral insufficiency was the most frequently detected echocardiographic sign (53 / 93.0%) and its association
with aortic insufficiency was noted in 27 / 47.4% patients. Only 24 / 29.6% patients fulfilled Jones criteria for ARF requiring
an evidence of previous group-A streptococcal infection (GASI). When compulsory GASI was disregarded, this number rose
to 71/87.7% patients (p<0.0001).
Conclusion. Girls were more affected by chorea; heart valves and joints were equally affected and represented the major
clinical features; no specific pattern of joint involvement (eg.: migratory arthritis) could be labeled as typical; and strict adherence
to Jones criteria, with compulsory documentation of a previous GASI, may lead to underdiagnosis of ARF. [Indian J Pediatr
2007; 74 (2) : 117-121] E-mail : bafape@bol.com.br

Key words : Rheumatic fever; Diagnosis; Diagnostic errors; Pediatrics; Rheumatology

Rheumatic fever is a public health problem in

developing countries with incidence rates that reach
epidemic levels. It is intimately linked to poor social
and economic conditions, frequently affecting
individuals that depend heavily on their physical
strength and well being to earn their living. Therefore,
especially due to its cardiac sequels, rheumatic fever
represents a great burden on afflicted patients and on
society as a whole.1, 2, 3, 4
There are still many controversial points related to the
clinical manifestations and diagnosis of rheumatic fever.
Physicians who frequently deal with new cases of the
disease often feel uncomfortable in establishing a definite
diagnosis, specially if they strictly follow Jones criteria.
This set of criteria was created by a North-American
physician in the mid-40s, when incidence of acute
rheumatic fever (ARF) in the USA was high.5 The Jones
criteria have been revised a few times since then - the last

revision was performed by the WHO Expert Consultation

panel on Rheumatic Fever and Rheumatic Heart Disease.6
Information on chosen methods and statistical analyses
used in such reviews has not yet been disclosed.6, 7
A significant confusing factor in diagnosing ARF
comes from the fact that recent studies have shown
unusual clinical manifestations of the disease. In many
instances, there are contradictory findings between
different studies and they are frequently in contrast to
what has been described in textbooks. Therefore,
physicians seldom can rely on a typical clinical picture
of ARF and diagnosis based on clinical judgement
remains a difficult task.
The present study attempts to determine whether
clinical and laboratory manifestations of acute
rheumatic fever (ARF) are in accordance to what has been
traditionally described as typical and how useful the
Jones criteria are for diagnosis.
MATERIAL AND METHODS

Correspondence and Reprint requests : Dr. Breno A.F. Pereira, Rua

T-62, 632, ap. 200, S. Bueno. Goinia GO, Brazil. CEP: 74223-180

Indian Journal of Pediatrics, Volume 74February, 2007

Data on clinical and laboratory features were collected

117

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A.F. Pereira et al

118

symptom of joint involvement; and (5) other arthralgias,

when the patient complained of joint pain that did not
show a migratory pattern of presentation.
Parents of enrolled patients agreed to sign an informed
consent. The study was approved by the Bioethics
Committee of the attributable institution (CEP-HC/UFG).
Data were stored in a MS-Excel 2000 database
system. STATA was used to calculate Pearsons chisquare, Students t test (for comparison of means and
difference of proportions) and analysis of 95% confidence
intervals.
RESULTS
Girls were more affected by ARF than boys (46 /56.8% vs.
35/48.2%, respectively) (p<0.001). Gender significantly
influenced the presence of chorea, which was clearly
more frequent in girls (23/50.0% vs. 5/14.3%) (p<0.001).
The mean age did not differ between patients with
(10.43 y.o.) and without (9.92 y.o.) chorea (p=0.353).
The frequency of clinical features is illustrated in Fig 1.
Heart and joints were the most frequent sites of
involvement (65/80.2% and 63/77.8%, respectively)
(p>0.05 - NS). Chorea was noted in 28/34.6% patients.
Arthritis occurred more frequently than isolated
arthralgia (47/58% vs. 16/19.8%, respectively) (p<0.001),
but no particular pattern of joint involvement was found
to be significantly more frequent when stratified into
subtypes of presentation (Table 1). Apical systolic
murmur was by far the most common clinical cardiac sign
(57/96.6%). Echocardiographic abnormalities were
present in 57/70.4% patients, among which 53/93% had
mitral insufficiency (MI). The association of mitral and
aortic insufficiency (AI) accounted for about half of these
findings (27/47.4%). Carditis was present in 19/28
(67.8%) patients with chorea.
Only 24/29.6% patients fulfilled the revised Jones
90

80.2
80
70

77.8
72.8

50

70.4

65
59

60

64.1

63
57

58

54.3
50

47

44

34.6

40

32.1

28

30

26

19.8

20
10

16

67.4

9.9

11.2

ac

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from hospital records of 81 children and adolescents

who were consecutively seen at the Pediatric
Rheumatology Unit of the Hospital das Clnicas/
Federal University of Gois, Brazil, between January
1996 and August 2001. This Unit is an academic,
tertiary, referral center located in Goinia, a city of 1
million inhabitants in Brazils Central region.
Prevalence of ARF in this area is high.8, 9, 10 and the staff
rheumatologists are nationally board-certified and well
experienced in managing this disease.
Since one of our goals was to assess the reliability of
Jones criteria and since no alternative diagnostic system
has been formally proposed yet, the gold standard for
ARF in this study was based on the authors clinical
judgement. Two of the authors (Pereira BAF and Silva
NAS) are staff pediatric rheumatologists and reviewed all
cases. Subjects were included in the study if: a) their ages
ranged from 5 to 15 years; b) they had a clinical diagnosis
of a first episode of ARF agreed by at least 2 boardcertified rheumatologists; and c) this diagnosis was
sustained for 6 months and 2 or more visits. Selected cases
followed the Units standard protocol for ARF and data
on their laboratory and clinical manifestations were
recorded. Subjects were excluded from the study if
diagnosis was pending, not sustained or attested by only
one rheumatologist or other health professional. Other
exclusion criteria were only one visit to our Unit and/or
follow-up shorter than 6 months. All cases were tested
against the Jones criteria in order to assess its reliability as
a diagnostic tool.
All patients were tested for anti-streptolysin O
antibodies (ASLO), erythrocyte sedimentation rate (ESR),
C reactive protein (CRP), and mucoprotein levels, within
4 weeks after onset of symptoms. ASLO tests were
performed by plate agglutination technique using 50 L.
of patients sera and one drop of reacting solution
containing ASLO sensitized latex particles (Biolab, Rio de
Janeiro, BR). Results were expressed in IU/mL.
Evidence of previous group A streptococcal infection
(GASI) was considered positive if history revealed an
episode of upper airways streptococcal infection within 5
weeks preceding the onset of symptoms or if ASLO levels
were greater than 320 IU/mL. Inflammatory activity was
determined by ESR, CRP, and/or mucoprotein levels.
First and/or second degree relatives were considered for
family history of ARF. Echocardiographic exams were
performed whenever a cardiac murmur was detected on
physical exam. Joint features were divided into 5 patterns
of presentation: (1) classical migratory arthritis,
traditionally described as the most typical in ARF6, 7 ;(2)
non steroidal anti-inflammatory drugs (NSAIDs)
responsive arthritis, when joints were not affected in a
migratory fashion and inflammation remitted within 72
hours after initiation of NSAID; (3) atypical arthritis,
when there was joint inflammation that did not fit into
any of the above; (4) migratory arthralgia, as described for
classical migratory arthritis but with pain as the sole

A = cardiac involvement; B = joint involvement; C = arthritis; D =

arthralgia; E = Sydenhams chorea. Statistic values: students t test
for difference of proportions (A) vs (B): t=0.386, p=0.700; s(A) vs (E):
t=6.628, p=0.000; (B) vs (E): t=6.156, p=0.000; (C) vs (D): t=6.345,
p=0.000
Fig. 1. Number (darker columns) and Percentage (lighter columns)
of Patients Presenting Distinct Features of ARF.

Indian Journal of Pediatrics, Volume 74February, 2007

27

Jones Criteria and Underdiagnosis of Rheumatic Fever

TABLE 1. Number, Percentage and 95% Confidence Interval rates
(95% CI) of Distinct Patterns of Joint, Cardiac and
Echocardiographic Findings in ARF Patients.
Pattern of involvement/
Joint involvement
Classical migratory arthritis
NSAIDs* responsive arthritis
Migratory arthralgia
Atypical arthritis
Other arthralgias
Total
Cardiac murmurs
Apical systolic murmur
Systolic and diastolic murmurs
Other murmurs
Total
Echocardiographic findings
Mitral insufficiency
Mitral and aortic insufficiencies
Myocarditis
Thickening of mitral leaflet
Total

95% CI

21
11
9
15
7
63

33.3
17.5
14.3
23.8
11.1
100

22.0
9.1
6.7
14.0
3.35

57
5
4
59

96.6
8.5
6.8
100

88.3 99.6
2.8 18.7
1.9 16.5

53
27
1
14
57

93.0
47.4
1.8
24.6
100

83.0
34.0
0.4
14.1

46.3
29.1
25.4
36.2
18.8

98.1
61.0
9.4
37.8

*non-steroidal anti-inflammatory drugs

criteria for diagnosis of first episodes of ARF, 6, 7 i.e.

evidence of a previous GASI plus 2 major signs or 1
major and 2 minor signs. Since chorea allows for a
diagnosis of ARF even in the absence of other major or
minor signs 6, 7 the authors added to these afore
mentioned patients a group of 25 other subjects that
had chorea with no evidence of previous GASI and
noticed 60.5% of fulfillment (49 patients). When
compulsory evidence of a previous GASI was
disregarded, this figure rose to 71/87.7% (Fig. 2).
DISCUSSION

Acute attacks of first episodes of ARF were described in

81 distinct patients. The significantly greater overall
proportion of female patients had also been noted in
other studies. 11, 12 The high number of patients with
chorea in the present study (28/34.6%) might have had
some influence in the gender distribution of the total
number of cases. Indeed, Carapetis and Currrie have
postulated that, with a few exceptions, reports from
certain geographical areas (Africa, Asia, the Pacific, the
Caribbean and Arab countries) usually show lower
relative numbers of patients with chorea, whereas those
from other regions and/or ethnic groups (USA,
Pakistan, Turkey, and Australian aborigines) present
higher proportions. 13 According to that account, this
study area may belong to the latter group, with figures
comparable only to Australias and the USAs. 13, 14, 15, 16
Interestingly, in this study patients with chorea were
not older than other ARF patients, as has been
traditionally described. In fact, they tended to be slightly
younger when compared to other patients from the
present study (p=0.353, NS) as well as to patients with
chorea from other series.1, 13, 17, 18 The fact that cases were
included only if they were younger than 15 years of age
might have excluded some teenagers and lowered the
mean age of the sample.
Articular and cardiac manifestations have been
described as the most frequent features of rheumatic
fever.1, 2, 3, 4, 19, 20 Around 80% of patients in this series had
joint complaints. Migratory arthritis has been said to be
the typical articular manifestation of ARF, 4, 6, 19 but in
our series, although arthritis occurred more frequently
than arthralgia, no particular pattern of joint
involvement was found to be more frequent when
stratified into clinical subtypes of presentation (Tab 1).
Other studies have already indicated the fairly frequent

FIG 2. Frequency of Patients (95% Confidence Interval) who Fullfilled Different Sets of Criteria for the Diagnosis of ARF.
Jones (with GASI) (*)
19.7

29.6
(n=24)

39.6

Jones (with GASI) or chorea (#)

49.8

60.5
(n=49)

71.1

Jones without GASI (h)

80.5

87.7
(n=71)

94.8

Groups of patients:

*- Jones (with GASI) Patients strictly fulfilling Jones criteria as in reference2;

#- Jones (with GASI) or chorea Patients strictly fulfilling Jones criteria as in reference2 and those with Sydenhams chorea with no evidence

of previous GASI and not fulfulling Jones criteria;

h- Jones without GASI Patients fulfilling Jones criteria regardless of evidence of previous GASI or Sydenhams chorea.

First and last numbers in each line represent 95% CI, middle numbers represent percentage and number between brackets the actual number

of patients fulfilling each set of criteria.

Middle numbers represent percentage and number between brackets the actual number of patients fulfilling each set of criteria. First and last

numbers in each line represent 95% CI of the percentage of patients fulfilling each set of criteria.

Indian Journal of Pediatrics, Volume 74February, 2007

119

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A.F. Pereira et al
occurrence of atypical joint manifestations. 21 This
finding represents an additional complication, since
diagnosis of ARF is highly dependent on clinical
information obtained by history.
Carditis, in the form of valvulitis, usually occurs in
more than three-quarters of patients with ARF.2, 3, 20 Some
studies have found higher rates due to the systematic use
of echo-Doppler. 2, 3 In this study patients were
submitted to an echo-Doppler exam only if they
presented clinical evidence of carditis, in accordance to
the American Heart Association and the WHO
guidelines.6, 7 However, there has been a flood of recent
works showing a much greater sensitivity for the
detection of valvulitis accomplished by the systematic
use of echo-Doppler in patients with other features of
ARF and with no clinical signs of carditis. 3, 17, 22, 23
Although any layer of the heart can be affected, mitral
valve insufficiency was present in more than 90% of
patients who underwent echo-Doppler, as has been
reported by other authors. 1, 2, 3, 20 In this series, 19/28
(67.8%) patients with chorea had carditis as well, a
figure similar to those described elsewhere.1, 13 In fact, it
has been shown that screening of choreic patients with
echo-Doppler may further increment the detection of
silent valvulitis. 17, 24, 25, 26
Evidence of a prior streptococcal infection was
considered essential for diagnosis of ARF in the 1965
revision of the Jones criteria and has been kept as such
since then. 27 In the recently published revision from
WHO, there is a note reminding of the existence of
probable cases, but even for these patients the need for
an evidence of previous GASI remained.6 In the present
study, only about 60% of patients with a first attack of
ARF had either chorea or a positive history of an upper
airways GASI and/or high titers of ASLO. Highly
suggestive clinical manifestations presented by the
other 40% of patients and the long time of follow-up set
as part of the gold standard indicate that obligatory
evidence of GASI may leave almost half of ARF patients
undiagnosed. This subgroup of undiagnosed ARF
patients will not receive adequate early prophylaxis
and will remain susceptible to recurrences of ARF that
might lead to chronic rheumatic heart disease. One
reason for such low sensitivity of Jones criteria in this
series might come from the fact that patients could have
been seen late on the course of the disease (when ASLO
titers were already low) or during recurrences of
subclinical first attacks of ARF that went unnoticed.
Nevertheless, criteria for diagnosis of ARF must
contemplate such possibilities since it is a disease that
has a devastating effect over developing nations where
such problems are common. Future case-control studies
shall determine some epidemiological parameters (e.g.,
specificity, accuracy) and may help to better evaluate
this set of diagnostic criteria.
This study is a further indication of how difficult and
complex diagnosis of ARF still is. Lack of laboratory
120

markers; atypical clinical presentations of joint

involvement; low availability of echo-Doppler in areas
where it is most needed; and low sensitivity of Jones
criteria (with compulsory evidence of a previous
streptococcal infection) undoubtedly contribute to
underdiagnosis. Criteria for diagnosis of ARF shall take
into account all these situations in order to be considered
as a relevant tool for physicians daily practice.
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Jones Criteria and Underdiagnosis of Rheumatic Fever

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