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The Ross Classification for Heart Failure in Children After 25 Years: A Review
and an Age-Stratified Revision

Article  in  Pediatric Cardiology · April 2012

DOI: 10.1007/s00246-012-0306-8 · Source: PubMed

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Pediatr Cardiol
DOI 10.1007/s00246-012-0306-8
ORIGINAL ARTICLE
The Ross Classification for Heart Failure in Children After 25
Years: A Review and an Age-Stratified Revision
Robert D. Ross
Received: 10 January 2012 / Accepted: 14 March 2012
Ó Springer Science+Business Media, LLC 2012
Abstract Accurate grading of the presence and severity
of heart failure (HF) signs and symptoms in infants and
children remains challenging. It has been 25 years since the
Ross classification was first used for this purpose. Since
then, several modifications of the system have been used
and others proposed. New evidence has shown that in
addition to signs and symptoms, data from echocardiog-
raphy, exercise testing, and biomarkers such as N-terminal
pro-brain natriuretic peptide (NT-proBNP) all are useful in
stratifying outcomes for children with HF. It also is
apparent that grading of signs and symptoms in children is
dependent on age because infants manifest HF differently
than toddlers and older children. This review culminates in
a proposed new age-based Ross classification for HF in
children that incorporates the most useful data from the last
two decades. Testing of this new system will be important
to determine whether an age-stratified scoring system can
unify the way communication of HF severity and research
on HF in children is performed in the future.
Keywords Age-based Ross classification
Heart failure

Ross classification
The grading of heart failure (HF) signs and symptoms in
infants and children remains challenging. Ideally, a system
for doing this would be accurate, reproducible, correlated
closely with disease severity and outcome, and fluid to
R. D. Ross (&)
Division of Pediatric Cardiology, Carmen and Ann Adams
Department of Pediatrics, Children’s Hospital of Michigan,
Wayne State University School of Medicine,
3901 Beaubien Blvd., Detroit, MI 48201, USA
e-mail: rross@dmc.org
reflect changes in symptoms over time and with therapy.
The classification also should predict risk from disease so
that management can be tailored to HF class. Children
classified as ‘‘no risk’’ would not require treatment. ‘‘Mild
risk’’ might be managed by closer observation, early
intervention, or even prophylaxis. ‘‘Moderate risk’’ would
engender more intensive treatment, and ‘‘severe risk’’
would require maximal therapy and perhaps transplantation
referral.
Until 1987, the only system available for grading HF in
children was the New York Heart Association (NYHA)
classification. However, this system was based on limita-
tions to physical activity for adults, which did not translate
well for use with children, particularly infants. Therefore,
we developed a symptom-based classification using more
age-appropriate variables (Table 1) and demonstrated that
plasma norepinephrine correlated in a stepwise fashion
with this new Ross HF classification from grades I to IV
[16]. This was significant in that it mirrored norepinephrine
changes in adults with HF that correlated closely with
mortality [3]. Subsequently, Wu et al. [25] confirmed the
catecholamine changes with Ross class and further showed
that progressive beta receptor downregulation occurred
with each progressive Ross class.
More recently, Fernandes et al. [7] evaluated children
with idiopathic dilated cardiomyopathy. These authors
found that both the presence and severity of mitral regur-
gitation (MR) increased with the Ross class and that the
presence of MR stratified children to a significantly worse
outcome of either death or transplantation, with a hazard
ratio of 1.9 (p \ 0.01). Progression of MR severity
increased these risks significantly.
Over time, use of the Ross classification system has
increased, but the system is associated with problems.
Assignment of classes I and IV tends to be straightforward,
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 Pediatr Cardiol

Table 1 Original Ross classification [16]
I: No limitations or symptoms
II: Mild tachypnea or diaphoresis with feedings in infants, dyspnea
at exertion in older children; no growth failure
III: Marked tachypnea or diaphoresis with feedings or exertion and
prolonged feeding times with growth failure from CHF
IV: Symptomatic at rest with tachypnea, retractions, grunting, or
diaphoresis
with either no symptoms (class I) or symptoms with the
patient at rest (class IV). However, classes II and III are
more subjective and can overlap. Also, few class IV
patients are found in children who may have a greater
ability to compensate for HF early on. This leads to many
studies combining classes III and IV to have adequate
numbers for data analysis.
In addition, growth failure may be the only manifesta-
tion of HF in young children, which makes it difficult to
determine whether that puts them in Ross class III or a
lower class in the absence of respiratory or other symptoms
listed. Also confusing is the definition of growth failure
which has differed over time with various authors, and
growth failure may be related to noncardiac conditions.
To evaluate the variables that have most accurately
defined HF, we studied 41 infants and used the blinded
average grade from four pediatric cardiologists to compare
signs and symptoms. Based on the most sensitive and
specific variables, a scoring system for grading HF in
infants was derived (Table 2) [17]. Interestingly, neither
diaphoresis nor growth failure proved to be significant.
This is likely due to the frequent sweating that normal
infants exhibit and the young median age of 2.5 months in
the study, which may have been too early for growth
failure from HF to have become manifest.
Several authors have modified the aforementioned
scoring system to expand its use to older children. The first
such attempt was by Reithmann et al. [14] in their study on
adenylyl cyclase in severe HF. They added basal heart and
respiratory rates for children by age, namely, for infants
and children 1–6 years old, children 7–10 years old, and
children 11–14 years old. This was a useful modification,
but these authors also reinstituted diaphoresis and added
cyanosis and a precordial thrill, neither of which are typi-
cally associated with HF. In 2002, Laer et al. [10] modified
this further, limiting their new version to six variables
(Table 3). A potential downside of this simplified version
is that half of the six categories relate to the work of
breathing, which may undervalue the other manifestations
of congestive heart failure (CHF) in children. Nevertheless,
many subsequent studies have used this Laer-modified
Ross scoring system to study HF.
At about the same time, a new system called the New
York University Pediatric Heart Failure Index (PHFI) was
proposed by Connelly et al. [4]. This 30-point scale uses
many of the signs and symptoms in the Ross classification
but adds points for medications used to treat HF and also
for a single-ventricle physiology. Although sicker patients
generally do require more medications, scoring in this way
may be problematic. If a child with severe symptoms of HF
is treated and the symptoms improve, the change in score
Table 3 Modified Ross score [10]
0 ?1 ?2

History
Table 2 Ross scoring system for heart failure in infants [17] Diaphoresis Head only Head and body Head and
at exertion body at rest
Score
Tachypnea Rare Several times Frequent
0 1 2 Physical examination
Breathing Normal Retractions Dyspnea
Feeding history
Age (years)
Volume consumed per feeding (oz) [3.5 2.5–3.5 \2.5
Respiratory rate (breaths/min) (years)
Time taken per feeding (min) \40 [40 –
0–1 \50 50–60 [60
Physical exam
1–6 \35 35–45 [45
Respiratory rate (n/min) \50 50–60 [60
7–10 \25 25–35 [35
Heart rate (n/min) \160 160–170 [170
11–14 \18 18–28 [28
Respiratory pattern Normal Abnormal –
Heart rate (beats/min) (years)
Peripheral perfusion Normal Decreased –
0–1 \160 160–170 [170
S3 or diastolic rumble Absent Present –
1–6 \105 105–115 [l15
Liver edge from right costal margin \2 2–3 [3
(cm) 7–10 \90 90–100 [100
11–14 \80 80–90 [90
Total score: 0–2 (no CHF), 3–6 (mild CHF), 7–9 (moderate CHF),
10–12 (severe CHF) Hepatomegaly \2 2–3 [3
size (cm)
CHF congestive heart failure

123
Pediatr Cardiol
will be blunted by the points received for these medications
and thus may not reflect the improvement [15]. Regarding
single-ventricle patients, while most have reduced exercise
capacity, some children with Fontan palliation have no
symptoms, experience normal aerobic capacity for age and
body size, and thus do not deserve higher HF scores.
In 2006, Tissieres et al. [23] compared the NYHA
classification, the Laer-modified Ross classification, and
the PHFI using 20 children with HF from rheumatic heart
disease. Although all three systems correlated with the
cardiothoracic index on chest X-ray, the PHFI faired better
on left ventricle (LV) mass, end-systolic wall stress, left
atrium/aortic ratio, and N-terminal pro-brain natriuretic
peptide (NT-proBNP).
Recently, a great deal of interest in both the adult and
pediatric HF literature has focused on the natriuretic pep-
tides in HF. From myocardial cells, BNP is released into
the bloodstream in response to various stressors on the
heart including LV volume and pressure overload. This
correlates well with symptoms of HF in adults and children
and can differentiate cardiac from pulmonary causes of
respiratory distress [6]. As the N-terminal fragment of the
prohormone BNP, NT-proBNP is a good marker of clinical
severity and worsening systolic function in children with
HF [13] and has a longer half-life than BNP. Sugimoto
et al. [22] found very sensitive and specific cutoff points of
NT-proBNP for Ross classes I to IV that had area-under-
the receiver operating curves of 0.96 to 0.99. There was a
dichotomy of values, with lower numbers for children older
than 3 years than for children younger than 3 years. For
distinguishing each class independently, NT-proBNP was
better than BNP itself.
Multiple other studies have confirmed the usefulness of
NT-proBNP and BNP as correlates of HF symptoms in
children, as markers of systolic dysfunction, and impor-
tantly, as predictors of the need for mechanical circulatory
support, heart transplantation, and death [1, 18, 24]. This
has held true for HF from cardiomyopathy and from con-
genital heart disease such as single ventricle with failing
Fontan palliation [11, 20]. The trend of NT-proBNP over
time in individual patients is most useful for predicting
outcomes [24].
Another factor found to be useful for predicting out-
comes in HF is exercise capacity. In adults, a peak exercise
oxygen consumption of less than 14 ml/kg/min is an
independent predictor of mortality and a criterion for list-
ing a patient to receive a heart transplant. However, this
cutoff may be less sensitive in the current era of improved
medical management for HF [2]. In addition, children have
different oxygen consumptions as they grow such that the
absolute number of 14 ml/kg/min is not a sensitive marker
of the need for transplantation [5]. Giardini et al. [8] per-
formed exercise stress tests on 82 children with dilated
cardiomyopathy and found that in a 4-year follow-up per-
iod, the percentage of peak oxygen consumption (based on
age and sex) stratified outcomes accurately. Using 62 % of
predicted normal as a cutoff, survival curves indicated a
significantly higher rate of death or urgent listing for
transplantation of 50.6 (for those B62 %) versus 4.4 %
(for those [62 %) at 24 months, with a hazard ratio of
10.8.
Growing evidence also indicates that poor systolic
function bodes ill in terms of long-term outcomes for
children as it does for adults. In both dilated cardiomyop-
athy and HF from congenital heart disease, low ejection
fractions predict death or the need for transplantation
[9, 12].
It is clear that with all this recent data on factors
predictive of outcomes in children with HF that a revision
in how we grade symptom severity is required. It also is
apparent that an age stratification is required to encom-
pass the changes in signs and symptoms that children
manifest from infancy to late childhood. A classification
system should include the biomarkers, echo parameters of
systolic function and mitral or systemic atrioventricular
valve (AV) insufficiency, and reflect exercise limitations
reflected by feeding and growth in infants and exercise
capacity indicated by percentage of predicted maxi-
mal oxygen uptake (VO2) in older children. Therefore, I
propose an age-based Ross classification using the origi-
nal variables that proved to be sensitive and specific and
adding the new evidence-based data. Table 4 depicts this
revised system.
The age ranges of 0–3 months, 4–12 months, 1–3 years,
4–8 years, and 9–18 years were chosen because the vari-
ables in the classification are generally stable during these
periods but vary between them. Each age range has 10
variables with scores of 0, 1, or 2 possible for a range of 0
to 20. The scoring system can be used as a continuous data
set for comparison with outcomes, or it can be categorized
by points assessed as Ross classes I (0–5), II (6–10), III
(11–15) and IV (16–20).
For all children, hepatomegaly is measured as the dis-
tance below the right costal margin with abdominal situs
solitus or from the left costal margin for situs inversus. The
ejection fraction generally is obtained from echocardiog-
raphy but can be derived from MRI or other imaging
methods for single ventricles or systemic right ventricles.
Systemic AV insufficiency refers to the mitral valve for
systemic left ventricles and to the systemic AV valve for
single ventricles or systemic right ventricles.
Each age range has unique aspects that require com-
ment. All heart rate and respiratory rates should be recor-
ded with the infant or child in the basal state without crying
or undo agitation, and the cutoff points have been selected
based on normals for these age ranges [19].
123
 Pediatr Cardiol

Table 4 Age-based Ross classification for heart failure in children Table 4 continued
0 1 2 0 1 2

0–3 Months 9–18 Years

Oz/feeding [3.5 2.5–3.5 \2.5 N/V Nl Intermittent Frequent
Time for feeding \20 20–40 [40 Breathing Nl Tachypnea Retractions
(min) RR/min \20 20–30 [30
Breathing Nl Tachypnea Retractions HR/min \90 90–100 [100
RR/min \50 50–60 [60 Perfusion Nl Reduced Shocky
HR/min \160 160–170 [170 Hepatomegaly (cm) \2 2–3 [3
Perfusion Nl Reduced Shocky NT-proBNP (pg/ml) \300 300–1,500 [1,500
Hepatomegaly (cm) \2 2–3 [3 EF% [50 30–50 \30
NT-proBNP (pg/ml) \450 450–1,700 [1,700 Max %VO2 [80 60–80 \60
([4 days)
AV insufficiency None Mild Moderate/
EF% [50 30–50 \30 severe
AV insufficiency None Mild Moderate/
severe Oz ounce, Nl normal, Wt% fall-off on weight curve %, RR respiratory
rate, HR heart rate, NT-proBNP N-terminal pro-brain natriuretic
4–12 Months
peptide, EF ejection fraction, AV systemic atrioventricular valve, N/
Feeding Nl Decreased Gavaged V nausea/vomiting; Max %VO2 % of predicted maximal oxygen
Wt% Nl C1 Curve C2 Curve uptake for age and sex
Breathing Nl Tachypnea Retractions
RR/min \40 40–50 [50
Age 0–3 Months
HR/min \12 120–130 [130
Perfusion Nl Reduced Shocky The volume of formula per feeding is for bottle-fed babies.
Hepatomegaly (cm) \2 2–3 [3 For breastfed infants, the volume taken has to be rated
NT-proBNP (pg/ml) \450 450–1,700 [1,700 subjectively as normal, decreased, or gavage supple-
EF% [50 30–50 \30 mented. Normally, NT-proBNP is elevated in newborns, so
AV insufficiency None Mild Moderate/ this measurement should be obtained after 4 days of life.
severe
1–3 Years
Feeding Nl Decreased Gavaged
Age 4–12 Months
Growth Nl Weight loss Cachexia
Breathing Nl Tachypnea Retractions Feeding is qualitatively graded because diets vary in this
RR/min \30 30–40 [40 age range and specific volumes of formula are not appli-
HR/min \110 110–120 [120 cable. The time of feeding is replaced by growth, as
Perfusion Nl Reduced Shocky depicted on the growth curve. A fall-off in growth, defined
Hepatomegaly (cm) \2 2–3 [3 as a decrease of C1 weight curve percentile (i.e., from the
NT-proBNP (pg/ml) \450 450–1,700 [1,700 50 to the 25 %) earns 1 point, whereas a fall-off of C2
EF% [50 30–50 \30 percentile curves (i.e., from 50 to 10 %) earns 2 points. If
AV insufficiency None Mild Moderate/ no previous weights are available, then 1 point is awarded
severe
for a weight percentage of C1 curve below the current
4–8 Years height percentile and 2 points for C2 curve percentiles for
N/V None Intermittent Frequent weight below that for height because increases in body
Growth Nl Weight loss Cachexia length typically are preserved in HF, whereas weight gain
Breathing Nl Tachypnea Retractions is not.
RR/min \25 25–35 [35
HR/min \100 90–100 [100
Perfusion Nl Reduced Shocky Age 1–3 Years
Hepatomegaly (cm) \2 2–3 [3
NT-proBNP (pg/ml) \300 300–1,500 [1,500 Because the time of early rapid growth has passed by these
EF% [50 30–50 \30 ages, the pattern on the growth curves has been changed to
AV insufficiency None Mild Moderate/ recent weight loss and cachexia for respectively 1 and 2
severe points.

123
Pediatr Cardiol
Age 4–8 Years
As children age, their gastrointestinal symptoms from HF
change to reports of nausea or vomiting, so scores are 1 for
these symptoms intermittently and 2 for frequent nausea or
vomiting. The cutoff values for NT-proBNP have been
adjusted down for the lower values found after the age of
3 years.
Age 9–18 Years
At this age, most children can perform a maximal stress
test, so this has replaced growth failure as a more objective
measure of heart failure decompensation.
BNP
Although NT-proBNP has a longer half-life than BNP and
correlates better with symptom class, retrospective studies
may have access only to BNP levels. If so, then BNP may
replace NT-proBNP in the grid for all ages beyond 4 days,
with points of 0 for less than 30 pg/ml, 1 for 30–140 pg/ml,
and 2 for more than 140 pg/ml. Because these peptides also
may be elevated from renal dysfunction, children with
advanced renal insufficiency may have a somewhat inflated
score for this component [21].
Class IV
Finally, some children will be so sick from HF that they
will require intravenous medications, circulatory support
such as extracorporeal membrane oxygenation (ECMO) or
a ventricular assist device, and mechanical ventilation.
These interventions make the children unfit for the use of
this grading system and should put them by definition into
class IV.
Future Challenges
The next challenge is to test this age-based Ross classifi-
cation using large numbers of infants and children with and
without overt HF to determine whether it accurately pre-
dicts outcomes for each age range. Although it does entail
more information gathering than the original Ross system,
most patients with HF get tested for these variables in
addition to the readily obtained historical and physical
examination findings. Use of this age-based stratification
should allow for more accurate grading, eliminating
the variance previously encountered based on age-related
differences in symptoms. Standardizing our approach for
future research and communication using one system that
incorporates all the significant features of HF culled from
the literature is a big step toward an evidence-based
approach to studying and treating childhood HF in the
future.
References
1. Aurbach SR, Richmond ME, Lamour JM et al (2010) BNP levels
predict outcome in pediatric heart failure patients: post hoc analysis
of the pediatric carvedilol trial. Circ Heart Fail 3:606–611
2. Butler J, Khadim G, Paul KM et al (2004) Selection of patients
for heart transplantation in the current era of heart failure therapy.
J Am Coll Cardiol 43:787–793
3. Cohn JN, Levine B, Olivari T et al (1984) Plasma norepinephrine
as a guide to prognosis in patients with chronic congestive heart
failure. N Engl J Med 311:819–823
4. Connelly D, Rutkowski M, Auslender M, Artman M (2001) The
New York University pediatric heart failure index: a new method
of quantifying chronic heart failure severity in children. J Pediatr
138:644–648
5. Das BB, Taylor AL, Boucek MM, Wolfe RW, Yetman AT (2006)
Exercise capacity in pediatric heart transplant candidates: Is there
any role for the 14 ml/kg/min guideline? Pediatr Cardiol 27:226–229
6. Evim MS, Ucar B, Kilic Z, Colak O (2010) The value of serum
N-terminal pro-brain natriuretic peptide levels in the differential
diagnosis and follow-up of congestive cardiac failure and respi-
ratory distress due to pulmonary aetiologies in infants and chil-
dren. Cardiol Young 20:495–504
7. Fernandes FP, Manlhiot C, McCrindle BW, Mertens L, Kantor
PF, Friedberg MK (2011) Usefulness of mitral regurgitation as a
marker of increased risk for death or cardiac transplantation in
idiopathic dilated cardiomyopathy in children. Am J Cardiol
107:1517–1521
8. Giardini A, Fenton M, Andrews RE, Derrick G, Burch M (2011)
Peak oxygen uptake correlates with survival without clinical
deterioration in ambulatory children with dilated cardiomyopa-
thy. Circulation 124:1713–1718
9. Guimaraes GV, d’Avila VM, Camargo PR, Moreira LFP, Luces
JRL, Bocchi EA (2008) Prognostic value of cardiopulmonary
exercise testing in children with heart failure secondary to idio-
pathic dilated cardiomyopathy in a non-B-blocker setting. Eur J
Heart Fail 10:560–565
10. Laer S, Mir TS, Behn F et al (2002) Carvedilol therapy in
pediatric patients with congestive heart failure: a study investi-
gating clinical and pharmacokinetic parameters. Am Heart J
143:916–922
11. Lechner E, Gitter R, Mair R et al (2008) Aminoterminal brain
natriuretic peptide levels in children and adolescents after Fontan
operation correlate with congestive heart failure. Pediatr Cardiol
29:901–905
12. Patel MS, Berg AM, Vincent RN, Mahle WT (2010) Serum
parameters and echocardiographic predictors of death or need for
transplant in newborns, children, and young adults with heart
failure. Am J Cardiol 105:1798–1801
13. Ratnasamy C, Kinnamon DD, Lipshultz SE, Rusconi P (2008)
Associations between neurohormonal and inflammatory activa-
tion and heart failure in children. Am Heart J 155:527–533
14. Reithmann C, Reber D, Kozlik-Feldmann R et al (1997) A
postreceptor defect of adenylyl cyclase in severely failing
123

myocardium from children with congenital heart disease. Eur J
Pharm 330:79–86
15. Ross RD (2001) Grading the graders of congestive heart failure in
children. J Pediatr 138:618–620
16. Ross RD, Daniels SR, Schwartz DC, Hannon DW, Shukla R,
Kaplan S (1987) Plasma levels of norepinephrine in infants and
children with congestive heart failure. Am J Cardiol 59:911–914
17. Ross RD, Bollinger RO, Pinsky WW (1992) Grading the severity
of congestive heart failure in infants. Pediatr Cardiol 13:72–75
18. Rusconi PG, Ludwig DA, Ratnasamy C et al (2010) Serial
measurements of serum NT-proBNP as markers of left ventric-
ular function and remodeling in children with heart failure. Am
Heart J 160:776–783
19. Saunders M, Gorelick MH (2011) Nelson textbook of pediatrics,
19th edn. Saunders Elsevier, Philadelphia, p 280
20. Shah A, Feraco AM, Harmon C, Tacy T, Fineman JR, Bernstein
HS (2009) Usefulness of various plasma biomarkers for diagnosis
of heart failure in children with single ventricle physiology. Am J
Cardiol 104:1280–1284
123
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Pediatr Cardiol
21. Srisawasdi P, Vanavanan S, Charoenpanichkit C, Kroll MH
(2010) The effect of renal dysfunction on BNP, NT-proBNP, and
their ratio. Am J Clin Pathol 133:14–23
22. Sugimoto M, Manabe H, Nakau K et al (2010) The role of
N-terminal pro-B type natriuretic peptide in the diagnosis of
congestive heart failure in children. Circ J 74:998–1005
23. Tissieres P, Aggouon Y, Da Cruz E et al (2006) Comparison of
heart failure classifications in children undergoing valvular sur-
gery. J Pediatr 149:210–215
24. Wong DTH, George K, Wilson J et al (2011) Effectiveness of
serial increases in amino-terminal pro-B-type natriuretic peptide
levels to indicate the need for mechanical circulatory support in
children with acute decompensated heart failure. Am J Cardiol
107:573–578
25. Wu JR, Chang HR, Huang TY, Chiang CH, Chen SS (1996)
Reduction in lymphocyte B-adrenergic receptor density in infants
and children with heart failure secondary to congenital heart
disease. Am J Cardiol 77:170–174