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Clinical course and analysis of ten fatal cases of clozapine-induced myocarditis and comparison with 66 surviving cases
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / s c h re s
Clinical course and analysis of ten fatal cases of clozapine-induced myocarditis andcomparison with 66 surviving cases
Kathlyn J. Ronaldson , Paul B. Fitzgerald , Andrew J. Taylor , Duncan J. Topliss John J. McNeil a Department of Epidemiology and Preventive Medicine, Monash University, The Alfred Centre, 99 Commercial Road, Melbourne, VIC 3004, Australiab Monash Alfred Psychiatry Research Centre, Alfred Hospital and Monash University, School of Psychology and Psychiatry, P.O. Box 315, Prahran, Melbourne VIC 3181, Australiac The Heart Centre, Alfred Hospital, P.O. Box 315, Prahran, Melbourne VIC 3181, Australiad Department of Endocrinology and Diabetes, Alfred Hospital, P.O. Box 315, Prahran, Melbourne VIC 3181, Australia
Background: Fatal clozapine-induced myocarditis has not been investigated systematically. We describe the
clinical course of 10 fatal cases of myocarditis with clozapine and identify factors associated with fatality.
Methods: Cases of myocarditis were documented from the patient's medical records and fatal cases also from
Results: The fatal cases of myocarditis occurred 1996–2009 and were diagnosed at autopsy. Before death,three had no symptoms of illness and only three had cardiac-speciﬁc diagnostic results. None was
investigated by cardiac imaging techniques, and in none was myocarditis suspected before death. Duration of
clozapine for the fatal cases was 14–33 days with an outlier at 4.5 months. Only 3 cases had signiﬁcant
Comparison of these ten cases with 66 non-fatal cases indicated no signiﬁcant difference in gender, age,
smoking status, dose at onset or concomitant sodium valproate. However, obesity (BMI N 30 kg/m2) was
signiﬁcantly more frequent among fatal than non-fatal cases (60% vs 26%; p b 0.03) and duration of clozapinewas signiﬁcantly longer for fatal cases (20.8 vs 17.0 days; p b 0.006), after exclusion of one outlier. Creatinekinase (CK) N 1000 U/L was also associated with death (p = 0.0004).
Conclusions: Routine monitoring for myocarditis for the ﬁrst 4 weeks of clozapine, and discontinuation ofclozapine in the presence of evidence consistent with myocarditis may assist to prevent fatalities occurringfrom early-onset myocarditis. Investigation by cardiac imaging will give a measure of severity and need forintervention. Obesity may increase the risk of mortality and CK N 1000 U/L may indicate life-threateningillness.
2011 Elsevier B.V. All rights reserved.
creased dramatically. Consequently, when reviewedthe cases reported to the Australian Therapeutic Goods Administra-
The association between myocarditis and therapeutic use of
tion up to the end of 2003, using numbers of patients registered with
clozapine has been known with some conﬁdence at least since the
the two sponsor companies, they estimated an incidence of 0.7–1.2%.
regulatory agencies in the United Kingdom (
Another Australian estimate of about 2% was based on data from a
in a review article have avoided estimating the incidence of
) published alerts on the subject. A subsequent article by
clozapine-induced myocarditis, citing a number of reasons for the risk
, describing 15 cases of clozapine-related
being substantially underestimated, including low rates of reporting
myocarditis occurring in Australia in the ﬁrst month of therapy,
to spontaneous adverse reaction reporting databases, variability in the
provided supportive evidence for the association, with the incidence
presentation of myocarditis making diagnosis difﬁcult, and the low
of fatality from this cause a thousand-fold increase on the background
likelihood of psychiatric patients seeking medical attention for
physical illness. The data presented by suggest
Since the publication of the paper by the
the mortality rate with cases of myocarditis is about 10%.
awareness of clozapine-induced myocarditis in Australia has in-
reported ﬁve fatal cases and subsequently
individual fatal cases have been described by . Fatal cases have also been listed in seriesbased on data collected by a national adverse reaction reporting
⁎ Corresponding author. Tel.: +613 9903 0840; fax: +613 9903 0556.
0920-9964/$ – see front matter 2011 Elsevier B.V. All rights reserved.
K.J. Ronaldson et al. / Schizophrenia Research 128 (2011) 161–165
have occurred in the United States up to 2001 (
Characteristics of the 10 fatal and 66 non-fatal cases of clozapine-induced myocarditis.
In addition, described a fatal overdose in
which myocarditis was diagnosed at autopsy.
To date there has been no review speciﬁcally of fatal cases. In this
paper we describe the clinical course of ten fatal cases, compare key
characteristics with those of surviving cases, and seek to identify
factors which may serve as clues to the prevention of myocarditis-
related fatality in patients starting clozapine.
Fatal and non-fatal cases of clozapine-related myocarditis were
a Data on smoking status available for 9 fatal and 61 non-fatal cases and on BMI for all
identiﬁed from reports submitted to the Therapeutic Goods Admin-
istration, the Australian drug regulatory authority, between January1993 and December 2009; details of other cases were communicated
to the authors by staff of the health services for which ethicscommittee approval had been obtained (see 2.1); and fatal cases
The time from commencement of clozapine to death was 14–34
alone were identiﬁed from cases in the National Coroners' Information
(mean 21.4) days with an outlier at 136 days (4.5 months). One
patient had discontinued clozapine at the time of death (Case 1).
Documentation of each case included the date of birth, sex,
Another had missed a dose 3 days before death, and then had a
clozapine start and end dates, dose of clozapine taken each day,
reduction in dose from 100 to 50 mg/day (Case 7). The others were
baseline pathology results and results obtained during the course of
continuing clozapine without interruption.
clozapine treatment and until death or resolution of symptoms for
Six patients were showing clinical signs of illness at the time of
surviving cases, signs and symptoms recorded in the progress notes and
death. Two of the cases, perhaps three, were apparently well, including
details described in the autopsy report. Documentation for each case
Case 3 who reported that he was “feeling great” on the day before he
was reviewed by the study steering group for compliance with the case
died overnight in his sleep. Cases 4, 5 and 6 were thought to have upper
deﬁnition for clozapine-related myocarditis ).
respiratory tract infections, Case 7 was investigated for neurolepticmalignant syndrome and Case 1 had mild fever and renal impairment
(creatinine 250 μmol/L). Case 10, which occurred after 4.5 months,had been admitted non-speciﬁcally unwell both physically and
Approval for the study was obtained from the Human Research
mentally 10 days before death. It is unclear whether this illness was
Ethics Committees of the following institutions and health services:
related to myocarditis, but the post mortem indicated acute and
Monash University, Austin Health, Barwon Health, Bayside Health,
Bendigo Health, Department of Human Services, Department of Justice,
Only four patients had cardiac-speciﬁc investigations but
Eastern Health, Mercy Health, North West Mental Health, Peninsula
none had echocardiography or other direct investigation of cardiac
Health, St Vincent's Health, Southern Health (all from Victoria);
Northern Sydney Central Coast Health, Sydney South West Area Health
Case 9 is notable for having died of myocarditis following re-
Service (Royal Prince Alfred Hospital and Concord Hospital Zones)
initiation of clozapine, having used clozapine previously without any
(from New South Wales); and Prince Charles Hospital (from Queens-
indication of an adverse effect, although documentation was insufﬁ-
land). The approvals covered access to medical records without patient
cient to conﬁdently exclude a missed episode of myocarditis during
consent. In addition, an Access Agreement was signed with the Victorian
Institute of Forensic Medicine for access to the National Coroners'
The plasma clozapine concentrations (0.1–2.7 mg/L) among the
Information System database and a Deed of Conﬁdentiality and Conﬂict
fatal cases reﬂect the prescribed clozapine dose of each individual. In
of Interest with the Therapeutic Goods Administration for access to
no case was alcohol or any illicit drug found in the post mortem blood.
A key feature of these cases is that myocarditis was not suspected
in any of these patients prior to death.
Statistical analysis was conducted using STATA/IC version 10. Risk
ratios as for a cohort study were calculated for categorical variables, with
Autopsy indicated that ﬁve of the fatal cases were free of coronary
p-values based on the Chi-squared test. The 2-tailed Students t-test was
artery disease, two had minimal atheroma and three had signiﬁcant
used to investigate the difference in means for continuous variables.
disease with stenosis greater than or equal to 50% Thosewith BMI greater than 30 kg/m2 were equally divided between those
with signiﬁcant atherosclerosis and those free of disease. The autopsyreport for Case 4, who had the most severe atherosclerotic narrowing,
Myocarditis was diagnosed at autopsy in each of the 10 fatal cases
recorded that ischaemic heart disease and hypertension had contrib-
by the presence of mixed inﬂammatory inﬁltrates in cardiac histology.
uted to the death as independent causes. Case 9 was found to have
All except one case had hyperinﬂated and/or congested lungs, and
thromboemboli occluding both pulmonary arteries and myocarditis
was a secondary cause. In no other case was pre-existing cardiovas-
The age and sex distribution of the fatal cases is indicated in
cular disease considered to have contributed to the deaths.
presents further characteristics of the same cases andthe clinical and diagnostic details. The ten cases occurred
3.3. Comparison of fatal and non-fatal cases
between 1996 and 2009. Six patients had a body mass index (BMI) ofmore than 30 kg/m2 and seven (of nine; data missing for one) were
compares characteristics of the fatal cases and the non-
fatal cases. There was no signiﬁcant difference between fatal and non-
K.J. Ronaldson et al. / Schizophrenia Research 128 (2011) 161–165
Table 2Characteristics of the 10 fatal cases of myocarditis.
fatal cases for gender, age, proportion of smokers, dose at onset or
proportion taking sodium valproate. However, the risk ratio for deathwith BMI above 30 kg/m2 was 3.5 (95% CI 1.1–10.9; p b0.03) and
Compared with surviving cases, there is nothing remarkable about
duration of clozapine was signiﬁcantly longer (p b0.006) for the fatal
the fatal cases in age, sex, smoking status, last clozapine daily dose and
cases compared with those that were non-fatal, even after removal of
concomitant medication. Sodium valproate was included in the
analysis because it was the only medication other than clozapine
In addition, all three of the fatal cases for which results were
taken by more than two fatal cases. The apparent association of a BMI
available had very high creatine kinase (CK) results (N1000 U/L). In
of more than 30 kg/m2 with a greater likelihood of death may be a
contrast, only 3 of 65 surviving cases had a CK value of more than
random occurrence, but it is biologically plausible that cardiac
1000 U/L (p = 0.0004; Fisher's exact test), and only 12 had results
compromise in the setting of obesity reduces the prospect of recovery.
exceeding twice the upper limit of normal.
The signiﬁcantly longer mean duration of clozapine use for fatal cases
Table 3Clinical and diagnostic features of the 10 fatal cases of myocarditis.
Case Pro-dromal Heart rate Other clinical observations
NMS, PE and serotonin 50% stenosis of left anterior
Abbreviations: bpm, beats per minute; CK, creatine kinase; CK MB, creatine kinase muscle and brain; CRP, C-reactive protein; FBE, full blood examination; NA, not available; NMS,neuroleptic malignant syndrome; PE, pulmonary embolism; RR respiration rate; WBC, white blood cells; ULN, upper limit of normal.
K.J. Ronaldson et al. / Schizophrenia Research 128 (2011) 161–165
may be an indication that fatality followed delayed recognition of
published case, clozapine was withdrawn when the 64-year-old
illness and delayed withdrawal of clozapine.
woman developed tachycardia, fever and hypoxia
She nevertheless died 4 days later of sudden cardiorespiratory
reported a range of plasma levels for patients currently taking
arrest. Fulminant myocarditis was diagnosed at autopsy. Likewise one
clozapine of 0.0–2.61 (mean 0.34; 114 patients) mg/L. In a study by
of the patients among the present ten had stopped taking clozapine
post mortem clozapine blood concentrations
following seven cases of fatal self-poisoning were 3.7–12 mg/L in
Since the fatal case occurring after 4.5 months of clozapine is the only
individuals who had been poorly compliant or who had used
case among 76 with onset later than clozapine day 33, late developing
clozapine prescribed for another person. These literature comparisons
cases appear to be very rare. Hence, it is difﬁcult to conceive of a cost-
suggest that there is no reason to believe that clozapine toxicity was a
effective monitoring scheme for a death occurring so late after clozapine
factor in the ten fatalities caused by myocarditis.
commencement. However, it is possible that the chronic myocardial
The high CK results for three cases are notable, in comparison with
inﬂammation found at autopsy originated during the ﬁrst 4 weeks of
data for the non-fatal cases and in view of the absence of data for the
clozapine and the monitoring employed was inadequate to effect
other fatal cases. found that higher CK values (mean for
11 cases 1708 ± 1217 U/L) were associated with fulminant myocarditiscompared with milder non-fulminant disease.
4.1. Coronary artery disease and fatal myocarditis
In the month following the publication of the article by Kilian et al.
in November 1999, Novartis Australia circulated a cardiac monitoring
Since the study was retrospective, it was not possible for us to
protocol in Australia. These guidelines have been followed in varying
reliably document pre-existing cardiovascular disease and risk factors
degrees across Australia since that date. Six of the ten cases described
for such disease, such as hypertension, diabetes and hyperlipidaemia,
here occurred in the context of use of these guidelines and consequent
to compare these characteristics in fatal and non-fatal cases. However,
awareness among clinicians and pathologists of the possibility of
we were able to ascertain that only 50% of the fatal cases had some
death from myocarditis in patients recently initiated on clozapine.
degree of atherosclerosis, and for only one of these was ischaemic
Hence, there may be an enhanced likelihood of fatal myocarditis in
heart disease considered to have contributed to the death.
persons taking clozapine at the time of death being identiﬁed at
reviewed a cohort of 134 individuals with schizophrenia who
autopsy in Australia, compared with other countries.
died aged 48.6 ± 14.8 years and whose families had donated brain
recently published an observational study
tissue to the Maryland Brain Collection in the US state of Maryland.
comparing rates of sudden cardiac death occurring in the community
Sixty eight percent had died of natural causes, including 45.7% who
in patients taking antipsychotic drugs among Medicaid enrollees in
died of cardiovascular disease. The frequency of atherosclerosis among
the US state of Tennessee. Although the exposure for clozapine was
these individuals, determined at autopsy, was 44%, and is similar to
low, the incident rate ratio was higher for clozapine than for other
that observed among these cases of fatal clozapine-induced myocar-
antipsychotics. It is feasible that at least some of these deaths may
ditis. It is apparent that coronary artery disease was not a major factor
have been caused by myocarditis. An early study by
in the death from myocarditis of these cases.
using mortality data for 196 current users of clozapine acrossthe US did not identify myocarditis as a cause of death, but conduction
disorders or sudden death and respiratory illness occurred at twiceand three times the rate, respectively, in current versus past users.
The question arises, would any of these ten deaths have been
Five deaths were attributed to pneumonia in an analysis conducted in
preventable if more had been understood about clozapine-induced
the United Kingdom by of causes of death for 21
myocarditis at the time of presentation? Since myocarditis was not
patients taking clozapine. In this study, cause of death was obtained
suspected in any of these cases, it may be that more care with
from case notes or death certiﬁcate and the number of deaths
monitoring for this outcome during the ﬁrst 4 weeks after com-
investigated by autopsy was not speciﬁed. Since patients developing
mencement of clozapine and/or taking appropriate steps in response
myocarditis frequently have the symptoms of a respiratory tract
to clinical and diagnostic indicators that myocarditis may have been
infection, autopsy ﬁndings typically reveal congested and/or hyper-
present would have prevented some of these deaths. The longer
inﬂated lungs, and myocarditis may be missed even if the myocar-
duration of clozapine exposure for the nine fatal cases occurring in the
ﬁrst 5 weeks of clozapine compared with the non-fatal would support
is possible that some of these fatalities with a diagnosis of pneumonia
the view that stopping clozapine earlier may have prevented death.
or respiratory illness may have been missed myocarditis.
Even those who do not develop obvious clinical signs and symptoms
of illness may be identiﬁed if routine monitoring is followed. Although
prevention of serious illness and fatality with monitoring is unlikely tobe as reliable as for symptomatic cases, three of the non-fatal cases were
Despite the risk of death from myocarditis, a recent study
asymptomatic and for these myocarditis was detected using routine
including all patients with a diagnosis of schizophrenia in Finland
monitoring. The case who had previously taken clozapine without any
found that clozapine was associated with a signiﬁcantly lower all-
indication of the development of myocarditis illustrates the importance
cause mortality than any other antipsychotic medication
of monitoring reintroduction of clozapine with just as much care as
In other studies, protection against mortality had been
There remains, however, the possibility that in these patients there
but an implication from the Finnish study is that this may be an
were factors such as severity of the inﬂammatory assault on the
incomplete explanation. Further, in a meta-analysis, clozapine rated
myocardium and host factors governing the response of the heart to
above other second generation antipsychotics on two out of three
this assault that may have meant that the patient would have
measures of efﬁcacy plus overall symptoms and was second only to
succumbed despite a prompt response to rises in cardiac enzymes or
amisulpride and sertindole for quality of life This
left ventricular impairment measured by echocardiography. In the
evidence of the superior efﬁcacy and safety of clozapine is an incentive
absence of documentation of such parameters and/or suitable
to investigate clozapine-induced myocarditis further so that it can be
response to these results, this possibility remains speculative. In one
prevented, or at least the consequences minimised.
K.J. Ronaldson et al. / Schizophrenia Research 128 (2011) 161–165
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with fatal clozapine-related myocarditis, and to compare them with
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a physical illness within 4 weeks of commencing clozapine. Those
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A salary was paid to Dr Ronaldson in 2006 and 2007 from a grant from the
Lee, C.H., Tsai, W.C., Hsu, C.H., Liu, P.Y., Lin, L.J., Chen, J.H., 2006. Predictive factors of a
Australian National Health and Medical Research Council (NHMRC). Professor
fulminant course in acute myocarditis. Int. J. Cardiol. 109 (1), 142–145.
Fitzgerald is supported by an NHMRC Practitioner Fellowship. The NHMRC had no
Leucht, S., Corves, C., Arbter, D., Engel, R.R., Li, C., Davis, J.M., 2009. Second-generation
input into study design, interpretation of data or decision to publish.
versus ﬁrst-generation antipsychotic drugs for schizophrenia: a meta-analysis.
Lancet 373 (9657), 31–41.
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Professor McNeil conceived of the study of clozapine and myocarditis and has had a
clozapine therapy: myocarditis, venous thromboembolism. Prescriber Update 20,
supervisory role in the conduct of the project. Dr Ronaldson conducted the data
collection and analysis and wrote the paper. Dr Taylor was the adjudicator determining
whether each potential case met the case deﬁnition. Professor Fitzgerald proposed
Meeker, J.E., Herrmann, P.W., Som, C.W., Reynolds, P.C., 1992. Clozapine tissue
analysis that could be conducted, using the data collected. All authors contributed to
concentrations following an apparent suicidal overdose of Clozaril. J. Anal. Toxicol.
and approved the ﬁnal shape of the manuscript.
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Clozapine treatment for suicidality in schizophrenia: International Suicide
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Professor McNeil has acted as a consultant for Mayne Pharma, one of the sponsors
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for clozapine in Australia, and for Hospira Australia after the takeover in 2007. Dr
clozapine. J. Clin. Psychopharmacol. 25 (1), 32–41.
Ronaldson, Prof Fitzgerald, Dr Taylor and Prof Topliss have declared no conﬂicts of
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drugs and the risk of sudden cardiac death. N. Engl. J. Med. 360 (3), 225–235.
Ronaldson, K.J., Taylor, A.J., Fitzgerald, P.B., Topliss, D.J., Elsik, M., McNeil, J.J., 2010.
Diagnostic characteristics of clozapine induced myocarditis identiﬁed by an
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Pathologist, Department of Forensic Medicine, NSW Health & Clinical Professor,
discontinuing clozapine: matched, case–control comparison with risperidone long-
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Annamraju, S., Sheitman, B., Saik, S., Stephenson, A., 2007. Early recognition of
Walker, A.M., Lanza, L.L., Arellano, F., Rothman, K.J., 1997. Mortality in current and
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