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WILDERNESS & ENVIRONMENTAL MEDICINE, 26, 380–383 (2015)
CASE REPORT
Russula subnigricans Poisoning: From Gastrointestinal
Symptoms to Rhabdomyolysis
Shide Lin, MD; Maoyuan Mu, MM; Fangwan Yang, MM; Chunfei Yang, BSM
From the Department of Infectious Diseases, First Affiliated Hospital of Zunyi Medical College, Zunyi, China (Dr Lin, Ms. Mu, and Mr F Yang);
and the Department of Internal Medicine, People’s Hospital of Dejiang County, Dejiang, China (Mr C Yang).
Wild mushroom poisoning is often reported to cause acute liver or renal failure. However, acute
rhabdomyolysis caused by wild mushroom poisoning has rarely been reported. We describe 7 patients
of 1 family with Russula subnigricans Hongo poisoning. Their clinical manifestations varied from
gastrointestinal symptoms to rhabdomyolysis, with 1 fatality. Our report provides supporting evidence
that rhabdomyolysis may result from ingestion of R subnigricans mushrooms. A key to survival for
patients with rhabdomyolysis caused by R subnigricans poisoning may be early recognition and
intensive supportive care.
Key words: rhabdomyolysis, mushroom poisoning, Russula subnigricans, basidiomycete
Introduction
More than 2000 species of mushrooms found worldwide
are safe for human consumption, but there are also many
wild mushrooms that are toxic.
1
In China, edible mush-
rooms are readily available, inexpensive, and widely
consumed. Wild poisonous mushrooms may closely
resemble those that are edible and can be accidentally
ingested. Thus, outbreaks of wild mushroom poisoning
frequently occur in rural areas of China. From 1994 to
2012, the Chinese Center for Disease Control and
Prevention (CDC) reported 311 mushroom poisoning
events, with 1954 poisoning cases and 409 deaths.
2
Poisoning caused by the “death cap”mushroom
Amanita phalloides has often been reported.
3
It is one
of the most toxic wild mushrooms in the world and can
cause acute liver failure and death in humans.
4,5
Cortinarius species have also been reported to cause
renal failure.
6,7
However, wild mushroom poisoning as
the cause of rhabdomyolysis has rarely been reported.
We describe a family of 7 patients poisoned by Russula
subnigricans Hongo wild mushrooms. Their clinical
manifestations varied from gastrointestinal symptoms
to rhabdomyolysis, with 1 fatality.
CASE REPORTS
Seven people from 1 family, including 4 women (age
range, 15–51 years) and 3 men (age range, 18–58 years),
ingested wild mushrooms on July 19, 2013. They were
hospitalized on July 20, 2013, with nausea, vomiting,
diarrhea, and dizziness. One patient had picked wild
mushrooms in the forests of Shiqian county, Guizhou
province, China, and all 7 patients had consumed 10 to
100 g of the mushrooms after cooking them at home,
20 hours before admission. At admission, all patients had
fatigue and muscle weakness and 5 patients had myalgia,
mainly in the upper parts of the legs. No fever was noted.
All patients had normal blood pressure. The findings on
physical examination, which included cardiopulmonary
auscultation and a neurologic assessment, were
unremarkable.
On admission, initial screening tests showed serum
creatine kinase (CK) levels were elevated in 6 patients
(Table). The median levels of CK, aspartate amino-
transferase (AST), and alanine aminotransferase (ALT)
were 2063 U/L (range, 126–66,950 U/L; normal, 38–174
U/L), 151 U/L (range, 24–636 U/L; normal, o40 U/L),
and 32 U/L (range, 12–178 U/L; normal, o50 U/L),
respectively. Coagulation tests and serum creatinine
(SCr) levels were normal. Three patients had hypok-
alemia (range, 3.02–3.41 mmol/L; normal, 3.50–5.30
mmol/L), and 2 patients had hypocalcemia (range, 2.06–
2.16 mmol/L; normal, 2.20–2.65 mmol/L).
Corresponding author: Shide Lin, MD, Department of Infectious
Diseases, Zunyi Medical College, 201 Dalian Street, Zunyi, Guizhou
563003, China (e-mail: linshide6@hotmail.com).
Because 6 patients had elevated serum CK levels,
rhabdomyolysis and acute myocarditis were suspected.
However, the absence of abnormalities on electrocardio-
gram and echocardiography ruled out a cardiac origin
for the increased serum levels of CK. Initially, gastric
lavage was performed in all patients, together with fluid
replacement. The patients were also treated with pen-
icillin G (400,000–500,000 U/kg per day, intravenous)
and silybin (silibinin; 10–20 mg/kg per day, oral).
The serum CK values in 4 of the 6 patients who
survived further increased on the day after admission
(Figure 1), their weakness worsened, and production
of dark urine was observed; and hypokalemia (range,
3.23–3.43 mmol/L) and hypocalcemia (range, 1.88–2.16
mmol/L) were found. These 4 patients were subse-
quently treated with hemodialysis to prevent acute
kidney injury. From the third day, their serum CK
levels gradually declined to the standard range, and
they experienced progressive recovery of muscle
strength.
In the 1 patient who died, weakness and myalgia
worsened during the first 12 hours after admission, and
dark urine was also observed. Arterial blood gas values
while breathing 50% inspired oxygen were a pH of 7.26,
PO
2
of 97.54 mm Hg, PCO
2
of 44.78 mm Hg, and HCO
3
–
of 20.52 mmol/L; hypokalemia (3.02 mmol/L) was also
found. The patient was admitted to the intensive care
unit 6 hours after admission and treated with hemodial-
ysis on the second day after admission. However, on the
third day after admission, the patient had hyperthermia (a
temperature of up to 401C) and signs of severe dehy-
dration and acute myocarditis, including cardiac arrhyth-
mia, cardiovascular collapse, and widening of the QRS
complex. His serum CK level further increased and
reached 228,750 U/L, and serum calcium decreased to
1.51 mmol/L. Elevated levels of blood urea nitrogen
(53.69 mg/dL) and SCr (2.73 mg/dL) indicated renal
dysfunction (Figure 2). Fever was treated with physical
cooling methods, including strategic ice packs. Despite
intensive physiological care, including continuous veno-
venous hemofiltration, intravenous fluid, and bicarbonate
administration, the patient died on the fourth day after
admission. Autopsy was denied. During hospitalization,
although his serum ALT and aspartate aminotransferase
levels also increased, the serum total bilirubin and
coagulation tests remained normal.
Table. Background data and laboratory findings of 7 patients with Russula subnigricans poisoning at the time of admission
Normal range Patient 1 Patient 2 Patient 3 Patient 4 Patient 5 Patient 6 Patient 7
*
Age, y –58 51 14 15 18 15 50
Sex –MFFFMFM
ALT, U/L o40 178
†
54
†
15 27 12 32 51
CK, U/L 38–174 31,590
†
66,950
†
2063
†
285
†
281
†
126 10,610
†
sCr, mg/dL 0.46–1.23 0.91 0.80 0.62 0.71 1.09 0.71 0.84
Tbil, μmol/L o22 16.6 11.3 19.5 11.4 17 12.9 19.8
ALT, alanine aminotransferase; CK, creatine kinase; sCr, serum creatinine; Tbil, total bilirubin.
n
The only patient to die; all other patients recovered.
†
Above normal limits.
0
20000
40000
60000
80000
100000
12345678910
CK (U/L)
Days after admission
patient 1
patient 2
patient 3
patient 4
patient 5
Figure 1. Serum creatine kinase (CK) levels in 5 patients who
survived during hospitalization.
0
0.5
1
1.5
2
2.5
3
0
50000
100000
150000
200000
250000
123
sCr (mg/dl)
CK (U/L)
Days after admission
CK
sCr
Figure 2. Serum creatine kinase (CK) and serum creatinine (sCr)
levels in the patient who died during hospitalization.
Rhabdomyolysis by Russula Mushroom 381
MUSHROOM IDENTIFICATION
Mushroom samples (Figure 3) were sent to our hospital
and identified as R subnigricans Hongo by a mycologist
from the Mushroom Research Institute of Shanghai
Academy of Agricultural Science.
Discussion
The world geographic distribution of R subnigricans is
not completely defined, although it has been identified in
the United States, China, and Japan. In China, R
subnigricans grows in several southern provinces. The
mushrooms are often confused with those of the similar
species Russula nigricans, which is less poisonous. The
differentiating features of these 2 species are that the
flesh of R subnigricans is white but turns red when
damaged. The flesh of R nigricans is initially white, then
red, and turns black when damaged.
8
Rhabdomyolysis is a clinical syndrome caused by
severe injury to skeletal muscle, leading to the release of
the intracellular muscle constituents into the circulation
and extracellular fluid. The most common cause of
rhabdomyolysis is muscular trauma; the other causes of
rhabdomyolysis include medications, hyperthermia, tox-
ins, infections, and endocrinopathies,
9
but neither muscle
ischemia nor unconsciousness was noted before the
onset of symptoms in our patients. Drug intoxication
could also be ruled out because none of the patients had
taken any drugs within 1 month before the onset of
symptoms. The patients collected the mushrooms from
the nearby mountain, and the mushrooms were carefully
washed before cooking, so the possibility of contamination
with pesticides as a cause of rhabdomyolysis was also ruled
out. Therefore, we concluded that the rhabdomyolysis was
caused by the wild mushroom R subnigricans.The
individual differences in the clinical manifestations of
poisoning among the patients may be related to the
different amounts they ingested. The patient with normal
CK level (patient 6; Table) had consumed the smallest
amount of mushroom.
Examples of rhabdomyolysis caused by wild mush-
room poisoning have been reported rarely worldwide. In
France, large quantities of the wild mushroom
Tricholoma equestre was reported to cause delayed
rhabdomyolysis in 12 patients, 3 of whom died.
10
In
Taiwan, an outbreak of R subnigricans poisoning was
reported, in which 2 patients progressed to rhabdo-
myolysis, and 7 patients recovered in 1 day with
supportive care at home.
8
In a recent report of 183
patients who died of mushroom poisoning from 1994 to
2012 in southern China, 24.59% of the deaths were caused
by R subnigricans. However, whether rhabdomyolysis was
the main cause of death in patients with R subnigricans
poisoning is not known.
2
Herein, we provide further
evidence that fatal rhabdomyolysis may result from wild
mushroom R subnigricans poisoning. Physicians should
be aware of the possibility of severe rhabdomyolysis after
large quantities of R subnigricans have been consumed.
Several toxins have been found in R subnigricans. Six
chlorinated phenyl ethers, designated russuphelins A, B,
C, D, E, and F, were isolated from R subnigricans by
Takahashi et al.
11,12
Russuphelin A was cytotoxic to
various solid tumor cells, and russuphelins B, C, and D
were cytotoxic to P388 leukemia cells in vitro. Recently,
Matsuura et al.
13
isolated the small, highly strained
cycloprop-2-ene carboxylic acid from Asian R subnigri-
cans. This compound was associated with fatal rhabdo-
myolysis in mice. However, whether this carboxylic acid
is also responsible for fatal rhabdomyolysis in humans
remains unknown.
A phalloides is the most toxic mushroom and the
major cause of mortality caused by mushroom ingestion
worldwide. In China, most patients with wild mushroom
poisoning cannot identify the wild mushrooms they
consumed. It is important for physicians to judge quickly
and correctly the potential toxicity of wild mushrooms
from clinical manifestations and initial laboratory exami-
nations to give reasonable and timely treatment.
However, most patients with wild mushroom poisoning
have only gastrointestinal symptoms during the first
Figure 3. Russula subnigricans mushrooms.
Lin et al382
24 to 48 hours.
14
Therefore, it is currently difficult to
distinguish A phalloides from R subnigricans poisoning.
In the present case study, most of the 7 patients
presented with obvious myalgia and elevated CK on
admission, and their CK levels further increased after
admission. Moreover, although their serum ALT levels
increased after admission, coagulation tests remained
normal. All these clinical features distinguish R
subnigricans from A phalloides poisoning. However,
because some patients with A phalloides poisoning may
also have elevated CK levels,
15
serum CK levels cannot
be used as a definitive way to differentiate R
subnigricans from A phalloides poisoning.
In conclusion, the experience of this group of patients
suggests that clinical presentations of patients with R
subnigricans poisoning can vary from gastrointestinal
symptoms to fatal rhabdomyolysis. Most of the patients
with rhabdomyolysis caused by R subnigricans poison-
ing presented early with myalgia, accompanied by
sustained increase of serum CK. A key to survival for
patients with rhabdomyolysis caused by R subnigricans
poisoning may be early recognition and intensive
supportive care.
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