THE JOURNAL OF INFECTIOUS DISEASES • VOL. 141, NO.

6· JUNE 1980
© 1980 by The University of Chicago. 0022-1899/80/4106-0005$00.75

Plague in Camels and Goats: Their Role in Human Epidemics

A. B. Christie, * T. H. Chen, and Sanford S. Elberg From Liverpool, England; and the Medical Microbiology
and Immunology Laboratory, School of Public Health,

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University of California, Berkeley, California

In 1976, in a small, remote Libyan village, one apparently sick camel was slaughtered
and skinned, and the camel meat was distributed for human consumption. A few days
later, 15 villagers suffered a severe febrile illness. Of the five individuals who had partie-
ipated in the killing and dispensation of the camel, all were dead within four days.
When samples of serum from nine of the remaining patients were examined, seven were
found to be positive for plague as determined by the passive hemagglutination test.
Another six persons became ill after killing two goats, and the serum of one goat con-
tained antibodies to Yersinia pestis. Because all of the remaining patients except one
were treated early enough, they recovered. These incidents confirm previous reports
that the camel and the goat are susceptible to naturally occurring plague infection and
have a significant role in the dissemination of human plague.

There is an extensive literature implicating camels
in human plague epidemics. This phenomenon
was observed as early as 1907 by N. N. Klodnisk
and cited by Fedorov [1]. Wu et al. [2] and Pollit-
zer [3], reviewing early reports of camel plague in
the past, noted that such reports were received
with skepticism by many researchers of the dis-
ease. Some authorities considered that camels can
contract plague under natural conditions through
contamination of their forage by plague-infected
rodent feces and the like. Conversely, numerous
experts remained unconvinced of the camel's sus-
ceptibility to plague and adopted a "wait and see"
attitude. This conflict of opinion led Fedorov [1]
and his colleagues to investigate again the suscep-
tibility of the camel to plague infection, either
transmitted experimentally by infected ticks and
fleas or by injections of plague bacilli via various
routes. They concluded that, although these ani-
mals did vary slightly in susceptibility to plague,
the mechanisms of their infection were the same as
in plague-susceptible rodents and in humans.
Camels can be infected by fleas and occasionally
Received for publication October 23, 1979, and in revised
form January 29, 1980.
We thank Dr. Mufta Usta Omar, Secretary of Health,
Socialists People's Libyan Jamahiriyah, for permission to
publish these data, and Professor Kamil Shawki of the Depart-
ment of Community Medicine, University of Garyounis,
Benghazi, for his collaboration in some preliminary studies.
Please address requests for reprints to Dr. T. H. Chen,
School of Public Health, University of California, Berkeley,
California 94720.
• Present address: 2 Beach Lawn, Waterloo, Liverpool, L22
8QA England.
724
by ticks that have recently fed on septicemic,
plague-afflicted rodents-a means of infection
that Fedorov [1] attributed to mechanical trans-
mission by their piercing mouth parts.
This report concerns 19 cases of human plague,
with six deaths from contact with killing of a dis-
eased camel and goats, in Libya in 1976. Seven of
those associating with the camel were confirmed
as plague-infected by the passive HA test [4] with
the plague-specific fraction 1 as antigen. Of the
other three patients, two were found to be suffer-
ing from typhoid fever, and one had a bubo (how-
ever, no serum was obtained for serologic testing).
Case Report
The outbreak occurred on February 26, 1976, in
Al-Azzizat, a village of 215 inhabitants well to the
south of Derna in northeast Libya. A camel had
been slain and skinned, and its flesh had been
eaten by an unknown number of villagers. A few
days later, 15 individuals were admitted to the
Derna Hospital with a severe febrile illness.
Five of these patients died within the first four
days of disease-four of them were men who had
slaughtered and skinned the camel; the fifth was
the dealer who had distributed the meat. All five
were dead before a team of physicians could reach
DernaHospital on March 5, eight days after the
camel was killed. Of the remaining 10 patients,
seven were adults, and three were children. Seven
of the 10 had eaten or handled the camel meat:
they all had buboes in the axilla or neck. The
eighth patient denied handling the meat, but she
 Role ofRuminants in Human Plague
was the daughter of the dealer. She had a bubo in
the groin, and it is probable that her infection was
due to either flea-bite or other mechanical means
in connection with the infected meat.
The 10 patients were examined by one of us
(A.B.C.) on March 1~. One, a nine-year-old girl
(the daughter of the dealer), seemed quite ill and
died several days later. Two other children,
brother and sister, appeared very toxic. The boy's
abdomen was swollen and tender, and he had been
passing melanotic stools for two days. Their
father was in the same ward, and he had an axil-
lary bubo. Upon close questioning, he said that
the boy had been ill for a number of days before
the camel was killed and that the girl had been too
sick to eat any of its meat. Clinically, these two
children appeared to be suffering only from
typhoid fever, despite their close association with
plague in respect to time and place. This diagnosis
was later established by positive Widal tests [5].
The other eight patients all had buboes and
proven bubonic plague. The villagers subsequently
revealed that the camel had been ailing for some
days before slaughter (this may have been why it
was slain). It was also said to have had a swelling
in the neck.
In late June 1976, an Al-Azzizat boy, aged 12,
contracted plague. He had skinned a sick goat in a
village three kilometers away. The boy had an ax-
illary bubo and recovered with treatment. Sera
from four goats were tested by the Plague Refer-
ence Laboratory in the U.S.S.R. for antibody to
Yersinia pestis, and one was positive.
In early June 1976, five persons from a single
household in Krom-el-Kheil, a village near Tobruk
(which is about 100 kilometers east of Derna) were
admitted to the hospital. The village consists of 13
households, each separated from the others by a
compound of 50 to 100 meters. The father of one
household was the first victim, with severe plague
and symptoms of meningitis. The others afflicted
were his wife., his sister, and two children, all of
whom were treated early and recovered. A day or
two before the onset of disease, the father had
killed and skinned a sick goat, after which the skin
was treated by the women of the household and
kept in the house. Four dead rats were discovered
in the compound-two recently dead and two that
had been dead for some time. In all likelihood, the
rat fleas were the source of the goat's infection.
No dead rats were found in any of the other com-
pounds, and no other villagers became ill. The
725
sera of four of the patients were positive for
plague (as determined by the U.S.S.R. Plague
Reference Laboratory).
The nine serum samples obtained from patients
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in the Derna Hospital who had been in contact
with the sick camel were examined by HA [4] for
the detection of specific antibody to plague, as
well as for tularemia by the tularemia agglutina-
tion test to eliminate the possibility that this
disorder was also involved. The universally ac-
cepted HA test [4, 6] for diagnosing plague is
highly reliable because it uses purified fraction 1
antigen, which is specific for Y. pestis and does
not cross-react with Francisella tularensis or any
other pathogens. Moreover, the death rate for un-
treated tularemia is much lower than that for
plague, about 5% for the ulceroglandular form
and 30% for the typhoidal or pulmonary form.
HA antibodies to the specific fraction 1 antigen of
Y. pestis were present in the sera of seven patients
by 10-15 days after infection (that is, from the day
of the camel-slaying). Table 1 records the HA
titers of these seven individuals and the titers of
the two children who contracted typhoid fever.
Summary
To recapitulate, the seven seropositive patients
and the one who was not serologically tested all
had buboes in the neck, axilla, or groin. These
seven patients all survived bubonic plague after
treatment with streptomycin or tetracycline or
Table 1. HA antibody titers of nine patients, seven of
whom were infected with plague and two with typhoid
fever.
Reciprocal HA titer on in-
dicated number of days after
camel slaughtering
Patient 10 15
1 32 256
2 128
3 32
4 8
5 32 128
6 32
7 32
8* o
9* 0
NOTE. All sera tested were negative for tularemia. Three
dots = no serum obtained.
* Patient no. 8, a small boy, and no. 9, his sister, had typhoid
fever, a diagnosis confirmed by a positive Widal test.
726
both, but the course of treatment is unknown to
us. Clearly, the six who died and the seven survi-
vors contracted the disease from the camel,
whether by participating in the killing, skinning,
handling the camel, and/or eating the meat. In the
light of this observation, there can be no doubt
that the six fatalities and even the patient without
serologic proof of the disease represented cases of
plague, as evidenced by their close association
with the animal, which was similar to that of the
seven seropositive patients.
Although we cannot pinpoint the exact source
of infection in the camel, it is very likely that the
infective, contaminated ingredients of rodent
forage eaten by the camel (in accordance with
Nikanoroff's [7] suggestion in 1926) or infected
fleas were the culprits. Since the camel resided in
one of the natural plague foci and dead rats were
found in the vicinity, these would logically appear
to be the avenues of infection. Moreover, the
swelling in the camel's neck constitutes strong evi-
dence that the infection originated either through
the mouth or from flea bites, resulting in the de-
velopment of the bubo.
Thus, these circumstances should confirm
earlier reports that the camel is subject to natural
infection and assumes a significant role in the dis-
semination of human plague. There were no past
records of human plague transmitted via sick
camels, even though villagers have virtually lived
with the camels-the main danger lay in the killing
and handling of the infected meat. Awareness and .
early recognition of illness in such animals that in-
habit a natural plague focus are by far the most
important steps in preventing human infections.
Vaccination (recommended by Fedorov [1]) may
be applicable to these animals in geographic areas
where intensive epizootics occur among the
rodents . We conclude that camels do indeed
number among the dangerous natural contractors
Christie, Chen, and Elberg
of plague and spread the disease to humans and
that this can happen when plague epizootics in
rodents evolve.
The killing and skinning of goats have infected
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a number of people in plague areas. All patients
recovered with early treament. We regard the goat
as a sentinel animal, indicative of plague in a given
focus and not necessarily the immediate cause of
cases in humans. Some circumstantial evidence
lends support to the observation of Naidu and his
collaborators that sheep are also susceptible to
plague, as cited by Wu et al. [2]. In January 1977
six fatal cases of bubonic plague occurred in the
area of Jadu, southwest Libya, among persons, all
but one of whom had a history of slaughtering
sheep that were judged by the shepherds to be
almost dying (authors' unpublished observations).
Y. pestis was isolated in this outbreak, a result
suggesting again the potential hazard to humans
by direct contact with the carcasses of plague-
infected sheep and/or goats.
References
1. Fedorov, V. N. Plague in camels and its prevention in the
USSR. Bull. W.H.O. 23:275-281, 1960.
2. Wu, L. T., Chu, J. W. H., Pollitzer, R., Wu, C. Y. Plague:
a manual for medical and public health workers.
Weishengshu National Quarantine Service, Shanghai,
1936, p. 232-235.
3. Pollitzer, R. Hosts of the infection. In Plague. W.H.O.
Monogr. Ser. no. 22. Geneva, 1954, p. 305-308.
4. Chen, T. H., Meyer, K. F. An evaluation of Pasteurella
pestis fraction I specific antibody for confirmation of
plague infections. Bull. W.H.O. 34:911-918, 1966.
5. Widal, F. Serodiagnostic de al fievre typhoide. Bull. Mem.
Soc. Hop. (Paris), Ser. 3. 13:561-566, 1896.
6. W.H.O. Expert Committee on Plague, Fourth Report.
W.H.O. Tech. Rep. Ser. 447:23-25, 1970.
7. Nikanoroff, S. M. Di Rolle der Kamele in der Epidemiolo-
gie der Astrachaner Pest. Zentralbl. Bakteriol. [Natur-
wiss.] 98:24-37, 1926.