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| Parasitol Res (2003) 90: 209–211
DOI 10.1007/s00436-003-0842-5
ORIGINAL PAPER
D. Robinson Ć N. Leo Ć P. Prociv Ć S.C. Barker
Potential role of head lice, Pediculus humanus capitis,
as vectors of Rickettsia prowazekii
Received: 24 September 2002 / Accepted: 9 January 2003 / Published online: 27 February 2003
Springer-Verlag 2003
Abstract Since the pioneering work of Charles Nicolle
in 1909 [see Gross (1996) Proc Natl Acad Sci USA
93:10539–10540] most medical o.cers and scientists
have assumed that body lice are the sole vectors of
Rickettsia prowazekii, the aetiological agent of louseborne
epidemic typhus (LBET). Here we review the
evidence for the axiom that head lice are not involved in
epidemics of LBET. Laboratory experiments demonstrate
the ability of head lice to transmit R. prowazekii,
but evidence for this in the .eld has not been reported.
However, the assumption that head lice do not transmit
R. prowazekii has meant that head lice have not been
examined for R. prowazekii during epidemics of LBET.
The strong association between obvious (high) infestations
of body lice and LBET has contributed to this
perception, but this association does not preclude head
lice as vectors of R. prowazekii. Indeed, where the prevalence
and intensity of body louse infections may be
high (e.g. during epidemics of LBET), the prevalence
and intensity of head louse infestations is generally high
as well. This review of the epidemiology of head louse
and body louse infestations, and of LBET, indicates that
head lice are potential vectors of R. prowazekii in the
.eld. Simple observations in the .eld would reveal
whether or not head lice are natural vectors of this major
human pathogen.
D. Robinson Ć N. Leo Ć P. Prociv Ć S.C. Barker (&)
Department of Microbiology and Parasitology,
and Institute for Molecular Biosciences,
University of Queensland,
4072 Brisbane, Australia
E-mail: s.barker@mailbox.uq.edu.au
Introduction
For now the plague fell upon the Athenians and
devoured the .ower of their manhood and
strength. It a.icted them not only in body but
also in spirit, so they raved against Pericles and
tried to ruin him, just as a man in a .t of delirium
will attack his physician or his father (Plutarch
1960).
Although louse-borne epidemic typhus (LBET) was
suspected as the cause of the plague that beset the Athenians,
the .rst major epidemic that can be con.dently
attributed to this disease occurred in the 15th century
(Perine et al. 1992). LBET, which is caused by infection
with Rickettsia prowazekii, is one of the most devastating
illnesses to a.ict human kind. The word ‘‘typhus’’ originates
from the Greek word ‘‘typhos’’ meaning smoke,
cloud, or stupor arising from fever; it describes one of the
classic symptoms of LBET. In undernourished populations,
who already su.er poor health and hygiene, LBET
can cause substantial mortality rates (Weiss 1998). Most
medical workers and scientists consider the body louse
(Pediculus humanus humanus) to be the only vector of
R. prowazekii, yet there is strong experimental evidence
that head lice (P. h. capitis) can be competent vectors of
R. prowazekii as well (Goldberger and Anderson 1912;
Murray and Torrey 1975).
Evidence that head lice can transmit R. prowazekii
In 1909, Charles Nicolle infected a chimpanzee with
R. prowazekii, and then placed body lice onto it. After
the lice had fed, he transferred them to another chimpanzee,
which subsequently developed typhus (Gross
1996). Subsequent similar experiments with head lice
gave the same result. Goldberger and Anderson (1912)
took hair that contained head lice from patients who
were admitted to hospital with LBET, and used these
210
lice to infect rhesus monkeys with R. prowazekii. Their
.ndings were later con.rmed by Murray and Torrey
(1975), who infected head lice with R. prowazekii by
feeding these lice on a rabbit that was infected with R.
prowazekii. Murray and Torrey (1975), using labelled
antibodies to R. prowazekii, found that from the sixth
day after exposure, head lice passed infective rickettsiae
in their faeces. No other experiments have been reported
to contradict these results.
If head lice are competent vectors of R. prowazekii
in the laboratory why don’t these lice transmit
R. prowazekiiin the field?
Maunder (1983) proposed two arguments to account for
the apparent observation that infestations of body lice,
not head lice, lead to epidemics of LBET. First,
Maunder argued that the faeces of body lice are more
likely to build up in clothes than in the hair, to levels
where infection of people with R. prowazekii is likely.
However, small amounts of faeces can be infective
(Buxton 1947), and the faeces of head lice may build up
to substantial levels on the scalp, hair and on pillows of
infested people (Burgess 1995). Moreover, the dust-like
faeces of P. humanus in the hair are perfectly placed for
infection via inhalation, scratches of the scalp or the
conjunctiva and mucosal membranes. Indeed, the faeces
may be so infective that hospital cleaners in Russia who
had no direct contact with patients became infected
when washing the linen of typhus patients (Patterson
1993), presumably through inhaling louse faeces that
became airborne while they were handling the linen.
Second, Maunder (1983) argued that since body lice
are present in larger numbers than head lice during
epidemics of LBET, body lice are the principal or sole
vectors of R. prowazekii. However, there is evidence that
head lice are also present in large numbers during epidemics
of LBET. For example, in the 1975 outbreak of
LBET in Uganda, nits were found in both the hair and
clothes of patients, con.rming the presence of head lice,
but the proportion of head and body lice was not measured
(Banegura et al. 1983). Between 1981 and 1990,
Ethiopian refugee camps accounted for 69% of all reported
cases of epidemic typhus (Perine et al. 1992).
Head lice were found on 65% of these people, and close
to 100% of children, whereas only 30% of these people
had body lice (Raoult and Roux 1999). Presumably,
head lice can be present in equally large numbers during
epidemics of typhus. The fact that head lice are prevalent
in many if not all human societies that have never had
LBET reinforces the perception that head lice do not
transmit R. prowazekii. But, of course, this observation
does not exclude head lice as vectors of R. prowazekii
during epidemics of LBET, since the conditions that lead
to prevalent and intense infestations of P. h. humanus,
such as crowding, usually lead to prevalent and intense
infestations of P. h. capitis too.
There is insu.cient evidence to decide whether head
lice: (1) transmit R. prowazekii in the .eld; or (2) have an
important role in epidemics of LBET. Certainly, head
lice have the potential to be vectors of R. prowazekii in
the .eld. Moreover, the delousing procedures that have
been used in the past, and the almost universal assumption
that only body lice transmit R. prowazekii,
may have masked the role of head lice in epidemics of
LBET. Head lice are generally ignored in investigations
of typhus outbreaks. Despite this, patients are often,
perhaps always, treated for head lice. The Russian army
sterilized clothes and bedding, then washed and shaved
people’s heads to bring epidemics of LBET under
control (Patterson 1993). So it cannot be concluded that
body lice were the only vectors present in these epidemics,
since head lice were also eliminated. In the
aftermath of World War I an outbreak of LBET occurred
which threatened to cause signi.cant loss of life.
The American army responded with an extensive campaign
to control epidemic typhus in Poland between
1919 and 1920 (Foster 1981). Although the aim was to
eliminate body lice, by providing clean clothing and
blankets, the people’s heads were also shaved. The 1975
outbreak of LBET in Uganda where patients were found
with nits in their clothing and hair led to a comprehensive
campaign of delousing and treatment with
tetracycline (Banegura et al. 1983). By destroying the
rickettsiae in the host, the bacteria could not be transmitted
by any head or body lice that survived delousing.
An outbreak of LBET in a Burundi jail in 1996, attributed
to the presence of body lice, was contained with
delousing procedures that included head-shaving (Bise
and Coninx 1997; Raoult et al. 1997). While the investigators
were unsure if head lice were involved in the
epidemic, they treated patients for head lice just in case.
Thus, the role of head lice in transmission of R. prowazekii
during epidemics of LBET cannot be determined
since both head lice and body lice were eliminated.
Clearly head lice have generally been overlooked in
studies of typhus outbreaks. Even in the unusual cases
when typhus su.erers are examined for head lice, these
lice are then not tested for the presence of R. prowazekii.
For example, during the 1997 outbreak in Lipetsk,
Russia, body louse infestations were described as ubiquitous
(Tarasevich et al. 1998). However, no mention
was made about the presence of head lice, or whether the
delousing measures used to control the outbreak
included head-shaving. During a 1997 .eld study in
Burundi, 102 refugees with febrile illness were examined
to determine the prevalence of typhus within the population
(Raoult et al. 1998). Serum was collected and
body lice were removed, but once again head lice were
not collected, or examined. In a Peruvian study, (Raoult
et al. 1999), again body lice were collected and tested for
R. prowazekii, but not head lice. An interesting case
occurred in 1998, when a man returning from Algeria to
France developed louse-borne typhus (Niang et al.
1999). No evidence of body lice was found but he did
recall having pruritus of the scalp and scratching during
his stay in Algeria (Niang et al. 1999).
If head lice do transmit R. prowazekii to people, why
have there not been outbreaks of LBET in the schools,
homes and institutions of developed countries where
these parasites are prevalent? The .rst requirement is
that the aetiological agent of LBET, R. prowazekii, must
be present. Further, people generally have to be stressed
or immuno-compromised from latent infections of
R. prowazekii to su.er patent infections of LBET (i.e.
Brill-Zinsser disease) (Patterson 1993; Raoult and Roux
1999).
Conclusions
Clearly, body lice have played a role in all epidemics of
LBET investigated so far, but this does not preclude head
lice as additional vectors of R. prowazekii. This question
will be answered only when head lice are collected during
outbreaks ofLBETand examined forR. prowazekii.Head
lice from typhus patients should be examined for R. prowazekii.
However, we note infection with R. prowazekii
has often killed researchers, doctors, nurses and even
laundry workers who have only had contact with faeces
from patients sheets. Care is essential!
Acknowledgement We thank Dr. Anna Murrell for advice.
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