Malaria transmission in non-endemic areas: case report, review of the literature and implications for public health management.

Abstract

In non-endemic areas, malaria is rare and locally acquired infections, particularly with Plasmodium falciparum, are exceptional events. The diagnosis is, therefore, likely to be delayed or missed in patients without a relevant travel history. This report describes a case of falciparum malaria in Berlin, Germany, in a patient who had not been to an endemic area for more than a decade. Potential routes of vector-related and direct transmission were evaluated, particularly with regard to a possible danger to the public. A review of the literature was conducted regarding possible routes of transmission and their probability assessed. Genotyping of parasite isolates of this and another patient with malaria admitted 16 days before revealed homology between the two strains. In a local entomological survey, anopheline vectors on the hospital grounds as well as in the residential area of both patients were found. Despite intensive investigations, the mode of transmission remained obscure. In this context, possible routes of vector-borne and direct occupational/accidental transmission in a major European city are reviewed and discussed, providing information and guidance in case other similar events occur elsewhere. Examples for investigations and measures to be taken in such a situation are provided. When local malaria transmission within a large non-immune population cannot be ruled out, genotyping of parasite isolates, local entomological surveys, preparedness for secondary cases, expert consultations in a multidisciplinary team and careful information management are essential. Malaria acquired in non-endemic areas remains an unlikely, but possible event for which awareness needs to be maintained.

Full text

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Malaria Journal
Open Access
Case report
Malaria transmission in non-endemic areas: case report, review of
the literature and implications for public health management
Thomas Zoller1, Torsten J Naucke2,3, Jürgen May4, Bodo Hoffmeister1,
Holger Flick1, Christopher J Williams5, Christina Frank*5, Frank Bergmann1,
Norbert Suttorp1 and Frank P Mockenhaupt6
Address: 1Medizinische Klinik mit Schwerpunkt Infektiologie und Pneumologie, Charité – Universitätsmedizin Berlin, Augustenburger Platz 1,
13353 Berlin, Germany, 2Institut für Medizinische Mikrobiologie, Immunologie und Parasitologie (IMMIP), Universitätsklinikum Bonn, Sigmund
Freud Straße 25, 53105 Bonn, Germany, 3Institut für Zoologie, Fachgruppe Parasitologie, Universität Hohenheim, 70599 Stuttgart, Germany,
4Bernhard Nocht Institute for Tropical Medicine, Infectious Disease Epidemiology, Bernhard-Nocht-Straße 74, 20359 Hamburg, Germany,
5Robert-Koch-Institut, Department for Infectious Disease Epidemiology, Seestraße 10, 13353 Berlin, Germany and 6Institute of Tropical Medicine
and International Health, Charité – University Medicine Berlin, Spandauer Damm 130, 14050 Berlin, Germany
Email: Thomas Zoller - thomas.zoller@charite.de; Torsten J Naucke - tjnaucke@aol.com; Jürgen May - may@bni-hamburg.de;
Bodo Hoffmeister - b.hoffmeister-infekt@charite.de; Holger Flick - holger.flick@charite.de;
Christopher J Williams - christopher.williams@norfolk.nhs.uk; Christina Frank* - FrankC@rki.de;
Frank Bergmann - frank.bergmann@charite.de; Norbert Suttorp - norbert.suttorp@charite.de;
Frank P Mockenhaupt - frank.mockenhaupt@charite.de
* Corresponding author
Abstract
In non-endemic areas, malaria is rare and locally acquired infections, particularly with Plasmodium
falciparum, are exceptional events. The diagnosis is, therefore, likely to be delayed or missed in
patients without a relevant travel history. This report describes a case of falciparum malaria in
Berlin, Germany, in a patient who had not been to an endemic area for more than a decade.
Potential routes of vector-related and direct transmission were evaluated, particularly with regard
to a possible danger to the public. A review of the literature was conducted regarding possible
routes of transmission and their probability assessed. Genotyping of parasite isolates of this and
another patient with malaria admitted 16 days before revealed homology between the two strains.
In a local entomological survey, anopheline vectors on the hospital grounds as well as in the
residential area of both patients were found. Despite intensive investigations, the mode of
transmission remained obscure. In this context, possible routes of vector-borne and direct
occupational/accidental transmission in a major European city are reviewed and discussed,
providing information and guidance in case other similar events occur elsewhere. Examples for
investigations and measures to be taken in such a situation are provided. When local malaria
transmission within a large non-immune population cannot be ruled out, genotyping of parasite
isolates, local entomological surveys, preparedness for secondary cases, expert consultations in a
multidisciplinary team and careful information management are essential. Malaria acquired in non-
endemic areas remains an unlikely, but possible event for which awareness needs to be maintained.
Published: 20 April 2009
Malaria Journal 2009, 8:71 doi:10.1186/1475-2875-8-71
Received: 26 November 2008
Accepted: 20 April 2009
This article is available from: http://www.malariajournal.com/content/8/1/71
© 2009 Zoller et al; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Background
Transmission of malaria in a non-endemic area is an
extremely unusual event, but is possible under certain
conditions. For those affected, the combination of a
missed or delayed diagnosis along with the high fatality of
Plasmodium falciparum infection may result in serious con-
sequences. These rare occasions pose a challenge to local
and public health authorities.
In the European Union, 6,000–10,000 imported cases of
malaria and 26 to 78 attributable deaths have been
reported annually between 1994 and 2006 [1]. In sick
travellers returning from malaria-endemic areas, a
detailed travel history is mandatory and malaria must be
excluded. Plasmodium falciparum-infected individuals
without a relevant travel history are at high risk of a
delayed/missed diagnosis and, consequently, of develop-
ing potentially life-threatening severe falciparum malaria.
Local transmission leading to isolated malaria cases in
non-endemic regions has occurred under various circum-
stances including (i) "airport", (ii) "port", and (iii) "bag-
gage" malaria, (iv) nosocomial transmission and (v)
transmission by local competent vectors. Also, small
malaria epidemics with continued localized transmission
occurred in northern Germany and Berlin up to 1947 [2],
and, more recently, in the USA [3].
With the aim to raise awareness for the potential of locally
acquired malaria and to provide information and guid-
ance, this report discusses possible routes of vector-borne
and occupational/accidental transmission. As an example
for investigations and measures to be taken in such a situ-
ation, a case of local transmission of P. falciparum in Ber-
lin, Germany, which occurred in July 2007 is presented.
Case presentation
A consultant physician of the Department of Obstetrics &
Gynaecology presented to the emergency room of the
same university hospital in Berlin on 26 July 2007. She
reported a four-day history of fever and headache. Com-
mon causes of fever were ruled out. On questioning, the
patient stated that she had never been to Asia or Africa.
However, she had travelled to Colombia eleven years
before where she contracted malaria. Despite an extremely
low probability of a tertian malaria relapse after this time,
thick and thin blood films were examined, revealing Plas-
modium falciparum at a density of 0.5% parasitized eryth-
rocytes. Plasmodium falciparum mono-infection was
confirmed by PCR [4]. Other laboratory abnormalities
included a thrombocytopaenia of 50/nL, an elevated C-
reactive protein of 9.74 mg/dL, and leukocyturia. The
patient was treated with oral artemether/lumefantrine
and recovered fully within three days.
Because the travel history was not consistent with
imported malaria, an investigation for a local source of
infection was carried out. A pregnant patient with falci-
parum malaria (hereafter referred to as the "primary
case") had been admitted to the delivery room on 10 July
2007, 16 days before the consultant was diagnosed with
malaria. The primary case had returned to Berlin from a
four-weeks visit to the Ivory Coast on 30 June 2007. She
had taken no chemoprophylaxis. Ivorian born, she had
been a Berlin resident for 7 years. After returning to Berlin,
she developed fever on 8 July 2007. On admission, she
presented with a P. falciparum mono-infection (PCR con-
firmed) with 3% parasitaemia. She was treated with
mefloquine, recovered fully and was discharged from hos-
pital on 16 July 2007. For a timeline of events, see Figure
1.
The consultant ("secondary case") encountered the pri-
mary case in person on only two occasions, once in the
evening of admission to the labour ward (10 July) and
then again the following morning. The secondary case,
supervising the resident physicians, could not recall any
direct physical contact on these two occasions, apart from
possibly shaking hands. In particular, the consultant did
not perform any medical procedures on the primary case
at any time during the entire hospital stay, nor did she
recall any needlestick injuries. On one occasion, the con-
sultant hand-carried a fully bagged blood sample of the
primary case, which had been collected by another physi-
cian on admission; she could, however, not recall seeing
any blood on the outside of the bag.
Methods and results regarding possible modes of
transmission and management
Suspecting local malaria transmission, all possible routes
of transmission, as outlined above, had to be considered
at the outset. One scenario included a possible danger to
the public from infective mosquito(es) present on the
hospital compound or in the residential area where both
cases live.
Genetic homology of parasite strains
Parasite isolates from primary and secondary case were
genotyped for the highly polymorphic P. falciparum msp-1
and msp-2 genes [5]. The results revealed complete homol-
ogy. This was confirmed in a second laboratory with a sec-
ond set of samples and by extending genotyping to PfRRM
microsatellite markers [6] and polymorphic DBL-alpha
sequences [7]. In contrast, human microsatellite markers
showed dissimilarity between the two samples, excluding
a mix-up or contamination of the samples taken from
both cases [6].

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Patient interviews
Sources of occupational or accidental inoculation
The delivery room and maternity wards were thoroughly
inspected and all persons directly or indirectly involved in
the management of the primary case were repeatedly
interviewed. No exposures compatible with a nosocomial
transmission could be recalled. In particular, the absence
of physical contact between index and secondary case was
confirmed independently. The secondary case did not
recall any injections, accidents or blood transfusions in
the months preceding the malaria episode. She had no rel-
evant skin damage during the possible direct-transmis-
sion window, apart from a small dressed wound on the
wrist following a horsefly bite. Moreover, she stated that
this wound had begun to close by the 10th July 2007. She
could not recall changing the dressing whilst on the
wards.
Baggage malaria
The index patient had used the same baggage both for her
trip to the Ivory Coast and her hospital admission 11 days
after returning. Both index patient and her husband stated
that the bags had been completely emptied after returning
to Berlin, and on inspection, nothing unusual was
observed.
Contact or transmission in residential area
Further interviews with the two patients revealed that
both live in the same, densely populated residential area
of Berlin, approximately 1.8 km apart from each other.
Timeline of events
Figure 1
Timeline of events. Vector-borne transmission (upper part): theoretical minimum time for sporogony is 10 days under African
temperature conditions. Under temperatures in Berlin during this time, at least 21 to 24 days can be expected (see text for
details) – sporogony periods for both hospital and residential vector transmission are too short, arguing against this possibility
of transmission. Direct/occupational exposure (lower part): only during the stay of the index patient on the obstetrics ward, there
was a theoretical possibility of direct inoculation of infectious material, a short incubation time of 4 up to17 days can be
expected. Occurrence of symptoms on 22 July was within the time frame to be expected for this scenario.

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However, none of the places frequently visited by the
patients in their daily activities were common to both.
Entomological survey
In August 2007, an entomological survey on the hospital
compound and the patients' area of residence was carried
out. In both places, viable Anopheles larvae were found: on
the hospital compound in small quantities in a fountain,
and in the residential area in a backyard water butt. Mor-
phological examination of the Anopheles larvae identi-
fied them as the species-complex Anopheles maculipennis
s.l., which includes species with potential vectorial com-
petence [8,9]. Adult Anopheles mosquitoes were not
found.
Information management of the suspected outbreak
situation
Meanwhile, the federal health administration of Berlin
convened a panel, which included infectious disease and
public health specialists, along with communications
officers. Although the occurrence of other mosquito-
transmitted secondary cases seemed unlikely, this risk
could not completely be ruled out at the time of the inves-
tigation. A selective approach to risk communication was
used, with an alert sent only to hospitals in Berlin with
emergency departments. The alert advised clinicians to
consider malaria in cases of unexplained fever, particu-
larly when coinciding with thrombocytopaenia. No fur-
ther, presumably locally acquired, P. falciparum infections
were reported to the health authorities. Public media did
not report the incident.
Discussion
Malaria has been endemic in Europe and particularly
around the North Sea at least from the 7th century until the
late 1950s [10]. Martini [11] reported an epidemic on the
German North Sea coast in 1826 with several thousand
cases and many casualties; transmission was facilitated by
unusually high summer temperatures. The last reported
cases of autochthonous tertian malaria were observed in
Berlin and Hamburg in 1947 [2]. Plasmodium falciparum is
thought to have never been endemic in Germany, but
continues to be imported by travellers returning from
endemic areas.
In the last six decades, only three cases of potentially local
P. falciparum transmission have been reported from Ger-
many. One of these, involving presumed transmission by
local Anopheles plumbeus on a hospital compound in Duis-
burg, Western Germany, shows some parallels to the case
reported here [12]. Two simultaneous cases of supposed
mosquito-borne infection occurred in 1994 close to a
sewage plant in Berlin [13]. In the present case, genetic
analysis of parasite isolates did confirm the index patient
as the source of the infection in the secondary patient.
Requirements for local mosquito transmission
Larvae of A. maculipennis s.l. were identified both on the
hospital compound and in the patients' residential area.
The time period required for completion of sporogony
(extrinsic incubation time) is critical in determining the
likelihood of mosquito-borne transmission. This period is
highly temperature-dependent, but usually takes at least
seven days under optimal average ambient temperatures
in Africa of 35°C [14] and up to 30 days under ambient
temperatures of 20°C [2]. Mosquitoes of the A. maculipen-
nis-species complex are potential vectors of P. falciparum
[15].
Transmission by local Anopheles mosquitoes on the
hospital compound
In Berlin, temperatures were exceptionally high exactly
during the time of potential extrinsic incubation with
night minimum temperatures >14°C in two nights and
>17°C in the following five nights. Local temperature
data was analysed and a probable extrinsic incubation
time of 21 to 24 days calculated for P. falciparum [2]. Mos-
quitoes resting within buildings (e.g. in the basement)
may have been exposed to higher average temperatures.
Adding to the extrinsic incubation period, the minimum
intrinsic incubation time of P. falciparum infection in
human experimental malaria is estimated as seven days
[16]. Assuming local transmission by anopheline vectors,
the entire incubation period in this case (extrinsic and
intrinsic) would amount to a minimum of 28 days, based
on theoretical considerations using experimental data cur-
rently available. This, however, exceeds the timespan of
11 days between the index patient's admission and first
symptoms in the secondary case (see Figure 1) arguing
against a mosquito-borne transmission on the hospital
grounds.
Transmission by local Anopheles in the residential area
The index and the secondary patient live in the same cen-
trally located borough of Berlin, some 1.8 km apart. After
returning from Ivory Coast on 30 June, the index patient
stayed in this area for eleven days before being admitted
to hospital. Theoretically, intrinsic plus extrinsic incuba-
tion period and the presence of An. maculipennis s.l. would
allow a mosquito-borne transmission of P. falciparum in
the city. However, it would be unusual, though not
impossible, for a local anopheline species to travel more
than 2 km within a short period of time. Furthermore, it
seems very improbable that this unlikely event (of trans-
mission in the residential area) should be followed by the
even less probable coincidental meeting of index and sec-
ondary case in the same hospital as doctor and patient.
Eventually, genetic analysis showed a high degree of
homology between both parasite isolates. Although this
does not completely exclude a mosquito passage of P. fal-

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ciparum (in which sexual parasite reproduction and
genetic recombination occur), it renders both scenarios
involving vector-borne transmission unlikely.
Airport/port malaria
"Airport malaria" results from infective bites of mosqui-
toes, which travelled aboard an airplane and has occurred
in a number of instances around major airports through-
out Europe. Mosquitoes can survive a flight even in non-
pressurized wheel bays [17]. In a series of 29 respective
patients from 1969 to 1988, most cases occurred within a
distance of 2 km from the next airport, but longer dis-
tances are also possible when vectors are transported fur-
ther, for example in a car [18]. In this series, four patients
died due to a delayed or missed diagnosis and approxi-
mately one third of the cases were persons working at or
around the airport. A case of "port" malaria has been
observed about 3.5 km off the port of Ghent, Belgium
[19]. In the secondary malaria patient, an "airport"
malaria was considered due to a recent visit to Frankfurt
airport, but dismissed after genotyping results revealed
homology with the index patient's parasite strain.
Baggage malaria
The possibility of carrying infective mosquitoes within
pieces of baggage to non-endemic areas or to areas far
from international airports has been suspected in a
number of previous cases [13,20,21]. The homology of
strains in the two patients could accord with transmission
by the same mosquito. In this scenario, the mosquito was
carried in the baggage from Ivory Coast to Berlin, infected
the index case before or during travel or at home in Berlin
and then – after being transported to the hospital –
infected the secondary patient.
Nosocomial transmission
Nosocomial P. falciparum infection, in which blood or
parasite-containing fluids from a parasitaemic patient
enter the bloodstream of a secondary patient, are well-
documented. Example routes include needlestick injuries
[22-26], incorrect use of blood glucose meters [27], or fail-
ure to exchange needles using multidose drug vials [28-
30]. The incubation time following direct blood contact
or needlestick injuries ranges from 4 to 17 days (median
12 days) [31].
There is also evidence of transmission through contami-
nated surfaces. This has been implicated in cases of
malaria following re-use of catheters for contrast media
[32] or handling of intravenous lines with contaminated
gloves [33] and suggests that the infection can be passed
by an intermediate and not necessarily visibly blood con-
taminated object. However, transmission in the absence
of percutaneous or intravenous breaches has been
described only in cases of direct contact with visible and
infected blood. Published examples include a nurse with
fingertip skin scratches (caused by peeling potatoes) [34],
and a doctor with a minor nail-cutting injury; both
became infected after having venosected malaria patients
[35]. In the broader nosocomial context, self-inoculation
of patients' blood as a consequence of a psychiatric disor-
der has been reported from a German hospital, producing
a series of thirteen malaria episodes in a laboratory tech-
nician [36].
The secondary case denied any needlestick injuries, inva-
sive medical procedures performed on herself, or any con-
tact between skin breaks and visible blood or
contaminated fluids from the index case. However, her
recall may not have been perfect, as she was interviewed
nearly a month after the possible exposure time.
Probable route of transmission
In the present case of falciparum malaria acquired locally
in Berlin, Germany, the route of transmission remains
obscure despite extensive investigations. Transmission by
local Anopheles on the hospital compound seems improb-
able in view of the timeline. While incubation times
would allow for mosquito-borne transmission in the resi-
dential area, this option would require combinations of
per se unlikely events. In addition, the absence of genetic
recombination renders a mosquito-borne transmission
unlikely. "Baggage malaria" cannot be ruled out but also
appears unlikely: the mosquito would have had to survive
for 11 days in the flat in Berlin (all bags had been emp-
tied), re-enter the baggage in which it is was imported
from Ivory Coast, to be carried to the hospital where it
infected the secondary case. Nosocomial transmission
would require fewer improbable events but suffers from
the lack of a clear exposure history for the secondary case.
Implications for public health management
Because of the high fatality of undiagnosed falciparum
malaria, suspected mosquito-borne transmission in non-
endemic areas has significant public health implications.
Protecting the population, even against a hypothetical
threat, has highest priority under such circumstances.
In the case described here, mosquito-borne transmission
was assumed in the early stages of investigation. It had to
be considered that at least one infectious A. maculipennis
s.l. could pose a danger during the rest of its lifespan
(approximately six weeks, < 1 blood meal/week). In case
of "baggage malaria", Anopheles gambiae would have been
present for at least a few days on the hospital compound
(life span approximately three weeks, one blood meal
every other day). Careful information management and
adequate risk communication in such a case is essential:
missing potential further cases of autochthonous malaria
must be avoided, but the extensive media coverage that

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might have followed a wider alert was also undesirable. In
particular, with extensive media coverage, a high number
of febrile patients with other diagnosis would need to
undergo malaria testing. Here, the policy of selectively
informing key health facilities and physicians who have
initial contact with febrile patients proved to be adequate.
In parallel, preparedness for potential subsequent events
included surplus procurement of rapid test devices, alloca-
tion of further diagnostic capacity (staff, infrastructure),
daily exchange of information between stakeholders, and
training of personnel primarily involved in case of
upward disease activity. Generally, in places outside
endemic areas but with temporal presence of vectors com-
petent for transmitting malaria, artemisinin-based anti-
malarial therapy may contribute to reduce the risk of local
transmission due to the gametocidal activity of artemisi-
nins [37].
When malaria transmission within a large non-immune
population cannot be ruled out, a case definition is
required to determine which patients should undergo
testing for malaria. The most common clinical symptoms
of P. falciparum malaria among returning travellers are
fever (93%), headache (51%), musculoskeletal pain
(35%) and fatigue (32%) [38]. Suggestive biochemical
markers involve (i) thrombocytopaenia, (ii) elevation of
serum lactate dehydrogenase and (iii) anaemia. Among
more than 4,000 unselected patients in Lisbon, Portugal,
seeking care in a hospital emergency department for any
reason, the prevalence of thrombocytopenia of less than
150,000/μL, 100,000/μL, 50,000/μL was 7%, 2.2% and
0.6%, respectively. Screening all samples with a thrombo-
cyte count <100,000/μL led to the detection of five unsus-
pected malaria cases [39]. Of emergency department
patients in Lisbon and Berlin in whom malaria was clini-
cally suspected and who presented platelet counts
<150.000/μL, more than 75% were found to be positive
for malaria [39]. In a non-endemic area with a susceptible
population, a pragmatic approach to cope with hypothet-
ical P. falciparum transmission could, therefore, be to limit
malaria diagnostic testing to selected individuals, such as
those presenting with at least one malaria-suggestive
symptom and a platelet count below 150,000/μl. From
the experience with the reported, probable case of locally
acquired malaria, a set of measures outlined in Table 1 is
recommended.
Conclusion
In conclusion, the route of transmission in this unusual
case of falciparum malaria in Berlin could not be deter-
mined. With climate change improving conditions for
competent anopheline vectors in non-endemic areas, the
risk of isolated P. falciparum infections or small outbreaks
secondary to imported cases increases. This possibility
should specifically be considered in large cities with high
numbers of returning travellers and semi-immune
migrants, who may carry infective gametocytes for
extended periods of time. Due to its gametocidal activity,
artemisinin-based anti-malarial therapy should be pre-
ferred in all settings with a competent vector population.
Direct routes of transmission, such as nosocomial trans-
mission or, rarely, self-inoculation should be considered
in cases of otherwise unexpected P. falciparum infection.
Genetic comparison of malaria species can be helpful in
evaluating transmission scenarios. Even in non-endemic
areas and in the absence of a travel history, it is important
to consider malaria in patients with unexplained fever.
Consent
Written informed consent was obtained from the patient
for publication of this case report and any accompanying
images. A copy of the written consent is available for
review by the Editor-in-Chief of this journal.
Competing interests
The authors declare that they have no competing interests.
Table 1: Key recommendations for public health management in malaria infections outside endemic areas
• Rapid and regular assessment of new information by a team of clinicians, malaria experts, entomologists and public health experts
• Timeline of events with incubation times for different transmission scenarios to assess their probability
• Molecular genotyping of isolates from index- and secondary cases
• Repeated interviews of index- and secondary cases as well as all other personnel involved
• Local entomological survey
• Selectively informing key health infrastructures and physicians
• Preparation of a press release in case of public media attention

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Authors' contributions
All authors have made substantial contributions to the
investigations presented in this manuscript. TZ and FPM
drafted the manuscript and all authors and have been
involved revising it. All authors have read and approved
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