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Brief communication Co-detection of Bartonella quintana and Yersinia pestis in an 11thЦ15th burial site in Bondy France.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 145:489–494 (2011)
Brief Communication: Co-Detection of Bartonella
quintana and Yersinia pestis in an 11th–15th
Burial Site in Bondy, France
Thi-Nguyen-Ny Tran,1 Cyrille Le Forestier,2 Michel Drancourt,1* Didier Raoult,1 and Gérard Aboudharam1
1
Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes, UMR CNRS 6236, IRD198,
IFR48, Faculté de médecine, Université de la Méditerranée, 13005 Marseille, France
2
Institut National de Recherches Archéologiques Préventives UMR 6130, Centre d’Etudes Préhistoire, Antiquité,
Moyen Âge, Direction interrégionale Centre, Ile de France, France
KEY WORDS
dental pulp; plague; Bondy; ‘‘suicide PCR’’
ABSTRACT
Historical and anthropological data suggest that skeletons excavated from an 11th to 15th century mass grave in Bondy, France, may be those of victims of the Great Plague. Using high-throughput realtime PCR investigation of the dental pulp collected from
14 teeth from five such skeletons, we detected Bartonella
quintana DNA in three individuals and Yersinia pestis
DNA in two individuals. DNA from five other deadly
pathogens was not found. Suicide PCR genotyping confirmed Y. pestis DNA belonging to the Orientalis biotype.
One individual had co-infection. These data suggest a
plague epidemic in a population already infected by the
body louse-transmitted B. quintana or a body lousedriven transmission of the plague that drove a medieval
epidemic in inland Europe. Am J Phys Anthropol
145:489–494, 2011. V 2011 Wiley-Liss, Inc.
Historical texts and works of art have related two
massive, deadly epidemics that erupted in medieval
Mediterranean countries and swept over inland European countries during the 6th–8th centuries and the
middle of the 14th century (Perry and Fetherston, 1997;
Gage and Kosoy, 2005). Later epidemics, known collectively as the Black Death, entered Mediterranean ports
in 1347 and reached as far as Scandinavia and Russia
(Perry and Fetherston, 1997; Byrne, 2004). The Black
Death was estimated to have killed up to one-third of
the European population at that time and to have profoundly influenced the history of major medieval states
(Biraben, 1975; Cantor, 2002; Byrne, 2004).
The Black Death presented as a deadly epidemic in
which victims were afflicted with painful, inflamed
lymph nodes. These inflamed lymph nodes are highly indicative of the plague bubo, which is caused by the bacterium Yersinia pestis (Yersin, 1894). The large number
of people affected within short periods of time, the
length of the epidemics, the clustering of cases (e.g.,
household cases), and the patterns of spatial and temporal spread, however, have raised controversies regarding
the etiology of the Black Death. Indeed, these particular
epidemiological features of the Black Death were clearly
incompatible with the rat-flea transmission model commonly suggested for the plague (Wren, 2003). Because of
these inconsistencies, some scholars have denied the
potential role of Y. pestis as the causative agent of the
Black Death, and several alternative hypotheses have
been proposed, including anthrax (Twigg, 1985; Cantor,
2002), influenza (Teh et al., 1923), and hemorrhagic
fever (Duncan and Scott, 2005). None of these hypotheses, however, has received additional support from any
experimental data.
One paleomicrobiological study failed to detect Y. pestis DNA in human remains collected from five different
burial sites dated from the 13th to 17th centuries in
Northern Europe (Gilbert et al., 2004). Further studies
performed by several research teams, however, have
detected the presence of Y. pestis-specific DNA sequences
and the pathogen’s F1 antigen at other burial sites in
France, Italy, Germany, the Netherlands, and England
(Drancourt et al., 1998, 2004; Raoult et al., 2000; Pusch
et al., 2004; Wiechmann and Grupe, 2005; Bianucci et
al., 2007, 2008, 2009; Cerutti et al., 2007; Drancourt et
al., 2007; Donat et al., 2008; Hadjouis et al., 2008;
Haensch et al., 2010; Wieschmann et al., 2010). These
paleomicrobiological data, while confirming that some
burial sites in medieval Europe were plague burial sites,
do not help resolve the lingering questions concerning
the epidemiology of the Black Death.
Using multiple molecular approaches, recent investigations of human remains dated from the 11th to 15th centuries in Bondy, France, have revealed co-infection of victims by Y. pestis and Bartonella quintana, a human liceborne organism (Raoult and Roux, 1999). Together with
other recently gathered experimental data, our observations pave the way toward a renewed understanding of
the transmission scenarios for the Black Death, including lice-borne and human-to-human transmission. These
findings will help resolve previous epidemiological inconsistencies.
C 2011
V
WILEY-LISS, INC.
C
*Correspondence to: Michel Drancourt, Unité des Rickettsies, Faculté de Médecine, 27, Boulevard Jean Moulin-cedex 5, France.
E-mail: michel.drancourt@univmed.fr
Received 22 November 2010; accepted 17 January 2011
DOI 10.1002/ajpa.21510
Published online 3 May 2011 in Wiley Online Library
(wileyonlinelibrary.com).
490
T.-N.-N. TRAN ET AL.
Fig. 1. Skeletons from the 11th to 15th centuries in Bondy, France yielded evidence for Yersinia pestis/Bartonella quintana coinfection. Copyright: Nicolas Latsanopoulos (Bureau de l’Archéologie, Service du patrimoine du Conseil général de Seine-SaintDenis, France). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
MATERIALS AND METHODS
Archaeological samples
In 2007, during piping work in Bondy, a small city
located 13 km east from Paris, France, three multiple
burial sites dated from the 11th to the 15th century
were discovered. The burial sites contained a total of 11
individuals of both genders and various ages (see Fig. 1).
Initially, stratigraphy and the analysis of the burial
remains were used to date the sites. C14-based datation
further yielded 1297–1373 with 70% probability and
1377–1414 with 30% probability. Individuals at the site
were covered with earth and not buried in coffins. Simultaneous deposition of the bodies was evidenced by the
direct contact between bones, the mechanical stress
between individuals, and the migration of some bones to
the contacts of the underlying skeletons (Duday, 2008).
All the buried corpses were laid on their backs in the
same east–west orientation with their heads placed at
the western position. In four individuals, the forearms
were bent 908 at the humeral axis (see Fig. 2). The
upper limbs of individuals 072 and 075 were not bent
and were found to be positioned alongside the body. The
bodies did not appear to have been thrown into the pit
but appeared to have been successively deposited next to
each other, except for subjects 071 and 073, which were
deposited on top of other bodies. Individuals 069, 072,
and 073 were placed first, followed by individuals 070
and 075, and finally individual 071. The multiple depositions involved individuals of both genders and various
ages. The skeletons were handled according to the principles of anthropological fieldwork, and the teeth were
placed into plastic bags. In the laboratory, the teeth
were washed with water and dried gradually. Teeth
American Journal of Physical Anthropology
belonging to different individuals were never in physical
contact from the time of their excavation to the time of
molecular biological analysis.
Molecular detection of multiple pathogens
Fourteen teeth were collected from five skeletons excavated from two Bondy burial sites. These skeletons did
not show any macroscopic signs of infectious disease.
Total DNA was extracted from the dental pulp collected
from teeth as previously described (Drancourt et al.,
1998). Using total DNA as a template, molecular detection of seven pathogens, including Bacillus anthracis,
Borrelia recurrentis, Bartonella quintana, Rickettsia
prowazekii, Salmonella enterica Typhi, Poxvirus, and
Y. pestis, was performed using multiplex high-throughput PCR and the 7900 HT Fast Real-Time PCR System
(Applied Biosystem, Courtaboeuf, France) as previously
described (Nguyen-Hieu et al., 2010; Table 1). Each plate
included two wells containing sterile water as negative
controls and two wells containing DNA extracted from
dental pulp collected from the skeletons of individuals
lacking macroscopic and anthropological evidence of
infection.
Y. pestis genotyping
Y. pestis genotyping was performed according to the
principles of ‘‘suicide PCR’’ as follows: (1) no positive control was used at any step of the processing of ancient
materials; (2) amplification was performed using a previously used glpD-PCR system (Drancourt et al., 2007) in
a building and in a laboratory where Y. pestis and
its DNA have never been previously worked on using
PLAGUE IN MEDIEVAL FRANCE
491
Fig. 2. Site plan featuring the positions of the studied individuals. Copyright: Nicolas Latsanopoulos (Bureau de l’Archéologie,
Service du patrimoine du Conseil général de Seine-Saint-Denis, France).
disposable instruments (Raoult et al., 2000); (3) each
step was conducted in a separate room and in a negative
air pressure hood; (4) three negative controls of DNA
dental pulp were placed between samples, and negative
control teeth (collected from skeletons of individuals
lacking anthropologic and macroscopic evidence of infection) were from a mass grave dating from the 5th to 7th
centuries. A total of 4 ll (1 ll for nested PCR) of DNA
were amplified in a 25-ll mixture containing 10 pmol of
each primer, 200 lmol/l each deoxyribonucleotide triphosphate (Invitrogen, Cergy-Pontoise, France), 1.5 U
HotStarTaq DNA Polymerase (Qiagen, Courtaboeuf,
France), and 2.5 lL MgCl2 (50-mmol/l) in 13 Taq buffer.
Suicide-nested PCR targeting the glpD gene was performed as previously described (Drancourt et al., 2007)
using a T3 thermocycler (Biometra, Archamps, France)
under the following conditions: an initial 2 min of denaturation at 958C was followed by 43 cycles (38 cycles for
nested PCR) of denaturation for 30 s at 948C, annealing
for 30 s at 588C, and extension for 90 s at 688C. The
amplification was completed by holding the reaction mixture for 7 min at 688C. PCR products were purified using
a QIAquick PCR purification kit (Qiagen, Courtaboeuf,
France). PCR products were separated by electrophoresis
for 25 min at 135 V in a 2% agarose gel in 0.53 TBE.
Marker VI was used as a DNA ladder when determining
the size of the amplified fragments. Purified positive
products were sequenced using ABI Prism1 Big Dye1
Terminator V1 and a 1 Cycle sequencing Kit (Applied
Biosystem, Courtaboeuf, France) in a 3130xl Genetic
Analyzer (Applied Biosystem). The sequences were
compared to the sequences deposited in the GenBank
database (www.ncbi.nlm.nih.gov/GenBank).
RESULTS
Molecular detection of multiple pathogens
A total of 14 dental pulp specimens were analyzed by
multiple molecular detection methods. All the negative
controls had negative results, and real-time PCR
detected B. quintana DNA in 3 of 14 dental pulp
specimens (identified tooth C33.JUG104.3 of individual
041, tooth C33.JUG180.1 of individual 070 and tooth
C33.JUG183.2 of individual 073) and Y. pestis DNA in
4 of 14 dental pulp specimens (identified tooth
American Journal of Physical Anthropology
492
T.-N.-N. TRAN ET AL.
TABLE 1. Sequences of primers and probes used for the molecular detection of seven pathogens
Target
gene
Specific pathogen
Bacillus anthracis
(anthrax)
pag
Borrelia recurrentis (louseborne relapsing fever)
Bartonella quintana
(Trench fever)
ITS
Rickettsia prowazekii
(typhus)
ompB
Salmonella Typhi (typhoid
fever)
Poxvirus (smallpox)
HA
Yersinia pestis (plague)
pla
Primer
Sequence
Lengh
(bp)
Bant_pag_P
Bant_pag_F
Bant_pag_R
Brec_P
Brec_F
Brec_R
Barto ITS_P
Barto ITS_F
Barto ITS_R
Rpr_ompB_P
Rpr_ompB_F
Rpr_ompB_R
Styp_put_P
Styp_put_F
Styp_put_R
Var_HA_P
Var_HA_F
Var_HA_R
Yper_PLA_P
Yper_PLA_F
Yper_PLA_R
6 FAM-TAC CGC AAA TTC AAG AAA CAA CTG
50 -AGG CTC GAA CTG GAG TGA A-30
50 -CCG CCT TTC TAC CAG ATT T-30
6 FAM-CTG CTG CTC CTT TAA CCA CAG GAG
50 -TCA ACT GTT TTT CTT ATT GCC ACA-30
50 -TCC TTA TGT TGG TTA TGG GAT TGA-30
6 FAM-GCG CGC GCT TGA TAA GCG TG
50 -GAT GCC GGG GAA GGT TTT C-30
50 -GCC TGG GAG GAC TTG AAC CT-30
6 FAM-CGG TGG TGT TAA TGC TGC GTT ACA
50 -AAT GCT CTT GCA GCT GGT TCT-30
50 -TCG AGT GCT AAT ATT TTT GAA GCA-30
6 FAM-GCT TTT TGT GAA GCA ACG CTG GCA
50 -CTC CAT GCT GCG ACC TCA AA-30
50 -TTC ATC CTG GTC CGG TGT CT-30
6 FAM-AAG ATC ATA CAG TCA CAG ACA CTG
50 -GAC KTC SGG ACC AAT TAC TA-30
50 -TTG ATT TAG TAG TGA CAA TTT CA-30
6 FAM-TCC CGA AAG GAG TGC GGG TAA
50 -ATG GAG CTT ATA CCG GAA AC-30
50 -GCG ATA CTG GCC TGC AAG-30
24
19
19
24
24
24
20
19
20
24
21
24
24
20
20
24
20
23
21
20
18
C33.JUG181.1 and tooth C33.JUG181.2 of individual
072 and tooth C33.JUG183.1 and tooth C33.JUG183.2 of
individual 073). Tooth C33.JUG83.2 of individual 073
yielded DNA from both pathogens. No pathogens other
than B. quintana and Y. pestis were detected in these
specimens.
Suicide-nested PCR detection
and genotyping of Y. pestis
In the presence of negative controls, suicide-nested
PCR confirmed the presence of Y. pestis in 2 of 14 dental
pulp specimens (tooth C33.JUG181.2 of individual 072
and tooth C33.JUG183.1 of individual 073). Sequencing
of the pathogen DNA from tooth C33.JUG181.2 of individual 072 yielded 100% sequence similarity with the
reference sequence of Y. pestis CO92 (GenBank accession
number AL590842). The partial glpD sequence of the
pathogen DNA extracted from tooth C33.JUG181.2
exhibited a 96-bp pair deletion indicative of the Orientalis biotype (Motin et al., 2002) when compared with homologous Y. pestis reference sequences in GenBank.
Combining the results of the molecular detection methods and suicide PCR, Y. pestis DNA was detected in four
teeth collected from two different individuals buried in
Bondy. Y. pestis was not detected in any of the three negative controls.
DISCUSSION
In this study, all ancient specimens were manipulated
according to the agreed upon paleomicrobiological protocols to ensure the authenticity of the data (Drancourt
and Raoult, 2005). In particular, direct contact between
individual remains was avoided at all times, both in the
field and in the laboratory. In addition, the teeth used
for examination were selected on the basis of a closed
apex, the absence of dental caries, and a lack of traumatic lesions to minimize any risk of external contamination of the dental pulp. Genotyping experiments were
performed in a laboratory where the targeted pathogens
had not been previously worked on, using the principles
American Journal of Physical Anthropology
Amplicon
Tm
94 bp
608C
111 bp
608C
102 bp
608C
134 bp
608C
138 bp
608C
100 bp
608C
98 bp
608C
of the suicide PCR protocol (Raoult et al., 2000). In all
experiments, negative controls were composed of dental
pulp collected from individuals without historical or anthropological evidence of epidemic disease, and PCR
mixes without DNA were used. In addition, the detection
of Y. pestis DNA was performed in two independent
experiments by different operators and confirmed by
sequencing.
The detection of Y. pestis confirms the presence of
plague in the 11th–15th centuries in Northern France. A
previous study of bones and teeth collected from five
sites in Northern Europe failed to detect Y. pestis DNA.
The study, however, yielded 16S rDNA sequences indicative of the genus Yersinia, including 16S rDNA sequences closely related to Y. pestis (Gilbert et al., 2004). Recovery of Y. pestis DNA in Bondy, currently located in
the suburbs of Paris at a latitude of 4889 north, along
with a previous report of Y. pestis DNA in skeletons
exhumed in Dreux, another French city located at 4884
north (Drancourt et al., 2004) and the recent detection of
Y. pestis DNA in Black Death skeletons in England and
in the Netherlands (Haensch et al., 2010), confirmed
Black Death in inland medieval Europe. These locations
depict the geographical extension of the Black Death,
starting from the Mediterranean sea ports where DNA
sequencing studies and immunological studies have previously demonstrated its presence (Drancourt et al.,
1998; Raoult et al., 2000; Cerutti et al., 2007) toward
Northern and Western inland France, where its presence
has been confirmed by DNA sequencing studies (Drancourt et al., 2004, 2007) and the detection of the F1 antigen known to be indicative of Y. pestis (Pusch et al.,
2004; Bianucci et al., 2008, 2009). In Bondy, we
confirmed an Orientalis biotype of Y. pestis, the same
biotype that has been found to date in the majority of
historical European plague victims (Drancourt et al.,
2004, 2007). A recent study based on the analysis of single-nucleotide polymorphisms found two non-Orientalis
genotypes of Y. pestis in 10 individuals in three archeological sites: Bergen op Zoom, the Netherlands (middle
14th century); Hereford, England (1335), and Saint-Laurent-de-Cabrerisse, France (1348–1374) (Haensch et al.,
493
PLAGUE IN MEDIEVAL FRANCE
2010). Altogether, these data indicate that several Y. pestis genotypes circulated in medieval Europe.
In this study, B. quintana DNA was found to have a
prevalence of 21%, which is consistent with previous
observations (Raoult and Roux, 1999). Several mass
graves have yielded evidence for the B. quintana infection, suggesting that this pathogen was widely distributed with a high prevalence in historic populations in
Europe. Such evidence is consistent with the estimated
high prevalence of the body louse vector of B. quintana
and with the pathogen’s relatively low mortality rate
(Brouqui et al., 1999). B. quintana has even been
detected in 4,000-year-old remains discovered in France
(Drancourt et al., 2005). Paleomicrobiology techniques
have previously detected B. quintana associated with the
epidemic typhus pathogen Rickettsia prowazekii found in
the remains of soldiers from Napoleon’s 1812 Great
Army buried in Vilnius (Raoult et al., 2006) and in dental pulp specimens dated to 1710–1712 in Douai, France
(Nguyen-Hieu et al., 2010). The association was interpreted as being indicative of body louse infestation in
the dead individuals, because both pathogens are known
to be transmitted by this human ectoparasite (Raoult
and Roux, 1999).
To our knowledge, this is the first report of a historical
co-infection of B. quintana and Y. pestis, and we are not
aware of any such association in modern times. In
Bondy, the fact that B. quintana and Y. pestis were
detected in the same mass grave and even in the same
individuals may be interpreted as coincidental plague in
B. quintana-infected individuals. Alternatively, other
observations raise questions about the mechanism of
transmission for the Black Death in Bondy. Plague can
be transmitted by rodent ectoparasites and is primarily
transmitted by rat fleas (Perry and Fetherston, 1997;
Wren, 2003; Gage and Kosoy, 2005); however, several
inconsistencies argue against the role of rat fleas in the
transmission of the Black Death. In medieval Europe,
plague-carrying rats were present in port areas and not
in inland areas; the plague epidemics were not associated with the expected rodent die-offs; and plague epidemics were active in the winter, which is a season
when rodent fleas would not have been active (McLean
and Fall, 2010). In Morocco, in 1941, the body louse,
which transmits B. quintana (Raoult and Roux, 1999),
was also found to be a plague vector in familial cases
(Blanc and Balthazard, 1941). In this situation, familial
cases of bubonic plague occurred in the absence of dead
or alive rats. Body lice were observed, but no fleas in the
vicinity of the infected cases were noted (Blanc and Baltazard, 1941, 1942, 1945). Blanc and Baltazard demonstrated the transmission of Y. pestis in mammals and
rats by inoculating them subcutaneously with infected
human body lice or their feces (Blanc and Baltazard,
1941; Blanc and Baltazard, 1942; Blanc and Balthazard,
1945). The potential role of lice in the transmission of
plague and the possibility that they may constitute a
vector for the plague has been further demonstrated
experimentally in rabbits (Houhamdi et al., 2006), and it
was recently shown that such body louse transmission is
restricted to the Orientalis biotype of Y. pestis (Ayyadurai et al., 2010). This Orientalis biotype was found in
Bondy and also in several other ancient plague burials.
These observations suggest that body lice was the vector
for interhuman transmission of plague in Bondy and
other inland medieval plague epidemics after the plague
had been introduced in Europe by infected rats and their
fleas through Mediterranean ports (Drancourt and
Raoult, in press).
CONCLUSIONS
Plague should be added to the list of deadly pathogens
that can be transmitted to humans by human body lice.
The body louse remains prevalent in some developing
countries where plague may persist and should be examined as a potential vector of plague in these populations.
Additional studies may help to elucidate the role of body
lice in plague transmission and aid in efforts to prevent
of future plague epidemics.
ACKNOWLEDGMENTS
The authors acknowledge Annick Bernard (URMITE,
Marseille, France) for her assistance with multiplex
high-throughput PCR. They also acknowledge Nicolas
Latsanopoulos (Bureau de l’Archéologie, Service du patrimoine du Conseil général de Seine-Saint-Denis,
France) for providing Figures 1 and 2.
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france, bond, site, burial, detection, yersinia, pestis, brief, communication, bartonella, quintana, 11thц15th
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