Publications by authors named "Minoarisoa Rajerison"

43 Publications

A decade of plague in Madagascar: a description of two hotspot districts.

BMC Public Health 2021 Jun 10;21(1):1112. Epub 2021 Jun 10.

Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Background: Human plague cases, mainly in the bubonic form, occur annually in endemic regions of the central highlands of Madagascar. The aim of this study was to compare the dynamics of the epidemiological features of the human plague in two districts of the central highlands region.

Methods: In Madagascar, all clinically suspected plague cases that meet clinical and epidemiological criteria specified in the World Health Organization (WHO) standard case definition are reported to the national surveillance system. Data on plague cases reported between 2006 and 2015 in the districts of Ambositra and Tsiroanomandidy were analysed. Statistical comparisons between the epidemiological characteristics of the two districts were conducted.

Results: A total of 840 cases of plague were reported over the studied period, including 563 (67%) probable and confirmed cases (P + C). Out of these P + C cases, nearly 86% (488/563) were cases of bubonic plague. Reported clinical forms of plague were significantly different between the districts from 2006 to 2015 (p = 0.001). Plague cases occurred annually in a period of 10 years in the Tsiroanomandidy district. During the same period, the Ambositra district was characterized by a one-year absence of cases.

Conclusion: The differences in the epidemiological situation with respect to the plague from 2006 to 2015 in the two central highlands districts may suggest that several factors other than biogeographical factors determine the representation of the plague and its dynamics in this region. Considering the epidemiological situations according to the specific contexts of the districts could improve the results in the fight against the plague in Madagascar.
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http://dx.doi.org/10.1186/s12889-021-11061-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8194207PMC
June 2021

Influence of Sociospatial determinants on knowledge, attitudes and practices related to the plague in a population living in endemic areas in the central highlands, Madagascar.

BMC Public Health 2021 Jun 9;21(1):1102. Epub 2021 Jun 9.

Institut Pasteur de Madagascar, 101, Antananarivo, Madagascar.

Background: Plague is endemic to the central highlands of Madagascar. Sporadic human cases or outbreaks can occur annually in these areas. In Madagascar, the associations between endemicity and the knowledge, attitudes and practices (KAP) of the population with regard to this disease remain poorly documented. The aim of this study was to assess KAP related to plague among the population living in the central highlands.

Methods: A cross-sectional survey was conducted in the general population from June to August 2017. Based on the reported cases of plague between 2006 and 2015 in two central highland districts, a KAP questionnaire was administered in the population. Based on the proportion of correct answers provided by respondents, KAP scores were classified into three KAP categories: low (< Mean - SD), medium (Mean ± SD) and good (> Mean + SD). Multivariate analyses were performed to determine the associations between population KAP scores related to plague and sociodemographic and epidemiological factors. In addition, individual interviews and focus groups with health professionals were conducted to assess plague perception.

Results: A total of 597 individuals participated in the survey; 20% (n = 119) had a good KAP score, 62% (n = 370) a medium KAP score and 18% (n = 108) a low KAP score. Among the 119 respondents with good KAP scores, 80% (n = 95) resided in Ambositra district, and 20% (n = 24) resided in Tsiroanomandidy district. According to the health professionals in the two districts, populations in endemic areas are well aware of the plague. There were significant associations (p <  0.05) of not owning a mobile phone, having no contact with a former plague case, and living in Tsiroanomandidy district with a lower KAP score.

Conclusion: The results of the study showed the need to adapt plague control interventions to the local context to allow a better allocation of human and financial resources. Doing so would minimize delays in patient management care and increase community resilience to plague epidemics.
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http://dx.doi.org/10.1186/s12889-021-11101-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8191115PMC
June 2021

Improved selective BIN agar for a better rate of isolation from primary clinical specimens in suspected Madagascar's plague cases.

J Clin Microbiol 2021 May 12. Epub 2021 May 12.

Department of Biochemistry and Molecular Genetics, Israel Institute for Biological Research, Ness-Ziona, Israel.

According to the WHO, 75% of the world's plague cases are found in Madagascar, with an average of 200-700 suspected cases annually (mainly bubonic plague). In 2017, a pneumonic plague epidemic of unusual proportions occurred, which raised several challenges for laboratory confirmation of cases, pointing to the need for the development of isolation procedures, especially those that can be performed in remote areas. As the WHO gold standard for plague diagnosis is bacterial culture, we sought to develop a simple method to prepare a highly selective medium, fit for use in remote endemic areas. The performance of the new medium, named improved-BIN, was examined in terms of growth support and selectivity with spiked samples as well in isolating from clinical specimens, and was compared to the results obtained with commercially available selective media. The preparation of the new medium is less complex and its performance was found to be superior to that of first-generation BIN medium. The growth support of the medium is higher, there is no batch diversity, and it maintains high selectivity properties. In 55 clinical specimens obtained from patients suspected to be infected with , approximately 20% more -positive isolates were identified by the improved-BIN than were identified by commercially available selective media. The improved-BIN medium is notably advantageous for the isolation of from clinical specimens obtained from plague patients, thus offering better surveillance tools and proper promotion of medical treatment to more patients suspected of being infected with .
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http://dx.doi.org/10.1128/JCM.00564-21DOI Listing
May 2021

Field assessment of dog as sentinel animal for plague in endemic foci of Madagascar.

Integr Zool 2021 Mar 17. Epub 2021 Mar 17.

Plague Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

The epidemiology of Yersinia pestis, the causative agent of plague, involves vectors and reservoirs in its transmission cycle. The passive plague surveillance in Madagascar targets mainly rodent and fleas. However, carnivores are routinely surveyed as sentinels of local plague activity in some countries. The aim of this study is to assess the use of domestic dog (Canis familiaris) as sentinel animal for field surveillance of plague in a highly endemic area in Madagascar. Cross-sectional surveys of plague antibody prevalence in C. familiaris were conducted in endemic areas with contrasting histories of plague cases in humans, as well as a plague free area. Rodent capture was done in parallel to evaluate evidence for Y. pestis circulation in the primary reservoirs. In 2 sites, dogs were later re-sampled to examine evidence of seroconversion and antibody persistence. Biological samplings were performed between March 2008 and February 2009. Plague antibody detection was assessed using anti-F1 ELISA. Our study showed a significant difference in dog prevalence rates between plague-endemic and plague-free areas, with no seropositive dogs detected in the plague free area. No correlation was found between rodents and dog prevalence rates, with an absence of seropositive rodents in some area where plague circulation was indicated by seropositive dogs. This is consistent with high mortality rates in rodents following infection. Re-sampling dogs identified individuals seropositive on both occasions, indicating high rates of re-exposure and/or persistence of plague antibodies for at least 9 months. Seroconversion or seropositive juvenile dogs indicated recent local plague circulation. In Madagascar, dog surveillance for plague antibody could be useful to identify plague circulation in new areas or quiescent areas within endemic zones. Within active endemic areas, monitoring of dog populations for seroconversion (negative to positive) or seropositive juvenile dogs could be useful for identifying areas at greatest risk of human outbreaks.
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http://dx.doi.org/10.1111/1749-4877.12541DOI Listing
March 2021

Rodent control to fight plague: field assessment of methods based on rat density reduction.

Integr Zool 2021 Mar 11. Epub 2021 Mar 11.

Institut Pasteur de Madagascar, Plague Unit, Antananarivo, Madagascar.

Rodents represent a serious threat to food security and public health. The extent to which rodent control can mitigate the risk from rodent-borne disease depends on both the effectiveness of control in reducing rodent abundance and the impact on disease epidemiology. Focusing on a plague-endemic region of Madagascar, this study compared the effectiveness of 3 methods: live-traps, snap-traps, and rodenticides. Control interventions were implemented inside houses between May and October 2019. Tracking tiles monitored rodent abundance. Rodent fleas, the vector involved in plague transmission, were collected. Rodent populations consisted of Rattus rattus and Mus musculus. In terms of trap success, we found that our live-trap regime was more effective than snap-traps. While all 3 control strategies appeared to reduce in-house rodent activity in the short term, we found no evidence of a longer-term effect, with in-house rodent abundance in treated sites comparable to non-treatment sites by the following month. Endemic flea, Synopsyllus fonquerniei, is a key plague vector usually found on rats living outdoors. Although we found no evidence that its abundance inside houses increased following control, this may have been due to a lack of power caused by significant variation in S. fonquerniei abundance. The presence of S. fonquerniei in houses was more likely when S. fonquerniei abundance on outdoor rats was higher, which in turn correlated with high rat abundance. Our results emphasize that control strategies need to consider this connectivity between in-house rat-flea populations and the outdoor populations, and any potential consequences for plague transmission.
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http://dx.doi.org/10.1111/1749-4877.12529DOI Listing
March 2021

Short- and long-term humoral immune response against Yersinia pestis in plague patients, Madagascar.

BMC Infect Dis 2020 Nov 10;20(1):822. Epub 2020 Nov 10.

Plague Unit, Institut Pasteur de Madagascar, 101, Antananarivo, Madagascar.

Background: Plague, a fatal disease caused by the bacillus, Yersinia pestis, still affects resources-limited countries. Information on antibody response to plague infection in human is scarce. Anti-F1 Ig G are among the known protective antibodies against Y. pestis infection. As a vaccine preventable disease, knowledge on antibody response is valuable for the development of an effective vaccine to reduce infection rate among exposed population in plague-endemic regions. In this study, we aim to describe short and long-term humoral immune responses against Y. pestis in plague-confirmed patients from Madagascar, the most affected country in the world.

Methods: Bubonic (BP) and pneumonic plague (PP) patients were recruited from plague- endemic foci in the central highlands of Madagascar between 2005 and 2017. For short-term follow-up, 6 suspected patients were enrolled and prospectively investigated for kinetics of the anti-F1 IgG response, whereas the persistence of antibodies was retrospectively studied in 71 confirmed convalescent patients, using an ELISA which was validated for the detection of plague in human blood samples in Madagascar.

Results: Similarly to previous findings, anti-F1 IgG rose quickly during the first week after disease onset and increased up to day 30. In the long-term study, 56% of confirmed cases remained seropositive, amongst which 60 and 40% could be considered as high- and low-antibody responders, respectively. Antibodies persisted for several years and up to 14.8 years for one individual. Antibody titers decreased over time but there was no correlation between titer and time elapsed between the disease onset and serum sampling. In addition, the seroprevalence rate was not significantly different between gender (P = 0.65) nor age (P = 0.096).

Conclusion: Our study highlighted that the circulating antibody response to F1 antigen, which is specific to Y. pestis, may be attributable to individual immune responsiveness. The finding that a circulating anti-F1 antibody titer could persist for more than a decade in both BP and PP recovered patients, suggests its probable involvement in patients' protection. However, complementary studies including analyses of the cellular immune response to Y. pestis are required for the better understanding of long-lasting protection and development of a potential vaccine against plague.
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http://dx.doi.org/10.1186/s12879-020-05565-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7653777PMC
November 2020

Human plague: An old scourge that needs new answers.

PLoS Negl Trop Dis 2020 08 27;14(8):e0008251. Epub 2020 Aug 27.

Epidemiology and Clinical Research Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Yersinia pestis, the bacterial causative agent of plague, remains an important threat to human health. Plague is a rodent-borne disease that has historically shown an outstanding ability to colonize and persist across different species, habitats, and environments while provoking sporadic cases, outbreaks, and deadly global epidemics among humans. Between September and November 2017, an outbreak of urban pneumonic plague was declared in Madagascar, which refocused the attention of the scientific community on this ancient human scourge. Given recent trends and plague's resilience to control in the wild, its high fatality rate in humans without early treatment, and its capacity to disrupt social and healthcare systems, human plague should be considered as a neglected threat. A workshop was held in Paris in July 2018 to review current knowledge about plague and to identify the scientific research priorities to eradicate plague as a human threat. It was concluded that an urgent commitment is needed to develop and fund a strong research agenda aiming to fill the current knowledge gaps structured around 4 main axes: (i) an improved understanding of the ecological interactions among the reservoir, vector, pathogen, and environment; (ii) human and societal responses; (iii) improved diagnostic tools and case management; and (iv) vaccine development. These axes should be cross-cutting, translational, and focused on delivering context-specific strategies. Results of this research should feed a global control and prevention strategy within a "One Health" approach.
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http://dx.doi.org/10.1371/journal.pntd.0008251DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7451524PMC
August 2020

Development and evaluation of loop-mediated isothermal amplification for detection of Yersinia pestis in plague biological samples.

PLoS One 2020 18;15(8):e0237655. Epub 2020 Aug 18.

Plague Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Background: Several tests are available for plague confirmation but bacteriological culture with Yersinia pestis strain isolation remains the gold standard according to the World Health Organization. However, this is a time consuming procedure; requiring specific devices and well-qualified staff. In addition, strain isolation is challenging if antibiotics have been administered prior to sampling. Here, we developed a loop-mediated isothermal amplification (LAMP) technique, a rapid, simple, sensitive and specific technique that would be able to detect Y. pestis in human biological samples.

Methods: LAMP primers were designed to target the caf1 gene which is specific to Y. pestis. The detection limit was determined by testing 10-fold serial dilution of Y. pestis DNA. Cross-reactivity was tested using DNA extracts from 14 pathogens and 47 residual samples from patients suffering from non-plague diseases. Specificity and sensitivity of the LAMP caf1 were assessed on DNA extracts of 160 human biological samples. Then, the performance of the LAMP caf1 assay was compared to conventional PCR and bacteriological culture.

Results: The detection limit of the developed Y. pestis LAMP assay was 3.79 pg/μl, similar to conventional PCR. The result could be read out within 45 min and as early as 35 minutes in presence of loop primer, using a simple water bath at 63°C. This is superior to culture with respect to time (requires up to 10 days) and simplicity of equipment compared to PCR. Furthermore, no cross-reactivity was found when tested on DNA extracts from other pathogens and human biological samples from patients with non-plague diseases. Compared to the gold standard, LAMP sensitivity and specificity were 97.9% (95% CI: 89.1%-99.9%) and 94.6% (95% CI: 88.6%-97.9%), respectively.

Conclusion: LAMP detected Y. pestis effectively with high sensitivity and specificity in human plague biological samples. It can potentially be used in the field during outbreaks in resource limited countries such as Madagascar.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0237655PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7437451PMC
October 2020

An open-label, randomized, non-inferiority trial of the efficacy and safety of ciprofloxacin versus streptomycin + ciprofloxacin in the treatment of bubonic plague (IMASOY): study protocol for a randomized control trial.

Trials 2020 Aug 17;21(1):722. Epub 2020 Aug 17.

University of Oxford, Oxford, UK.

Background: Bubonic plague is the primary manifestation of infection with Yersinia pestis, accounting for 90% of all plague cases and with 75% of global cases reported in Madagascar. All drugs in use for treating plague are registered based on experimental data and anecdotal evidence, and no regimen currently recommended is supported by a randomized clinical trial. The IMASOY trial intends to fill this knowledge gap by comparing two 10-day regimens included in the national guidelines in Madagascar. The primary objective of the trial is to test the hypothesis that ciprofloxacin monotherapy is non-inferior to streptomycin followed by ciprofloxacin for the treatment of bubonic plague, thus avoiding the need for injectable, potentially toxic, aminoglycosides.

Methods: A two-arm parallel-group randomized control trial will be conducted across peripheral health centres in Madagascar in five districts. Males and non-pregnant females of all ages with suspected bubonic or pneumonic plague will be recruited over the course of three plague 'seasons'. The primary endpoint of the trial is to assess the proportion of patients with bubonic plague who have a therapeutic response to treatment (defined as alive, resolution of fever, 25% reduction in the size of measurable buboes, has not received an alternative treatment and no clinical decision to continue antibiotics) as assessed on day 11.

Discussion: If successful, the trial has the potential to inform the standard of care guidelines not just in Madagascar but in other countries afflicted by plague. The trial is currently ongoing and expected to complete recruitment in 2022.

Trial Registration: ClinicalTrials.gov NCT04110340 . Registered on 1 October 2019.
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http://dx.doi.org/10.1186/s13063-020-04642-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7429934PMC
August 2020

Factors Influencing Atypical Clinical Presentations during the 2017 Madagascar Pneumonic Plague Outbreak: A Prospective Cohort Study.

Am J Trop Med Hyg 2020 06;102(6):1309-1315

Institut Pasteur de Madagascar, Antananarivo, Madagascar.

In late 2017, Madagascar experienced a large urban outbreak of pneumonic plague, the largest outbreak to date this century. During the outbreak, there were widespread reports of plague patients presenting with atypical symptoms, such as prolonged duration of illness and upper respiratory tract symptoms. Reported mortality among plague cases was also substantially lower than that reported in the literature (25% versus 50% in treated patients). A prospective multicenter observational study was carried out to investigate potential reasons for these atypical presentations. Few subjects among our cohort had confirmed or probable plague, suggesting that, in part, there was overdiagnosis of plague cases by clinicians. However, 35% subjects reported using an antibiotic with anti-plague activity before hospital admission, whereas 55% had antibiotics with anti-plague activity detected in their serum at admission. Although there may have been overdiagnosis of plague by clinicians during the outbreak, the high frequency of community antibiotic may partly explain the relatively few culture-positive sputum samples during the outbreak. Community antibiotic use may have also altered the clinical presentation of plague patients. These issues make accurate detection of patients and the development of clinical case definitions and triage algorithms in urban pneumonic plague outbreaks difficult.
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http://dx.doi.org/10.4269/ajtmh.19-0576DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7253123PMC
June 2020

Human Exposure to Hantaviruses Associated with Rodents of the Murinae Subfamily, Madagascar.

Emerg Infect Dis 2020 03;26(3):587-590

We conducted a national human serologic study of a hantavirus detected in Madagascar rodents using a commercial kit and a new ELISA targeting the virus. Our results suggest a conservative estimate of 2.7% (46/1,680) IgG seroprevalence. A second single-district study using the new ELISA revealed a higher prevalence (7.2%; 10/139).
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http://dx.doi.org/10.3201/eid2603.190320DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7045827PMC
March 2020

Performance of plague rapid diagnostic test compared to bacteriology: a retrospective analysis of the data collected in Madagascar.

BMC Infect Dis 2020 Jan 30;20(1):90. Epub 2020 Jan 30.

Epidemiology and Clinical Research Unit, Institut Pasteur de Madagascar, Antananarivo, 101, Madagascar.

Background: Plague is a highly fatal disease caused by Yersinia pestis. Late diagnosis hampers disease outcome and effectiveness of control measures, induces death and disease spread. Advance on its diagnosis was the use of lateral flow rapid diagnostic test (RDT).

Methods: We assessed the performance of the plague RDT based on Y. pestis F1 antigen detection more than 15 years after its deployment in Madagascar. We compared the RDT with bacteriological culture results, using data from plague notified cases collected during the periods for which both tests were performed independently and systematically.

Results: Used with bubonic plague (BP) patient samples, RDTs had a sensitivity of 100% (95% CI: 99.7-100%), a specificity of 67% (95% CI: 64-70%) with a good agreement between bacteriology and RDT results (86%; κ = 0.70, 95% CI 0.67-0.73). For pneumonic plague (PP), RDT had a sensitivity of 100% (95% CI: 91-100%) and a specificity of 59% (95% CI: 49-68%) and concordance between the bacteriological and plague RDT results was moderate (70%; κ = 0.43, 95% CI 0.32-0.55). Analysis focusing on the 2017-2018 plague season including the unprecedented epidemic of PP showed that RDT used on BP samples still had a sensitivity of 100% (95% CI: 85-100%) and a specificity of 82% (95% CI: 48-98%) with a very good agreement with bacteriology 94% (κ = 0.86, 95% CI 0.67-1); for PP samples, concordance between the bacteriological and plague RDT results was poor (61%; κ = - 0.03, 95% CI -0.17 - 0.10).

Conclusions: RDT performance appeared to be similar for the diagnosis of BP and PP except during the 2017 PP epidemic where RDT performance was low. This RDT, with its good sensitivity on both plague clinical forms during a normal plague season, remained a potential test for alert. Particularly for BP, it may be of great value in the decision process for the initiation of therapy. However, for PP, RDT may deliver false negative results due to inconsistent sample quality. Plague diagnosis could be improved through the development of next generation of RDTs.
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http://dx.doi.org/10.1186/s12879-020-4812-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6993518PMC
January 2020

in livestock in Madagascar: uncultured strains, mixed infections and small mammal-livestock transmission highlight challenges in controlling and diagnosing leptospirosis in the developing world.

Parasitology 2019 12 26;146(14):1707-1713. Epub 2019 Sep 26.

School of Biological Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, UK.

In developing countries, estimates of the prevalence and diversity of Leptospira infections in livestock, an important but neglected zoonotic pathogen and cause of livestock productivity loss, are lacking. In Madagascar, abattoir sampling of cattle and pigs demonstrated a prevalence of infection of 20% in cattle and 5% in pigs by real-time PCR. In cattle, amplification and sequencing of the Leptospira-specific lfb1 gene revealed novel genotypes, mixed infections of two or more Leptospira species and evidence for potential transmission between small mammals and cattle. Sequencing of the secY gene demonstrated genetic similarities between Leptospira detected in Madagascar and, as yet, uncultured Leptospira strains identified in Tanzania, Reunion and Brazil. Detection of Leptospira DNA in the same animal was more likely in urine samples or pooled samples from four kidney lobes relative to samples collected from a single kidney lobe, suggesting an effect of sampling method on detection. In pigs, no molecular typing of positive samples was possible. Further research into the epidemiology of livestock leptospirosis in developing countries is needed to inform efforts to reduce human infections and to improve livestock productivity.
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http://dx.doi.org/10.1017/S0031182019001252DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6935375PMC
December 2019

Field assessment of insecticide dusting and bait station treatment impact against rodent flea and house flea species in the Madagascar plague context.

PLoS Negl Trop Dis 2019 08 6;13(8):e0007604. Epub 2019 Aug 6.

Medical Entomology Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Bubonic is the most prevalent plague form in Madagascar. Indoor ground application of insecticide dust is the conventional method used to control potentially infected rodent fleas that transmit the plague bacterium from rodents to humans. The use of bait stations is an alternative approach for vector control during plague epidemics, as well as a preventive control method during non-epidemic seasons. Bait stations have many advantages, principally by reducing the amount of insecticide used, lowering the cost of the treatment and minimizing insecticide exposure in the environment. A previous study reported promising results on controlling simultaneously the reservoir and vectors, when slow-acting rodenticide was incorporated in bait stations called "Boîtes de Kartman". However, little evidence of an effective control of the fleas prior to the elimination of rodents was found. In this study, we evaluated bait stations containing insecticide powder and non-toxic attractive rodent bait for their potential to control rat fleas. Its efficacy was compared to the standard method. The impact of both methods on indoor and outdoor rodent fleas, as well as the human household flea Pulex irritans were analyzed at different time points after treatments. Bait stations did not cause any significant immediate or delayed reduction of rat fleas and increasing the number of operational bait stations per household did not significantly improve their efficacy. Insecticide ground dusting appeared to be the most efficient method to control indoor rat fleas. Both methods appeared to have little impact on the density of outdoor rat fleas and human fleas. These results demonstrate limited effectiveness for bait stations and encourage the maintenance of insecticide dusting as a first-line control strategy in case of epidemic emergence of plague, when immediate effect on rodent fleas is needed. Recommendations are given to improve the efficacy of the bait station method.
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http://dx.doi.org/10.1371/journal.pntd.0007604DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6697362PMC
August 2019

Epidemiological characteristics of an urban plague epidemic in Madagascar, August-November, 2017: an outbreak report.

Lancet Infect Dis 2019 05 28;19(5):537-545. Epub 2019 Mar 28.

Plague Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Background: Madagascar accounts for 75% of global plague cases reported to WHO, with an annual incidence of 200-700 suspected cases (mainly bubonic plague). In 2017, a pneumonic plague epidemic of unusual size occurred. The extent of this epidemic provides a unique opportunity to better understand the epidemiology of pneumonic plagues, particularly in urban settings.

Methods: Clinically suspected plague cases were notified to the Central Laboratory for Plague at Institut Pasteur de Madagascar (Antananarivo, Madagascar), where biological samples were tested. Based on cases recorded between Aug 1, and Nov 26, 2017, we assessed the epidemiological characteristics of this epidemic. Cases were classified as suspected, probable, or confirmed based on the results of three types of diagnostic tests (rapid diagnostic test, molecular methods, and culture) according to 2006 WHO recommendations.

Findings: 2414 clinically suspected plague cases were reported, including 1878 (78%) pneumonic plague cases, 395 (16%) bubonic plague cases, one (<1%) septicaemic case, and 140 (6%) cases with unspecified clinical form. 386 (21%) of 1878 notified pneumonic plague cases were probable and 32 (2%) were confirmed. 73 (18%) of 395 notified bubonic plague cases were probable and 66 (17%) were confirmed. The case fatality ratio was higher among confirmed cases (eight [25%] of 32 cases) than probable (27 [8%] of 360 cases) or suspected pneumonic plague cases (74 [5%] of 1358 cases) and a similar trend was seen for bubonic plague cases (16 [24%] of 66 confirmed cases, four [6%] of 68 probable cases, and six [2%] of 243 suspected cases). 351 (84%) of 418 confirmed or probable pneumonic plague cases were concentrated in Antananarivo, the capital city, and Toamasina, the main seaport. All 50 isolated Yersinia pestis strains were susceptible to the tested antibiotics.

Interpretation: This predominantly urban plague epidemic was characterised by a large number of notifications in two major urban areas and an unusually high proportion of pneumonic forms, with only 23% having one or more positive laboratory tests. Lessons about clinical and biological diagnosis, case definition, surveillance, and the logistical management of the response identified in this epidemic are crucial to improve the response to future plague outbreaks.

Funding: US Agency for International Development, WHO, Institut Pasteur, US Department of Health and Human Services, Laboratoire d'Excellence Integrative Biology of Emerging Infectious Diseases, Models of Infectious Disease Agent Study of the National Institute of General Medical Sciences, AXA Research Fund, and the INCEPTION programme.
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http://dx.doi.org/10.1016/S1473-3099(18)30730-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6483974PMC
May 2019

High Prevalence of spp. in Rodents in an Urban Setting in Madagascar.

Am J Trop Med Hyg 2019 05;100(5):1079-1081

Plague Unit, WHO Collaborating Center, Institut Pasteur, Antananarivo, Madagascar.

Leptospirosis is a neglected zoonotic bacterial disease caused by pathogenic spp. Only limited studies have been conducted on the presence of spp. in rats in Antananarivo, the capital city of Madagascar. We assessed prevalence in small mammals in urban areas of Antananarivo where sanitation is inadequate and there is risk of flooding during the rainy season. We captured rodents and shrews at two sites and examined kidney samples from 114 animals using culture and a real-time polymerase chain reaction (PCR) assay specific to pathogenic spp. We identified 23 positive samples containing and , with a high prevalence in (44.9%). Our results indicate that small mammals, in particular , present a major public health risk for acquiring leptospirosis in Antananarivo.
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http://dx.doi.org/10.4269/ajtmh.18-0642DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6493950PMC
May 2019

Trends of Human Plague, Madagascar, 1998-2016.

Emerg Infect Dis 2019 02;25(2):220-228

Madagascar is more seriously affected by plague, a zoonosis caused by Yersinia pestis, than any other country. The Plague National Control Program was established in 1993 and includes human surveillance. During 1998-2016, a total of 13,234 suspected cases were recorded, mainly from the central highlands; 27% were confirmed cases, and 17% were presumptive cases. Patients with bubonic plague (median age 13 years) represented 93% of confirmed and presumptive cases, and patients with pneumonic plague (median age 29 years) represented 7%. Deaths were associated with delay of consultation, pneumonic form, contact with other cases, occurrence after 2009, and not reporting dead rats. A seasonal pattern was observed with recrudescence during September-March. Annual cases peaked in 2004 and decreased to the lowest incidence in 2016. This overall reduction occurred primarily for suspected cases and might be caused by improved adherence to case criteria during widespread implementation of the F1 rapid diagnostic test in 2002.
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http://dx.doi.org/10.3201/eid2502.171974DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6346457PMC
February 2019

Exposure to Yersinia pestis increases resistance to plague in black rats and modulates transmission in Madagascar.

BMC Res Notes 2018 Dec 14;11(1):898. Epub 2018 Dec 14.

Unité d'Immunologie, Institut Pasteur de Madagascar, Ambatofotsikely, P.O. Box 1274, Antananarivo, Madagascar.

Objectives: In Madagascar, plague (Yersinia pestis infection) is endemic in the central highlands, maintained by the couple Rattus rattus/flea. The rat is assumed to die shortly after infection inducing migration of the fleas. However we previously reported that black rats from endemic areas can survive the infection whereas those from non-endemic areas remained susceptible. We investigate the hypothesis that lineages of rats can acquire resistance to plague and that previous contacts with the bacteria will affect their survival, allowing maintenance of infected fleas. For this purpose, laboratory-born rats were obtained from wild black rats originating either from plague-endemic or plague-free zones, and were challenged with Y. pestis. Survival rate and antibody immune responses were analyzed.

Results: Inoculation of low doses of Y. pestis greatly increase survival of rats to subsequent challenge with a lethal dose. During challenge, cytokine profiles support activation of specific immune response associated with the bacteria control. In addition, F1 rats from endemic areas exhibited higher survival rates than those from non-endemic ones, suggesting a selection of a resistant lineage. In Madagascar, these results support the role of black rat as long term reservoir of infected fleas supporting maintenance of plague transmission.
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http://dx.doi.org/10.1186/s13104-018-3984-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6295079PMC
December 2018

Risk of maritime introduction of plague from Madagascar to Mayotte.

Acta Trop 2018 Nov 31;187:140-143. Epub 2018 Jul 31.

Medical Entomology Unit, Institut Pasteur, Antananarivo, Madagascar; Medical Entomology Platform, Institut Pasteur du Cambodge, Phnom Penh, Cambodia.

Plague is a rodent-borne disease caused by Yersinia pestis. Most human infections are bubonic plague, as a result of being bitten by infected rodent fleas. Madagascar, Democratic Republic of Congo and Peru are the three most affected countries. Plague was introduced into eastern Madagascar in 1898 by boat from India. It is estimated that the risk of introduction of plague from Madagascar to neighboring islands is very high due to the maritime links. We conducted a study of plague reservoirs and vectors in Longoni Port in Mayotte and Mahajanga Port in Madagascar during two seasons to highlight a non-negligible risk of introduction of Y. pestis to Mayotte. The results showed that two main reservoirs of plague in Madagascar Suncus murinus and Rattus rattus and the main flea vector Xenopsylla cheopis exists in and surrounding the port of Longoni. Y. pestis was isolated from Rattus norvegicus captured close to the port of Mahajanga during this study. Plague bacteria circulate within populations of rodent without causing rodent die-off in Mahajanga. The risk of introduction of plague from Madagascar to Mayotte exists due to the regular exchanges. Continuous surveillance of rat, shrew and flea populations is therefore necessary in all the surrounding countries that have regular exchanges with Madagascar to prevent the spread of the plague.
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http://dx.doi.org/10.1016/j.actatropica.2018.07.029DOI Listing
November 2018

Mixed pneumonic plague and nosocomial MDR-bacterial infection of lung: a rare case report.

BMC Pulm Med 2018 May 29;18(1):92. Epub 2018 May 29.

Plague Unit- Institut Pasteur de Madagascar, BP1274 Ambatofotsikely, 101, Antananarivo, Madagascar.

Background: Plague is a life-threatening disease caused by the bacterium, Yersinia pestis. Madagascar is the leading country for human plague cases worldwide. Human plague is a serious disease, particularly in its septicaemic and pneumonic forms. We report a case of pneumonic plague co-infected by a MDR-Stenotrophomonas maltophilia.

Case Presentation: A 24 year-old man originated from Soavinandriana, a plague focus, felt uneasy and developed high fever with chills. He started treatment by himself, by private medical care and by a traditional healer for nine days moving several times from place to place. His condition had deteriorated when he presented to a district hospital with a syndrome of dyspnea, bronchial rale and altered state of consciousness. Two days later, plague diagnosis, performed as a last resort, revealed a positive F1 antigen on rapid diagnostic test. Additional tests (pla PCR and plague serology) evidenced a Y. pestis infection. However, streptomycin treatment did not achieve a complete recovery as the course of disease was complicated by the presence of MDR-S. maltophilia in his lung. This opportunistic infection could have been favored by an immunosuppression due to Y. pestis pulmonary infection and probably been acquired during his stay at a District Hospital. He was treated with a combination of ciprofloxacin and gentamycin and recovered fully.

Conclusions: Pneumonic plague infection may promote another virulent or avirulent bacterial infection particularly when it is not initially suspected. However, coinfection is rarely described and its occurrence frequency is unknown. In middle or low resources areas, which is the case of most plague endemic countries, control and prevention of infections in health facilities is not optimal. Co-infection with an opportunistic pathogen agent, such as S. maltophilia, is a risk which must not be disregarded as demonstrated by this case report. When deciding of a national control strategy, it should be taken into account in the choice of the first line treatment.
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http://dx.doi.org/10.1186/s12890-018-0656-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5975559PMC
May 2018

Mixed Leptospira Infections in a Diverse Reservoir Host Community, Madagascar, 2013-2015.

Emerg Infect Dis 2018 06;24(6):1138-1140

We identified mixed infections of pathogenic Leptospira in small mammals across a landscape-scale study area in Madagascar by using primers targeting different Leptospira spp. Using targeted primers increased prevalence estimates and evidence for transmission between endemic and invasive hosts. Future studies should assess rodentborne transmission of Leptospira to humans.
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http://dx.doi.org/10.3201/eid2406.180035DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6004868PMC
June 2018

Low cost, low tech SNP genotyping tools for resource-limited areas: Plague in Madagascar as a model.

PLoS Negl Trop Dis 2017 12 11;11(12):e0006077. Epub 2017 Dec 11.

The Pathogen and Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, United States of America.

Background: Genetic analysis of pathogenic organisms is a useful tool for linking human cases together and/or to potential environmental sources. The resulting data can also provide information on evolutionary patterns within a targeted species and phenotypic traits. However, the instruments often used to generate genotyping data, such as single nucleotide polymorphisms (SNPs), can be expensive and sometimes require advanced technologies to implement. This places many genotyping tools out of reach for laboratories that do not specialize in genetic studies and/or lack the requisite financial and technological resources. To address this issue, we developed a low cost and low tech genotyping system, termed agarose-MAMA, which combines traditional PCR and agarose gel electrophoresis to target phylogenetically informative SNPs.

Methodology/principal Findings: To demonstrate the utility of this approach for generating genotype data in a resource-constrained area (Madagascar), we designed an agarose-MAMA system targeting previously characterized SNPs within Yersinia pestis, the causative agent of plague. We then used this system to genetically type pathogenic strains of Y. pestis in a Malagasy laboratory not specialized in genetic studies, the Institut Pasteur de Madagascar (IPM). We conducted rigorous assay performance validations to assess potential variation introduced by differing research facilities, reagents, and personnel and found no difference in SNP genotyping results. These agarose-MAMA PCR assays are currently employed as an investigative tool at IPM, providing Malagasy researchers a means to improve the value of their plague epidemiological investigations by linking outbreaks to potential sources through genetic characterization of isolates and to improve understanding of disease ecology that may contribute to a long-term control effort.

Conclusions: The success of our study demonstrates that the SNP-based genotyping capacity of laboratories in developing countries can be expanded with manageable financial cost for resource constraint laboratories. This is a practical formula that reduces resource-driven limitations to genetic research and promises to advance global collective knowledge of infectious diseases emanating from resource limited regions of the world.
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http://dx.doi.org/10.1371/journal.pntd.0006077DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5739503PMC
December 2017

The Asian house shrew Suncus murinus as a reservoir and source of human outbreaks of plague in Madagascar.

PLoS Negl Trop Dis 2017 Nov 20;11(11):e0006072. Epub 2017 Nov 20.

IRD, Centre de Biologie et de Gestion des populations (ird/inra/cirad/montpelliersupagro), Montpellier, France.

Identifying key reservoirs for zoonoses is crucial for understanding variation in incidence. Plague re-emerged in Mahajanga, Madagascar in the 1990s but there has been no confirmed case since 1999. Here we combine ecological and genetic data, from during and after the epidemics, with experimental infections to examine the role of the shrew Suncus murinus in the plague epidemiological cycle. The predominance of S. murinus captures during the epidemics, their carriage of the flea vector and their infection with Yersinia pestis suggest they played an important role in the maintenance and transmission of plague. S. murinus exhibit a high but variable resistance to experimental Y. pestis infections, providing evidence of its ability to act as a maintenance host. Genetic analyses of the strains isolated from various hosts were consistent with two partially-linked transmission cycles, with plague persisting within the S. murinus population, occasionally spilling over into the rat and human populations. The recent isolation from a rat in Mahajanga of a Y. pestis strain genetically close to shrew strains obtained during the epidemics reinforces this hypothesis and suggests circulation of plague continues. The observed decline in S. murinus and Xenopsylla cheopis since the epidemics appears to have decreased the frequency of spillover events to the more susceptible rats, which act as a source of infection for humans. Although this may explain the lack of confirmed human cases in recent years, the current circulation of plague within the city highlights the continuing health threat.
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http://dx.doi.org/10.1371/journal.pntd.0006072DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5714386PMC
November 2017

Plague risk in vulnerable community: assessment of Xenopsylla cheopis susceptibility to insecticides in Malagasy prisons.

Infect Dis Poverty 2017 Nov 7;6(1):141. Epub 2017 Nov 7.

Unité d'Entomologie Médicale, Institut Pasteur de Madagascar, Ambatofotsikely, 101, Antananarivo, PO box 1274, Madagascar.

Background: Prisons in Madagascar are at high risk of plague outbreak. Occurrence of plague epidemic in prisons can cause significant episode of urban plague through the movement of potentially infected humans, rodents and fleas. Rodent and flea controls are essential in plague prevention, by reducing human contact with plague reservoirs and vectors. Insecticide treatment is the key step available for the control of rat fleas which transmit the disease from infected rodents to human. The implementation of an adapted flea control strategy should rely on the insecticide susceptibility status of the targeted population. For the purpose of plague prevention campaign in prisons, we conducted insecticide resistance survey on Xenopsylla cheopis, the rat flea.

Methods: Fleas were collected on rats caught in six prisons of Madagascar. They were exposed to insecticide treated filter papers and mortality was recorded following World Health Organization protocol.

Results: The fleas collected in the prisons had different resistance patterns, while a high level of resistance to insecticides tested was described in the Antanimora prison, located in the heart of Antananarivo, the capital of Madagascar.

Conclusions: This finding is alarming in the context of public health, knowing that the effectiveness of flea control could be jeopardized by insecticide resistance. In order to establish more accurate rat fleas control in prisons, the main recommendations are based on continuous monitoring insecticide susceptibility of flea, insecticide rotation, and the development of a new method for flea control.
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http://dx.doi.org/10.1186/s40249-017-0356-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5674827PMC
November 2017

Plasmid-mediated doxycycline resistance in a Yersinia pestis strain isolated from a rat.

Int J Antimicrob Agents 2018 Feb 10;51(2):249-254. Epub 2017 Oct 10.

Yersinia Research Unit, WHO Collaborating Center, Institut Pasteur, 28 rue du Dr Roux, 75724 Paris, Cedex 15, France. Electronic address:

The emergence of antibiotic-resistant Yersinia pestis strains represents a public health concern. Two antibiotic-resistant Y. pestis strains isolated from Madagascar have been previously identified and characterised. Both strains carried conjugative plasmids that conferred resistance to streptomycin or to multiple antibacterial drugs, respectively. Here we characterised a novel Y. pestis strain (IP2180H) that exhibited resistance to doxycycline. This strain was isolated from a rat in Antananarivo (Madagascar) in 1998. Resistance was carried by a conjugative plasmid (pIP2180H) homologous to pB71 from Salmonella enterica. The plasmid of the previously identified streptomycin-resistant Y. pestis strain was also sequenced and it was found that the three antibiotic resistance Y. pestis plasmids sequenced until now are genetically unrelated and are also unrelated to multidrug resistance plasmids from the phylogenetically close bacterial species Yersinia pseudotuberculosis. The fact that the three antibiotic-resistant Malagasy Y. pestis strains were isolated from different hosts, at different times, from distant locations, and carried unrelated plasmids indicates independent horizontal acquisition of genetic material and further demonstrates the capacity of Y. pestis to acquire antibiotic resistance plasmids under natural conditions. Since these resistance plasmids can frequently carry or easily trap antibiotic resistance cassettes, the emergence of new multidrug-resistant Y. pestis strains may be expected and would represent a major health threat.
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http://dx.doi.org/10.1016/j.ijantimicag.2017.09.015DOI Listing
February 2018

Temporal phylogeography of Yersinia pestis in Madagascar: Insights into the long-term maintenance of plague.

PLoS Negl Trop Dis 2017 Sep 5;11(9):e0005887. Epub 2017 Sep 5.

Plague Research Unit, Institut Pasteur de Madagascar, Antananarivo, Madagascar.

Background: Yersinia pestis appears to be maintained in multiple, geographically separate, and phylogenetically distinct subpopulations within the highlands of Madagascar. However, the dynamics of these locally differentiated subpopulations through time are mostly unknown. To address that gap and further inform our understanding of plague epidemiology, we investigated the phylogeography of Y. pestis in Madagascar over an 18 year period.

Methodology/principal Findings: We generated whole genome sequences for 31 strains and discovered new SNPs that we used in conjunction with previously identified SNPs and variable-number tandem repeats (VNTRs) to genotype 773 Malagasy Y. pestis samples from 1995 to 2012. We mapped the locations where samples were obtained on a fine geographic scale to examine phylogeographic patterns through time. We identified 18 geographically separate and phylogenetically distinct subpopulations that display spatial and temporal stability, persisting in the same locations over a period of almost two decades. We found that geographic areas with higher levels of topographical relief are associated with greater levels of phylogenetic diversity and that sampling frequency can vary considerably among subpopulations and from year to year. We also found evidence of various Y. pestis dispersal events, including over long distances, but no evidence that any dispersal events resulted in successful establishment of a transferred genotype in a new location during the examined time period.

Conclusions/significance: Our analysis suggests that persistent endemic cycles of Y. pestis transmission within local areas are responsible for the long term maintenance of plague in Madagascar, rather than repeated episodes of wide scale epidemic spread. Landscape likely plays a role in maintaining Y. pestis subpopulations in Madagascar, with increased topographical relief associated with increased levels of localized differentiation. Local ecological factors likely affect the dynamics of individual subpopulations and the associated likelihood of observing human plague cases in a given year in a particular location.
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http://dx.doi.org/10.1371/journal.pntd.0005887DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5600411PMC
September 2017

Genetic structure and gene flow of the flea Xenopsylla cheopis in Madagascar and Mayotte.

Parasit Vectors 2017 Jul 20;10(1):347. Epub 2017 Jul 20.

Medical Entomology Unit, Institut Pasteur of Madagascar, Ambatofotsikely, PO box 1274, 101, Antananarivo, Madagascar.

Background: The flea Xenopsylla cheopis (Siphonaptera: Pulicidae) is a vector of plague. Despite this insect's medical importance, especially in Madagascar where plague is endemic, little is known about the organization of its natural populations. We undertook population genetic analyses (i) to determine the spatial genetic structure of X. cheopis in Madagascar and (ii) to determine the potential risk of plague introduction in the neighboring island of Mayotte.

Results: We genotyped 205 fleas from 12 sites using nine microsatellite markers. Madagascan populations of X. cheopis differed, with the mean number of alleles per locus per population ranging from 1.78 to 4.44 and with moderate to high levels of genetic differentiation between populations. Three distinct genetic clusters were identified, with different geographical distributions but with some apparent gene flow between both islands and within Malagasy regions. The approximate Bayesian computation (ABC) used to test the predominant direction of flea dispersal implied a recent population introduction from Mayotte to Madagascar, which was estimated to have occurred between 1993 and 2012. The impact of this flea introduction in terms of plague transmission in Madagascar is unclear, but the low level of flea exchange between the two islands seems to keep Mayotte free of plague for now.

Conclusion: This study highlights the occurrence of genetic structure among populations of the flea vector of plague, X. cheopis, in Madagascar and suggests that a flea population from Mayotte has been introduced to Madagascar recently. As plague has not been reported in Mayotte, this introduction is unlikely to present a major concern for plague transmission. Nonetheless, evidence of connectivity among flea populations in the two islands indicates a possibility for dispersal by fleas in the opposite direction and thus a risk of plague introduction to Mayotte.
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http://dx.doi.org/10.1186/s13071-017-2290-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5520349PMC
July 2017

Molecular and serological evidence of flea-associated typhus group and spotted fever group rickettsial infections in Madagascar.

Parasit Vectors 2017 03 4;10(1):125. Epub 2017 Mar 4.

Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, UK.

Background: Rickettsiae are obligate intracellular bacteria responsible for many febrile syndromes around the world, including in sub-Saharan Africa. Vectors of these pathogens include ticks, lice, mites and fleas. In order to assess exposure to flea-associated Rickettsia species in Madagascar, human and small mammal samples from an urban and a rural area, and their associated fleas were tested.

Results: Anti-typhus group (TGR)- and anti-spotted fever group rickettsiae (SFGR)-specific IgG were detected in 24 (39%) and 21 (34%) of 62 human serum samples, respectively, using indirect ELISAs, with six individuals seropositive for both. Only two (2%) Rattus rattus out of 86 small mammals presented antibodies against TGR. Out of 117 fleas collected from small mammals, Rickettsia typhi, a TGR, was detected in 26 Xenopsylla cheopis (24%) collected from rodents of an urban area (n = 107), while two of these urban X. cheopis (2%) were positive for Rickettsia felis, a SFGR. R. felis DNA was also detected in eight (31%) out of 26 Pulex irritans fleas.

Conclusions: The general population in Madagascar are exposed to rickettsiae, and two flea-associated Rickettsia pathogens, R. typhi and R. felis, are present near or in homes. Although our results are from a single district, they demonstrate that rickettsiae should be considered as potential agents of undifferentiated fever in Madagascar.
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http://dx.doi.org/10.1186/s13071-017-2061-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5336680PMC
March 2017

Pneumonic Plague Transmission, Moramanga, Madagascar, 2015.

Emerg Infect Dis 2017 03;23(3):521-524

During a pneumonic plague outbreak in Moramanga, Madagascar, we identified 4 confirmed, 1 presumptive, and 9 suspected plague case-patients. Human-to-human transmission among close contacts was high (reproductive number 1.44) and the case fatality rate was 71%. Phylogenetic analysis showed that the Yersinia pestis isolates belonged to group q3, different from the previous outbreak.
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http://dx.doi.org/10.3201/eid2303.161406DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5382734PMC
March 2017