Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity

Abstract

Monkeypox is a viral zoonotic disease on the rise across endemic habitats. Despite the growing importance of monkeypox virus, our knowledge on its host spectrum and sylvatic maintenance is limited. Here, we describe the recent repeated emergence of monkeypox virus in a wild, human-habituated western chimpanzee (Pan troglodytes verus, hereafter chimpanzee) population from Taï National Park, Ivory Coast. Through daily monitoring, we show that further to causing its typical exanthematous syndrome, monkeypox can present itself as a severe respiratory disease without a diffuse rash. By analysing 949 non-invasively collected samples, we identify the circulation of at least two distinct monkeypox virus lineages and document the shedding of infectious particles in faeces and flies, suggesting that they could mediate indirect transmission. We also show that the carnivorous component of the Taï chimpanzees’ diet, mainly consisting of the sympatric monkeys they regularly hunt, did not change nor shift towards rodent consumption (the presumed reservoir) before the outbreaks, suggesting that the sudden emergence of monkeypox virus in this population is probably due to changes in the ecology of the virus itself. Using long-term mortality surveillance data from Taï National Park, we provide evidence of little to no prior viral activity over at least two decades. We conclude that great ape sentinel systems devoted to the longitudinal collection of behavioural and health data can help clarify the epidemiology and clinical presentation of zoonotic pathogens.

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Fig. 1: Map of the chimpanzee territories in TNP.
Fig. 2: Monkeypox lesions in two wild chimpanzees.
Fig. 3: Genomic characterization of MPXVs found in the Taï chimpanzee communities.
Fig. 4: Bayesian chronogram of West African MPXVs.
Fig. 5: Snapshot of molecular analyses in faecal samples.
Fig. 6: Social network metrics.

Data availability

Raw reads of 16S amplicons are available in the European Nucleotide Archive (ENA) under project accession number PRJEB34040 and sample accession numbers ERS3658904ERS3659288. Raw reads resulting from MPXV target enrichment in non-invasive samples are available in the ENA under project accession number PRJEB34056, sample accession numbers ERS3659494ERS3659510. Consensus sequences are available in GenBank, accession numbers MN346690MN3466703. Annotated MPXV genomes, as well as sequences derived from the fly species identification, are available in Zenodo (https://zenodo.org record number 3373886 and 3606577, respectively). Source Data for Fig. 6 and Extended Data Figs. 79 are provided with the paper.

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Acknowledgements

We thank the Ministère de l’Enseignement Supérieur et de la Recherche Scientifique, the Ministère de Eaux et Fôrets in Ivory Coast and the Office Ivoirien des Parcs et Réserves for permitting the study. We are grateful to the Centre Suisse de Recherches Scientifiques en Côte d’Ivoire and the staff members of the Taï Chimpanzee Project for their support. The Max Planck Society has provided core funding for the Taï Chimpanzee Project since 1997. We thank all primatologists, research assistants and veterinarians who collected samples for the Taï Chimpanzee project over the years. We are grateful to the Sequencing Unit of the Robert Koch Institute for their support. We thank S. Lemoine for providing the map illustrating the territories of the Taï chimpanzees. This work was supported by the Robert Koch Institute, the Alexander von Humboldt Foundation postdoctoral fellowship programme, the German Research Council projects LE1813/10-2, LE1813/14-1, WI2637/4-2 and WI2637/3-1 within the research group FOR2136 (Sociality and Health in Primates) and LE1813/11-1 (Great Ape Health in Tropical Africa), and the ARCUS Foundation grant G-PGM-1606-1874. Work was partly carried out under the Global Health Protection Programme supported by the Federal Ministry of Health on the basis of a decision by the German Bundestag.

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Authors

Contributions

Data and samples from the three outbreaks were collected by K.P. and L.S. The field investigations as well as diagnostic and research activities were coordinated by L.V.P., S.C.-S. and F.H.L. Molecular laboratory analyses were performed by L.V.P., C.R., A.S. and M.U. Social network analyses were performed by M.U. Virus isolation experiments were conducted and coordinated by S.M. and A.N. C.B., R.M.W. and E.C.-H. coordinated the field work and provided the behavioural data. The data were analysed by L.V.P. and S.C.-S. and the manuscript was drafted by L.V.P., S.C.-S. and F.H.L. The manuscript was revised and approved by all authors.

Corresponding author

Correspondence to Fabian H. Leendertz.

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Extended data

Extended Data Fig. 1 Clinical course of MPXV infection in an infant East chimpanzee.

Pictures a-h show the evolution of the skin lesions over a 19-day period. Day 1 corresponds to the first day of symptoms’ observation by researchers. a Papular lesions covering the entire body. b Lesions in vesiculopustular stage, also evident on eyelids. c Ulceration and umbilication of facial lesions, some crusts already visible. d Most facial lesions have ulcerated and crusted, lesions on limbs are still at a vesicular stage. e Most facial lesions have crusted and scabbed, lesions on the abdomen and extremities are still in previous stages. f Facial lesions mostly scabbed and crusts fallen off, on the abdomen and extremities crusting and scabbing are underway. g, h Lesions on the entire body have resolved.

Extended Data Fig. 2 Clinical signs associated with MPXV infection during the 3 outbreaks in wild chimpanzees.

The number following the group name is the total number of chimpanzees in the group. Dates below each group indicate the timeframe when clinical signs were observed. Numbers in brackets after each age group correspond to the number of chimpanzees belonging to that age group. Numbers under disease manifestation categories indicate the number and age class of chimpanzees who manifested those clinical signs. The number of asymptomatic chimpanzees in which MPXV DNA was detected in faeces is also reported in the last column.

Extended Data Fig. 3 Summary of samples types and MPXV DNA detection in all non-invasive samples collected before, during and after the appearance of clinical signs associated with MPXV infection in the three chimpanzee communities.

Collection periods are reported for each group.

Extended Data Fig. 4 Molecular analyses in faecal samples.

a, Detection of MPXV DNA and non-chimpanzee mammalian DNA b, in chimpanzee faecal samples from the South community over time. Each line represents a chimpanzee. Bold names correspond to chimpanzees in which mild to severe signs compatible with MPXV infection were observed. Boxes represent age groups (infant, juvenile, adolescent and adult). Vertical light grey shadowing indicates the period in which clinical signs were observed in the group. Horizontal dark grey shadowing indicates the period in which clinical signs were observed in severely ill chimpanzees.

Extended Data Fig. 5 Molecular analyses in faecal samples.

a, Detection of MPXV DNA and non-chimpanzee mammalian DNA b, in chimpanzee faecal samples from the North community over time. Each line represents a chimpanzee. Bold names correspond to chimpanzees in which mild to severe signs compatible with MPXV infection were observed. Boxes represent age groups (infant, juvenile, adolescent and adult). Vertical light grey shadowing indicates the period in which clinical signs were observed in the group. Horizontal dark grey shadowing indicates the period in which clinical signs were observed in severely ill chimpanzees.

Extended Data Fig. 6 Molecular analyses in faecal samples.

a, Detection of MPXV DNA and non-chimpanzee mammalian DNA b, in chimpanzee faecal samples from the East community over time. Each line represents a chimpanzee. Bold names correspond to chimpanzees in which mild to severe signs compatible with MPXV infection were observed. Boxes represent age groups (infant, juvenile, adolescent and adult). Vertical light grey shadowing indicates the period in which clinical signs were observed in the group. Horizontal dark grey shadowing indicates the period in which clinical signs were observed in severely ill chimpanzees.

Extended Data Fig. 7 Social network metrics.

Individual social network metrics in-strength a, out-strength b, in-degree c, and out-degree d, in the North community. Individuals (n=9) are classified as MPXV negative and positive according to PCR results from faecal samples. Timeframes before, during and after the outbreak are based on first and last positive PCR result. The network metrics are also shown for the year 2015 as control. The horizontal line in the whisker plots represents the mean. The lower and upper bounds of the boxes indicate the first and third quartile, respectively. Vertical lines are the upper and lower whisker representing a maximum of the largest/smallest value, but not over 1.5 times the interquartile distance. P values were calculated with a two-sided Mann-Whitney test. (female male). Source data

Extended Data Fig. 8 Ratio of non-chimpanzee mammalian DNA detection in chimpanzee faecal samples from the three communities.

Individuals (n=46) are divided into MPXV positive and negative based on PCR results from faecal samples. The horizontal line in the whisker plots represents the mean. The lower and upper bounds of the boxes indicate the first and third quartile, respectively. Vertical lines are the upper and lower whisker representing a maximum of the largest/smallest value but not over 1.5 times the inter quartile distance. P values were calculated with a two-sided Mann-Whitney test. (female male). Source data

Extended Data Fig. 9 Ratio of non-chimpanzee mammalian DNA detection in faecal samples of female chimpanzees with offspring from the three communities.

Individuals (n=23) are divided into MPXV positive and negative based on the status of their offspring during the outbreaks. The horizontal line in the whisker plots represents the mean. The lower and upper bounds of the boxes indicate the first and third quartile, respectively. Vertical lines are the upper and lower whisker representing a maximum of the largest/smallest value but not over 1.5 times the inter quartile distance. P values were calculated with a two-sided Mann-Whitney test. Source data

Supplementary information

41564_2020_706_MOESM3_ESM.mp4

Monkeypox respiratory symptoms in a wild chimpanzee. This video shows the severe respiratory symptoms, such as breathing with an open mouth, and limited rash observed in a chimpanzee (Pushkin) from the south group infected with MPXV in 2017.

41564_2020_706_MOESM4_ESM.mp4

Monkeypox-limited exanthema and grooming in a wild chimpanzee. This video shows the limited rash observed in a chimpanzee (Ravel) from the south group infected with MPXV in 2017 and grooming, including ingestion of nasal discharge, by group members.

41564_2020_706_MOESM5_ESM.mp4

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the mother is also shown.

41564_2020_706_MOESM6_ESM.mp4

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the sister is also shown.

41564_2020_706_MOESM7_ESM.mp4

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the mother and sister is also shown.

Supplementary Information

Supplementary information guide, discussion, tables 1–6 and Fig. 1.

Reporting Summary

Supplementary Video 1

Monkeypox respiratory symptoms in a wild chimpanzee. This video shows the severe respiratory symptoms, such as breathing with an open mouth, and limited rash observed in a chimpanzee (Pushkin) from the south group infected with MPXV in 2017.

Supplementary Video 2

Monkeypox-limited exanthema and grooming in a wild chimpanzee. This video shows the limited rash observed in a chimpanzee (Ravel) from the south group infected with MPXV in 2017 and grooming, including ingestion of nasal discharge, by group members.

Supplementary Video 3

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the mother is also shown.

Supplementary Video 4

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the sister is also shown.

Supplementary Video 5

Monkeypox diffuse rash and grooming in wild chimpanzees. This video shows the diffuse exanthema and lethargy observed in the chimpanzees from the east community infected with MPXV in 2018. Grooming activity, including ingestion of lesion material, by the mother and sister is also shown.

Supplementary Table

This excel file contains several sheets showing the results that were derived from the non-invasive samples collected during the three MPXV outbreaks (Supplementary Table 3). Results shown include PCR, whole-genome sequencing and virus isolation. The excel file also contains the information on the necropsy samples collected in TNP and included in this study (Supplementary Table 6), providing details on the species that necropsies were performed on as well as types of tissue tested.

Source data

Source Data Fig. 6

Statistical source data.

Source Data Extended Data Fig. 7

Statistical source data.

Source Data Extended Data Fig. 8

Statistical source data.

Source Data Extended Data Fig. 9

Statistical source data.

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Patrono, L.V., Pléh, K., Samuni, L. et al. Monkeypox virus emergence in wild chimpanzees reveals distinct clinical outcomes and viral diversity. Nat Microbiol (2020). https://doi.org/10.1038/s41564-020-0706-0

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