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Phylogenetic and network analysis of Pediculus humanus in Nigeria reveal the presences of clade E body lice and novel haplotypes

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Abstract

An investigation was conducted for the first time to determine the prevalence and genetic diversity of human lice, for the first time in Nigeria, using conventional PCR and sequencing methods. Three mitochondrial genes, cytochrome oxidase subunit 1 (cox1), cytochrome b (cytb), and 12S rRNA of Nigerian human lice, were amplified, sequenced, and analyzed. Overall, high prevalence (72.5%; 103/142) of lice infestation was recorded among the examined volunteers. Head lice infestation was more common 63 (61.2%) than body lice infestation 34 (33.0%). Co-infestation with both head and body lice was recorded in six humans (5.8%). The Nigerian human lice specimens were placed mostly into clade A with few in clade E, including body lice for the first time. Six, three, and eight haplotypes of Nigerian human lice were obtained for the cytb, cox1, and 12S rRNA genes, respectively. Additionally, one (E51), three (A31, A32, and E5), and six (A20, A21, A23, A24, A30, and E1) novel haplotypes were recorded for cox1, cytb, and 12S rRNA, respectively, from the Nigerian specimens which were corroborated by the ML phylogenetic trees and MJ network analyses. Genetic diversity indices indicate minimal variation in the parameters analyzed among the clades of the three genes. However, a statistically significant Snn test, negative Tajima’s D test for clade A (cox1 and 12S rRNA genes), and negative Fu and Li’s D test in clade A for cox1 gene indicate a geographical structure and the signature of population expansion of the Nigerian human lice. The findings from this study provide additional data on the human lice structure in Africa.

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Data availability

Nucleotide sequences generated in this study have been deposited in GenBank and is publically available. Other data can be made available on request to the authors.

References

  • Amanzougaghene N, Mumcuoglu KY, Fenollar F, Alfi S, Yesilyurt G, Raoult D et al (2016a) High ancient genetic diversity of human lice, Pediculus humanus, from Israel reveals new insights into the origin of clade b lice. PloS One 11:1–14. https://doi.org/10.1371/journal.pone.0164659

    Article  CAS  Google Scholar 

  • Amanzougaghene N, Akiana J, Mongo Ndombe G, Davoust B, Nsana NS, Parra HJ et al (2016b) Head lice of pygmies reveal the presence of relapsing fever Borreliae in the Republic of Congo. PLoS NTDs 10:1–18. https://doi.org/10.1371/journal.pntd.0005142

    Article  CAS  Google Scholar 

  • Amanzougaghene N, Fenollar F, Sangaré AK, Sissoko MS, Doumbo OK, Raoult D (2017) Detection of bacterial pathogens including potential new species in human head lice from Mali. PloS One 12:e0184621

    Article  PubMed  PubMed Central  Google Scholar 

  • Amanzougaghene N, Fenollar F, Davoust B, Djossou F, Ashfaq M, Bitam I, Raoult R, Mediannikov O (2019) Mitochondrial diversity and phylogeographic analysis of Pediculus humanus reveals a new Amazonian Clade “F”. Infect Genet Evol 70:1–8. https://doi.org/10.1016/j.meegid.2019.02.006

    Article  CAS  PubMed  Google Scholar 

  • Amanzougaghene N, Fenollar F, Raoult D, Mediannikov O (2020a) Where are we with human lice? A review of the current state of knowledge. Front Cell Infect Microbiol 9. https://doi.org/10.3389/fcimb.2019.00474

  • Amanzougaghene N, Mediannikov O, Ly TDA, Gautret P, Davoust B, Fenollar F et al (2020b) Molecular investigation and genetic diversity of Pediculus and Pthirus lice in France. Parasite Vect 13(1):177. https://doi.org/10.1186/s13071-020-04036-y

    Article  Google Scholar 

  • Angelakis E, Rolain JM, Raoult D, Brouqui P (2011) Bartonella quintana in head louse nits. FEMS Immunol & Med Microbiol 62:244–246

    Article  CAS  Google Scholar 

  • Araújo A, Ferreira LF, Guidon N, Maues Da Serra Freire N, Reinhard KJ, Dittmar K (2000) Ten thousand years of head lice infection. Parasitol Today 16:269. https://doi.org/10.1016/S0169-4758(00)01694-X

    Article  PubMed  Google Scholar 

  • Aris-Brosou S, Excoffier L (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol Biol Evol 13:494–504. https://doi.org/10.1093/oxfordjournals.molbev.a025610

    Article  CAS  PubMed  Google Scholar 

  • Ascunce MS, Fane J, Kassu G, Toloza AC, Picollo MI, González-Oliver A et al (2013) Mitochondrial diversity in human head louse populations across the Americas. American J Phys Anthropol 152:118–129. https://doi.org/10.1002/ajpa.22336

    Article  Google Scholar 

  • Ashfaq M, Prosser S, Nasir S, Masood M, Ratnasingham S, Hebert PDN (2015) High diversity and rapid diversification in the head louse, Pediculus humanus (Pediculidae: Phthiraptera). Sci Rep 5:14188. https://doi.org/10.1038/srep14188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036

    Article  CAS  PubMed  Google Scholar 

  • Bonilla DL, Durden LA, Eremeeva ME, Dasch GA (2013) The biology and taxonomy of head and body lice—implications for louse-borne disease prevention. PLoS Pathog 9(11):e1003724. https://doi.org/10.1371/journal.ppat.1003724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boumbanda Koyo CS, Amanzougaghene N, Davoust B, Tshilolo L, Lekana-Douki JB, Raoult D, Mediannikov O, Fenollar F (2019) Genetic diversity of human head lice and molecular detection of associated bacterial pathogens in Democratic Republic of Congo. Parasite Vect 12:290

    Article  Google Scholar 

  • Boumbanda-Koyo CS, Mediannikov O, Amanzougaghene N, Oyegue-Liabagui SL, Imboumi-Limoukou RK, Raoult D, Lekana-Douki JB, Fenollar F (2020) Molecular identification of head lice collected in Franceville (Gabon) and their associated bacteria. Parasite Vect 13:410

    Article  CAS  Google Scholar 

  • Boutellis A, Bitam I, Fekir K, Mana N, Raoult D (2015) Evidence that clade A and clade B head lice live in sympatry and recombine in Algeria. Med Vet Entomol 29:94–98

    Article  CAS  PubMed  Google Scholar 

  • Boutellis A, Veracx A, Angelakis E, Diatta G, Mediannikov O, Raoult D (2012) Bartonella quintana in head lice from Senegal. Vector Borne Zoonotic Dis 12:564–567

    Article  PubMed  Google Scholar 

  • Brouqui P (2011) Arthropod-borne diseases associated with political and social disorder. Annu Rev Entomol 56:357–374. https://doi.org/10.1146/annurev-ento-120709-144739

    Article  CAS  PubMed  Google Scholar 

  • Burgess IF (1995) Human lice and their management. Adv Parasitol 36:271–342

    Article  CAS  PubMed  Google Scholar 

  • Candy K, Amanzougaghene N, Izri A, Brun S, Durand R, Louni M, Raoult D, Fenollar F, Mediannikov O (2028) Molecular survey of head and body lice, Pediculus humanus, in France. Vector-Borne Zoon Dis 18:243–251

    Article  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drali R, Shako JC, Davoust B, Diatta G, Raoult D (2015) A new clade of African body and head lice infected by Bartonella quintana and Yersinia pestis - Democratic Republic of the Congo. Am J Trop Med Hyg 93:990–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drali R, Boutellis A, Raoult D, Rolain JM, Brouqui P (2013) Distinguishing body lice from head lice by multiplex real-time PCR analysis of the Phum_PHUM540560 Gene. PloS One 8:1–6. https://doi.org/10.1371/journal.pone.0058088

    Article  CAS  Google Scholar 

  • Eichler W (1956) Three new forms of head-lice from New Guinea, Java and Southwest Africa. Dermatol Wochenschr 133:657–660

    CAS  PubMed  Google Scholar 

  • Eichler W (1982) Head lice problems. I. Taxonomic position of Pediculus capitis. Angew Parasitol 23:102–109

    CAS  PubMed  Google Scholar 

  • Ewing HE (1926) A revision of the American lice of the genus Pediculus, together with a consideration of the significance of their geographical and host distribution. Proceedings of the US National Museum 68(p):1–30

    Article  Google Scholar 

  • Hammoud A, Louni M, Baldé MC, Beavogui AH, Gautret P, Raoult D, Fenollar F, Misse D, Mediannikov O (2021) Molecular characterization and genetic diversity of haplogroup E human lice in Guinea, West Africa. Microorganisms. 9:257. https://doi.org/10.3390/microorganisms9020257

    Article  PubMed  PubMed Central  Google Scholar 

  • Izri A, Uzzan B, Maigret M, Gordon MS, Bouges-Michel C (2010) Clinical efficacy and safety in head lice infection by Pediculus humanis capitis De Geer (Anoplura: Pediculidae) of a capillary spray containing a silicon-oil complex. Parasite 17:329–335. https://doi.org/10.1051/parasite/2010174329

    Article  CAS  PubMed  Google Scholar 

  • Kempf M, Abdissa A, Diatta G, Trape JF, Angelakis E, Mediannikov O et al (2012) Detection of Acinetobacter baumannii in human head and body lice from Ethiopia and identification of new genotypes. Int J Infect Dis 16:14–16

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Leo NP, Barker SC (2005) Unravelling the evolution of the head lice and body lice of humans. Parasitol Res 98:44–47

    Article  PubMed  Google Scholar 

  • Light JE, Allen JM, Long LM, Carter TE, Barrow L, Raoult D et al (2008) Geographic distributions and origins of human head lice (Pediculus humanus capitis) based on mitochondrial data. J Parasitol 94:1275–1281. https://doi.org/10.1645/GE-1618.1

    Article  PubMed  Google Scholar 

  • Louni M, Amanzougaghene N, Mana N, Fenollar F, Raoult D, Bitam I, Mediannikov O (2018) Detection of bacterial pathogens in clade E head lice collected from Niger’s refugees in Algeria. Parasites Vect 11:348

    Article  Google Scholar 

  • Mumcuoglu K (2008) Pediculus and Pthirus. In: Raoult D, Drancourt M (eds) Paleomicrobiology of Past human infections. Springer, pp 215–222. https://doi.org/10.1007/978-3-540-75855-6

    Chapter  Google Scholar 

  • Nuttall GHF (1920) On Fahrenholz’s purported new species subspecies and varieties of Pediculus. Parasitol. 12:136–153

    Article  Google Scholar 

  • R Development Core Team R (2019) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, p 2009

    Google Scholar 

  • Raoult D, Reed DL, Dittmar K, Kirchman JJ, Rolain JM, Guillen S, Light JE (2008) Molecular identification of lice from pre-Columbian mummies. J Infect Dis 197:535–543

    Article  PubMed  Google Scholar 

  • Reed DL, Smith VS, Hammond SL, Rogers AR, Clayton DH (2004) Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biol 2. https://doi.org/10.1371/journal.pbio.0020340

  • Sangaré AK, Boutellis A, Drali R, Socolovschi C, Barker SC, Diatta G et al (2014) Detection of Bartonella quintana in African body and head lice. Am J Trop Med Hyg 91:294–301

    Article  PubMed  PubMed Central  Google Scholar 

  • Sunantaraporn S, Sanprasert V, Pengsakul T, Phumee A, Boonserm R, Tawatsin A et al (2015) Molecular survey of the head louse Pediculus humanus capitis in Thailand and its potential role for transmitting Acinetobacter spp. Parasite Vect 8:127

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tobe SS, Kitchener A, Linacre A (2009) Cytochrome b or cytochrome c oxidase subunit I for mammalian species identification an answer to the debate. Forensic Sci Int Genet Suppl Ser 2:306–307

    Article  Google Scholar 

  • Veracx A, Rivet R, McCoy KD, Brouqui P, Raoult D (2012) Evidence that head and body lice on homeless persons have the same genotype. PloS One:e45903

  • Xiong H, Campelo D, Pollack RJ, Raoult D, Shao R, Alem M et al (2014) Second-generation sequencing of entire mitochondrial coding-regions (~15.4kb) holds promise for study of the phylogeny and taxonomy of human body lice and head lice. Med Vet Entomol 28:40–50. https://doi.org/10.1111/mve.12076

    Article  PubMed  Google Scholar 

  • Yong Z, Fournier PE, Rydkina E, Raoult D (2003) The geographical segregation of human lice preceded that of Pediculus humanus capitis and Pediculus humanus humanus. C R Biol 326:565–574

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Gajibo, AU, Laminu B, and Modu M for their assistance during the human lice samples collection.

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Authors and Affiliations

  1. Parasitology Division, National Veterinary Research Institute (NVRI), Vom, Plateau State, PMB 01, Nigeria

    Joshua Kamani

  2. Animal Health Research Centre, National Institute for Agricultural and Food Research and Technology (INIA), Centro Superior de Investigaciones Científicas (CSIC), Valdeolmos, Madrid, Spain

    Sacristán Irene

  3. Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel

    Yaarit Nachum-Biala & Shimon Harrus

  4. School of Geographical and Earth Sciences, University of Glasgow, Glasgow, UK

    Mike Shand

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Contributions

All authors read and approved the final version of the manuscript. Conceptualization, Investigation, Methodology, Writing—original draft; Writing—review &; editing (Joshua Kamani). Investigation, Data curation, Formal analysis, writing— review &; editing (Irene Sacristán) Investigation, Methodology, Writing—review &; editing (Nachum-Biala Yaarit). Design fig.1, Data curation, Formal analysis, writing—review &; editing (Mike Shand). Conceptualization, Methodology, Supervision, writing—review &; editing (Harrus Shimon)

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Correspondence to Joshua Kamani.

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Ethical approval

Lice sampling was made in line with the specifications of the Declaration of Helsinki of the World Medical Association for the non-invasive sample collection from humans. Prior to sample collection, the representatives of the volunteers and the local authorities were briefed about the purpose of the study.

Consent to participate

Verbal consent to participate in the study and for the results to be published was obtained from each of the volunteers before they were examined for the presence of lice on the head or on their clothing in the presence of their representatives.

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The authors declare no competing interests.

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Kamani, J., Irene, S., Nachum-Biala, Y. et al. Phylogenetic and network analysis of Pediculus humanus in Nigeria reveal the presences of clade E body lice and novel haplotypes. Parasitol Res 122, 3087–3100 (2023). https://doi.org/10.1007/s00436-023-07999-w

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