Skip to main content

Advertisement

SpringerLink
Log in

Fast screening of enteropathogens in marine water samples

  • Environmental Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

  • 3 Altmetric

Abstract

This study aimed to fast screen the microbiological contamination of recreational waters using a TaqMan Array Card (TAC), a multiplexed platform designed for the simultaneous detection of 35 enteropathogens. Surface and deep marine water samples were concentrated by skimmed milk flocculation and processed for nucleic acid extraction protocol using QIAamp Fast DNA Stool Mini Kit. Twelve microorganisms and parasites, including bacteria (n = 6), protozoa (4), and viruses (2), were detected in 85.7% (24/28) of samples. Campylobacter (82.1%), Cryptosporidium (39.3%), and adenovirus (14.3%) were the most detected pathogens. Neither fungi nor helminths were detected. A spatial pollution profile of microbiological contamination was observed in the area. Methodologies for simultaneous detection of multiple pathogens, such as TAC, can assist decision-makers by providing a quick assessment of the microbiological water quality in areas used for recreational purposes, which in many cases are in accordance with the bacteriological indicators.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The authors declare that data supporting the findings of this study are available within the article.

Code availability

Not applicable.

References

  1. Girones R, Ferrús MA, Alonso JL, Rodriguez-Manzano J, Calgua B, Corrêa AdeA, Hundesa A, Carratala A, Bofill-Mas S (2010) Molecular detection of pathogens in water - the pros and cons of molecular techniques. Water Res 44(15):4325–4339. https://doi.org/10.1016/j.watres.2010.06.030

    Article  CAS  PubMed  Google Scholar 

  2. Ramírez-Castillo FY, Loera-Muro A, Jacques M, Garneau P, Avelar-González FJ, Harel J, Guerrero-Barrera AL (2015) Waterborne pathogens: detection methods and challenges. Pathogens 4(2):307–334. https://doi.org/10.3390/pathogens4020307

    Article  PubMed  PubMed Central  Google Scholar 

  3. CONAMA - Conselho Nacional do Meio Ambiente/National Environment Council. Ministério do Meio Ambiente. RESOLUÇÃO CONAMA nº 274, de 29 de novembro de 2000. DOU no 18, 25 de janeiro de 2001, Seção 1, páginas 70–71

  4. WHO – World Health Organization (2021) Guidelines on recreational water quality. Volume 1: coastal and fresh waters. World Health Organization, Geneva

  5. Bailey ES, Hopkins M, Casanova L, Sobsey MD (2021) Evaluating fecal indicator and pathogen relationships in sewage impacted surface waters to blend with reclaimed water for potable reuse in North Carolina. Pathogens 10(12):1603. https://doi.org/10.3390/pathogens10121603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Farrell ML, Joyce A, Duane S, Fitzhenry K, Hooban B, Burke LP, Morris D (2021) Evaluating the potential for exposure to organisms of public health concern in naturally occurring bathing waters in Europe: a scoping review. Water Res 206:117711. https://doi.org/10.1016/j.watres.2021.117711

    Article  CAS  PubMed  Google Scholar 

  7. Korajkic A, McMinn BR, Harwood VJ (2018) Relationships between microbial indicators and pathogens in recreational water settings. Int J Environ Res Public Health 15(12):2842. https://doi.org/10.3390/ijerph15122842

    Article  CAS  PubMed Central  Google Scholar 

  8. Gonzales-Gustavson E, Cárdenas-Youngs Y, Calvo M, da Silva MF, Hundesa A, Amorós I, Moreno Y, Moreno-Mesonero L, Rosell R, Ganges L, Araujo R, Girones R (2017) Characterization of the efficiency and uncertainty of skimmed milk flocculation for the simultaneous concentration and quantification of water-borne viruses, bacteria and protozoa. J Microbiol Methods 134:46–53. https://doi.org/10.1016/j.mimet.2017.01.006

    Article  CAS  PubMed  Google Scholar 

  9. Liu J, Gratz J, Amour C, Kibiki G, Becker S, Janaki L, Verweij JJ, Taniuchi M, Sobuz SU, Haque R, Haverstick DM, Houpt ER (2013) A laboratory-developed taqman array card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51(2):472–480. https://doi.org/10.1128/JCM.02658-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Liu J, Kabir F, Manneh J, Lertsethtakarn P, Begum S, Gratz J, Becker SM, Operario DJ, Taniuchi M, Janaki L, Platts-Mills JA, Haverstick DM, Kabir M, Sobuz SU, Nakjarung K, Sakpaisal P, Silapong S, Bodhidatta L, Qureshi S, Kalam A, Saidi Q, Swai N, Mujaga B, Maro A, Kwambana B, Dione M, Antonio M, Kibiki G, Mason CJ, Haque R, Iqbal N, Zaidi AKM, Houpt ER (2014) Development and assessment of molecular diagnostic tests for 15 enteropathogens causing childhood diarrhoea: a multicentre study. Lancet Infect Dis 14(8):716–724. https://doi.org/10.1016/S1473-3099(14)70808-4

    Article  PubMed  Google Scholar 

  11. Fries AS, Coimbra JP, Nemazie DA, Summers RM, Azevedo JPS, Filoso S, Newton M, Gelli G, de Oliveira RCN, Pessoa MAR, Dennison WC (2019) Guanabara Bay ecosystem health report card: science, management, and governance implications. Reg Stu Mar Sci 25:100474. https://doi.org/10.1016/j.rsma.2018.100474

    Article  Google Scholar 

  12. Fistarol GO, Coutinho FH, Moreira AP, Venas T, Cánovas A, de Paula SE Jr, Coutinho R, de Moura RL, Valentin JL, Tenenbaum DR, Paranhos R, do Valle RdeA, Vicente AC, Amado Filho GM, Pereira RC, Kruger R, Rezende CE, Thompson CC, Salomon PS, Thompson FL (2015) l and sanitary conditions of Guanabara Bay Rio de Janeiro. Front Microbiol 6:1232. https://doi.org/10.3389/fmicb.2015.01232

    Article  PubMed  PubMed Central  Google Scholar 

  13. INEA - Instituto Estadual do Ambiente/State Environmental Institute (2021) Dados Brutos do Monitoramento de Qualidade das Águas da Baía de Guanabara. http://www.inea.rj.gov.br/wp-content/uploads/2021/05/Dados-Brutos-2014-2019.pdf. Accessed 31 March 2022

  14. Lertsethtakarn P, Silapong S, Sakpaisal P, Serichantalergs O, Ruamsap N, Lurchachaiwong W, Anuras S, Platts-Mills JA, Liu J, Houpt ER, Bodhidatta L, Swierczewski BE, Mason CJ (2018) Travelers’ diarrhea in Thailand: a quantitative analysis using TaqMan® Array Card. Clin Infect Dis 67(1):120–127. https://doi.org/10.1093/cid/ciy040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Platts-Mills JA, Liu J, Rogawski ET, Kabir F, Lertsethtakarn P, Siguas M, Khan SS, Praharaj I, Murei A, Nshama R, Mujaga B, Havt A, Maciel IA, McMurry TL, Operario DJ, Taniuchi M, Gratz J, Stroup SE, Roberts JH, Kalam A, Aziz F, Qureshi S, Islam MO, Sakpaisal P, Silapong S, Yori PP, Rajendiran R, Benny B, McGrath M, McCormick BJJ, Seidman JC, Lang D, Gottlieb M, Guerrant RL, Lima AAM, Leite JP, Samie A, Bessong PO, Page N, Bodhidatta L, Mason C, Shrestha S, Kiwelu I, Mduma ER, Iqbal NT, Bhutta ZA, Ahmed T, Haque R, Kang G, Kosek MN, Houpt ER, Network Investigators MAL-ED (2018) Use of quantitative molecular diagnostic methods to assess the aetiology, burden, and clinical characteristics of diarrhoea in children in low-resource settings: a reanalysis of the MAL-ED cohort study. Lancet Glob Health 6(12):e1309–e1318. https://doi.org/10.1016/S2214-109X(18)30349-8

    Article  PubMed  PubMed Central  Google Scholar 

  16. Rogawski ET, Liu J, Platts-Mills JA, Kabir F, Lertsethtakarn P, Siguas M, Khan SS, Praharaj I, Murei A, Nshama R, Mujaga B, Havt A, Maciel IA, Operario DJ, Taniuchi M, Gratz J, Stroup SE, Roberts JH, Kalam A, Aziz F, Qureshi S, Islam MO, Sakpaisal P, Silapong S, Yori PP, Rajendiran R, Benny B, McGrath M, Seidman JC, Lang D, Gottlieb M, Guerrant RL, Lima AAM, Leite JP, Samie A, Bessong PO, Page N, Bodhidatta L, Mason C, Shrestha S, Kiwelu I, Mduma ER, Iqbal NT, Bhutta ZA, Ahmed T, Haque R, Kang G, Kosek MN, Houpt ER, Network Investigators MAL-ED (2018) Use of quantitative molecular diagnostic methods to investigate the effect of enteropathogen infections on linear growth in children in low-resource settings: longitudinal analysis of results from the MAL-ED cohort study. Lancet Glob Health 6(12):e1319–e1328. https://doi.org/10.1016/S2214-109X(18)30351-6

    Article  PubMed  PubMed Central  Google Scholar 

  17. IBGE – Instituto Brasileiro de Geografia e Estatística/Brazilian Institute of Geography and Statistics (2021) Rio de Janeiro. https://www.ibge.gov.br/cidades-e-estados/rj/rio-de-janeiro.html?. Accessed 08 October 2021

  18. Soares-Gomes A, da Gama BAP, Baptista Neto JA, Freire DG, Cordeiro RC, Machado W, Bernardes MC, Coutinho R, Thompson FL, Pereira RC (2016) An environmental overview of Guanabara Bay, Rio de Janeiro. Reg Stu Mar Sci 8:319–330. https://doi.org/10.1016/j.rsma.2016.01.009

    Article  Google Scholar 

  19. Calgua B, Mengewein A, Grunert A, Bofill-Mas S, Clemente-Casares P, Hundesa A, Wyn-Jones AP, López-Pila JM, Girones R (2008) Development and application of a one-step low cost procedure to concentrate viruses from seawater samples. J Virol Methods 153(2):79–83. https://doi.org/10.1016/j.jviromet.2008.08.003

    Article  CAS  PubMed  Google Scholar 

  20. Lappan R, Henry R, Chown SL, Luby SP, Higginson EE, Bata L, Jirapanjawat T, Schang C, Openshaw JJ, O’Toole J, Lin A, Tela A, Turagabeci A, Wong THF, French MA, Brown RR, Leder K, Greening C, McCarthy D (2021) Monitoring of diverse enteric pathogens across environmental and host reservoirs with TaqMan array cards and standard qPCR: a methodological comparison study. Lancet Planet Health 5(6):e297–e308. https://doi.org/10.1016/S2542-5196(21)00051-6.ErratuminLancetPlanetHealth.2021Jun;5(6):e336

    Article  PubMed  PubMed Central  Google Scholar 

  21. Baker KK, Senesac R, Sewell D, Sen Gupta A, Cumming O, Mumma J (2018) Fecal fingerprints of enteric pathogen contamination in public environments of Kisumu, Kenya, associated with human sanitation conditions and domestic animals. Environ Sci Technol 52(18):10263–10274. https://doi.org/10.1021/acs.est.8b01528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pedrosa de Macena LDG, Castiglia Feitosa R, Vieira CB, Araújo IT, Taniuchi M, Miagostovich MP (2021) Microbiological assessment of an urban lagoon system in the coastal zone of Rio de Janeiro. Brazil Environ Sci Pollut Res Int 28(1):1170–1180. https://doi.org/10.1007/s11356-020-10479-8

    Article  CAS  PubMed  Google Scholar 

  23. Pitkanen T, Hanninen M-L (2017) Members of the family Campylobacteraceae: Campylobacter jejuni, Campylobacter coli. In Rose JB, Jiménez-Cisneros B (eds) Water and sanitation for the 21st century: health and microbiological aspects of excreta and wastewater management (Global Water Pathogen Project), 1st edn. Michigan State University, E. Lansing, MI, UNESCO. http://www.waterpathogens.org/book/campylobacter. Accessed 08 October 2021

  24. Aquino MH, Filgueiras AL, Matos R, Santos KR, Ferreira T, Ferreira MC, Teixeira LM, Tibana A (2010) Diversity of Campylobacter jejuni and Campylobacter coli genotypes from human and animal sources from Rio de Janeiro. Brazil Res Vet Sci 88(2):214–217. https://doi.org/10.1016/j.rvsc.2009.08.005

    Article  CAS  PubMed  Google Scholar 

  25. Gomes CN, Souza RA, Passaglia J, Duque SS, Medeiros MIC, Falcão JP (2016) Genotyping of Campylobacter coli strains isolated in Brazil suggests possible contamination amongst environmental, human, animal and food sources. J Med Microbiol 65(1):80–90. https://doi.org/10.1099/jmm.0.000201

    Article  CAS  PubMed  Google Scholar 

  26. Operario DJ, Platts-Mills JA, Nadan S, Page N, Seheri M, Mphahlele J, Praharaj I, Kang G, Araujo IT, Leite JPG, Cowley D, Thomas S, Kirkwood CD, Dennis F, Armah G, Mwenda JM, Wijesinghe PR, Rey G, Grabovac V, Berejena C, Simwaka CJ, Uwimana J, Sherchand JB, Thu HM, Galagoda G, Bonkoungou IJO, Jagne S, Tsolenyanu E, Diop A, Enweronu-Laryea C, Borbor SA, Liu J, McMurry T, Lopman B, Parashar U, Gentsch J, Steele AD, Cohen A, Serhan F, Houpt ER (2017) Etiology of severe acute watery diarrhea in children in the global rotavirus surveillance network using quantitative polymerase chain reaction. J Infect Dis 216(2):220–227. https://doi.org/10.1093/infdis/jix294.Erratum.In:JInfectDis.2017216(8):1048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chukwu MO, Luther King Abia A, Ubomba-Jaswa E, Obi L, Dewar JB (2019) Characterization and phylogenetic analysis of campylobacter species isolated from paediatric stool and water samples in the Northwest Province, South Africa. Int J Environ Res Public Health 16(12):2205. https://doi.org/10.3390/ijerph16122205

    Article  CAS  PubMed Central  Google Scholar 

  28. Szczepanska B, Andrzejewska M, Spica D, Klawe JJ (2017) Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol 17(1):80. https://doi.org/10.1186/s12866-017-0991-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Castilho MC, Castro TL, Araújo VS, Trajano RS, Santos PA, Pimenta PM, Lucheze K, Melo JT, Gonçalves AM, Nogueira RT, de Luna MG, Freitas-Almeida AC (2009) High frequency of hemolytic and cytotoxic activity in Aeromonas spp. isolated from clinical, food and environmental in Rio de Janeiro Brazil. Antonie Van Leeuwenhoek 96(1):53–61. https://doi.org/10.1007/s10482-009-9335-6

    Article  CAS  PubMed  Google Scholar 

  30. Momba M, Azab El-Liethy M (2017) vibrio cholerae and cholera biotypes. In Rose JB, Jiménez-Cisneros B (eds) Water and sanitation for the 21st century: health and microbiological aspects of excreta and wastewater management (global water pathogen project), 1st edn. Michigan State University, E. Lansing, MI, UNESCO. https://www.waterpathogens.org/book/Vibrio. Accessed 31 March 2022

  31. Brasil, Ministério da Saúde/ Ministry of Health (2021) Cólera: causas, sintomas, transmissão, tratamento e diagnóstico. https://www.gov.br/saude/pt-br/assuntos/saude-de-a-a-z/c/colera/colera. Accessed 31 March 2022

  32. Aw T (2018) Environmental aspects and features of critical pathogen groups. In Rose JB, Jiménez-Cisneros B (eds) Water and sanitation for the 21st century: health and microbiological aspects of excreta and wastewater management (global water pathogen project), 1st edn. Michigan State University, E. Lansing, MI, UNESCO. http://www.waterpathogens.org/book/environmental-aspects-and-features-of-critical-pathogen-groups. Accessed 08 October 2021

  33. Efstratiou A, Ongerth J, Karanis P (2017) Evolution of monitoring for giardia and cryptosporidium in water. Water Res 123:96–112. https://doi.org/10.1016/j.watres.2017.06.042

    Article  CAS  PubMed  Google Scholar 

  34. Barbosa CV, Barreto MM, Andrade RJ, Sodré F, d’Avila-Levy CM, Peralta JM, Igreja RP, de Macedo HW, Santos HLC (2018) Intestinal parasite infections in a rural community of Rio de Janeiro (Brazil): prevalence and genetic diversity of Blastocystis subtypes. PLoS ONE 13(3):e0193860. https://doi.org/10.1371/journal.pone.0193860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Carvalho-Costa FA, Gonçalves AQ, Lassance SL, de Albuquerque CP, Leite JP, Bóia MN (2007) Detection of Cryptosporidium spp and other intestinal parasites in children with acute diarrhea and severe dehydration in Rio de Janeiro. Rev Soc Bras Med Trop 40(3):346–348. https://doi.org/10.1590/s0037-86822007000300020

    Article  PubMed  Google Scholar 

  36. Dos Santos Zanetti A, Malheiros AF, de Matos TA, Dos Santos C, Battaglini PF, Moreira LM, Lemos LMS, Castrillon SKI, da Costa BoamorteCortela D, Ignotti E, Espinosa OA (2021) Diversity, geographical distribution, and prevalence of Entamoeba spp in Brazil: a systematic review and meta-analysis. Parasite 28:17. https://doi.org/10.1051/parasite/2021028

    Article  PubMed  PubMed Central  Google Scholar 

  37. Rames E, Roiko A, Stratton H, Macdonald J (2016) Technical aspects of using human adenovirus as a viral water quality indicator. Water Res 96:308–326. https://doi.org/10.1016/j.watres.2016.03.042

    Article  CAS  PubMed  Google Scholar 

  38. Dias J, Pinto RN, Vieira CB, de Abreu CA (2018) Detection and quantification of human adenovirus (HAdV), JC polyomavirus (JCPyV) and hepatitis A virus (HAV) in recreational waters of Niterói, Rio de Janeiro, Brazil. Mar Pollut Bull 133:240–245. https://doi.org/10.1016/j.marpolbul.2018.05.031

    Article  CAS  PubMed  Google Scholar 

  39. Staggemeier R, Heck TMS, Demoliner M, Ritzel RGF, Röhnelt NMS, Girardi V, Venker CA, Spilki FR (2017) Enteric viruses and adenovirus diversity in waters from 2016 Olympic venues. Sci Total Environ 586:304–312. https://doi.org/10.1016/j.scitotenv.2017.01.223

    Article  CAS  PubMed  Google Scholar 

  40. Victoria M, Fumian TM, Rocha MS, Dalmao F, Leite JP, Girones R, Miagostovich MP (2014) Gastroenteric virus dissemination and influence of rainfall events in urban beaches in Brazil. J Appl Microbiol 117(4):1210–1218. https://doi.org/10.1111/jam.12592

    Article  CAS  PubMed  Google Scholar 

  41. Fumian TM, Vieira CB, Leite JP, Miagostovich MP (2013) Assessment of burden of virus agents in an urban sewage treatment plant in Rio de Janeiro. Brazil J Water Health 11(1):110–119. https://doi.org/10.2166/wh.2012.123

    Article  CAS  PubMed  Google Scholar 

  42. Portes S, Carvalho-Costa FA, Rocha MS, Fumian TM, Maranhão AG, de Assis RM, Xavier M, Rocha MS, Miagostovich MP, Leite J, Volotão EM (2017) Enteric viruses in HIV-1 seropositive and HIV-1 seronegative children with diarrheal diseases in Brazil. PLoS ONE 12(8):e0183196. https://doi.org/10.1371/journal.pone.0183196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Xavier Mda P, Carvalho Costa FA, Rocha MS, Andrade Jda S, Diniz FK, Andrade TR, Miagostovich MP, Leite JP, Volotão Ede M (2015) Surveillance of human astrovirus infection in Brazil: the first report of MLB1 Astrovirus. PLoS ONE 10(8):e0135687. https://doi.org/10.1371/journal.pone.0135687

    Article  CAS  PubMed  Google Scholar 

  44. Coelho V (2007) Baia de Guanabara: Uma História de Agressão Ambiental. Casa Da Palavra, Rio de Janeiro

    Google Scholar 

Download references

Acknowledgements

We thank Prof. Dr. Renato da Silva Carreira, Pontifical Catholic University of Rio de Janeiro (PUC-Rio), for helping in the first sampling and to Eric Houpt (Rotanetwork University of Virginia/CDC/PAHO/WHO) for TAC provisioning. This research work is within the scope of the activities of FIOCRUZ as a collaborating center of PAHO/WHO of Public and Environmental Health.

Funding

This work was funded by the Brazilian National Council for Scientific and Technological Development [CNPq, grant numbers 406414/2016–5, 166082/2015–5].

Author information

Authors and Affiliations

  1. Department of Microbiology and Parasitology, Federal Fluminense University, Niterói, Rio de Janeiro, Brazil

    Carmen Baur Vieira

  2. Laboratory of Comparative and Environmental Virology, Oswaldo Cruz Foundation, Rio de Janeiro, Rio de Janeiro, Brazil

    Irene Trigueiros Araújo, Fernando César Ferreira & Marize Pereira Miagostovich

  3. Division of Infectious Diseases and International Health, University of Virginia, Charlottesville, VA, USA

    Jie Liu

  4. Department of Sanitation and Environmental Health, Oswaldo Cruz Foundation, Rio de Janeiro, Rio de Janeiro, Brazil

    Renato Castiglia Feitosa

Authors
  1. Carmen Baur Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Irene Trigueiros Araújo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando César Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Renato Castiglia Feitosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Marize Pereira Miagostovich
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study conception and design were performed by Carmen Baur Vieira, Marize Pereira Miagostovich, and Renato Castiglia Feitosa. Material preparation and data collection were performed by Carmen Baur Vieira, Irene Trigueiros Araújo, and Fernando César Ferreira. Jie Liu and Irene Trigueiros Araújo contributed to the TAC methodology. Analysis was performed by Carmen Baur Vieira. The first draft of the manuscript was written by Carmen Baur Vieira, Marize Pereira Miagostovich, and Renato Castiglia Feitosa. Marize Pereira Miagostovich contributed to the project administration and funding acquisition. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Carmen Baur Vieira.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflicts of interest

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 60 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Vieira, C.B., Araújo, I.T., Ferreira, F.C. et al. Fast screening of enteropathogens in marine water samples. Braz J Microbiol 53, 1439–1446 (2022). https://doi.org/10.1007/s42770-022-00770-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-022-00770-w

Keywords

Search

Navigation