Main Article Content
Abstract
Biofilms encompass a cluster of microorganisms encased in a slimy matrix of extracellular polymeric substances, which imbibe antibiotic resistance. Salmonella specie is a major bacterial cause of food-borne diseases in both humans and animals. The prevalence of Salmonella species is increasing which may form biofilm, and bacteria that form biofilm may be more resistant to antimicrobial agents. This study is intended to determine the presence and antimicrobial susceptibility patterns of Salmonella species among greater cane rats and carry out the biofilm formation of isolated Salmonella species and dispersion using Garcinia kola. A total of 20 cane rats were obtained from a farm in Lagos state and roadside hunters. Samples of rectal swabs were collected aseptically for bacterial culture. Bacteria isolation was done with selective media using standard bacteriological techniques following pre-enrichment of the samples with buffered peptone water. Gram staining and biochemical tests were used for confirmation of the organisms. An antimicrobial susceptibility test was performed following standard protocol. Zones of inhibition were measured and categorized as totally sensitive and resistant. Nine (9) isolates of Salmonella species were obtained from rectal swabs of greater cane rats. A modified crystal violet assay was employed to develop biofilm and test the effect of a crude extract of Garcinia kola on biofilm dispersal. Data obtained from this study was subjected to statistical analysis using descriptive statistics and paired t-test at a level of significance of P ≤ 0.05. The overall prevalence of Salmonella species obtained in this study was 45%. Antimicrobial study showed susceptibility of 77.8% for Chloramphenicol and 66.7% for Cefuroxime while all isolates were 100% susceptible to Amikacin and Gentamicin. The effect of Garcinia kola extract on different isolates at 430nm showed a significant difference (p= 0.0348) in biofilm formation in isolates with Garcinia kola extract when compared with isolates without extract. The effect of Garcinia kola extract on different isolates at 650nm elicited significant (p = 0.0216) biofilm inhibitions across the isolates. The antibiofilm activity displayed by Garcinia kola suggests its potential to serve as an alternative antimicrobial agent to combat drug resistant bacteria such as Salmonella species. However, further investigations should be carried out on the individual bioactive compounds to know the exact metabolites responsible for the antibiofilm activity of this bacteria species.
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References
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- Abebe, E., Gugsa, G. and Ahmed, M. (2020). Review on major food-borne zoonotic bacterial pathogens. J. Trop. Med., 2020:4674235, DOI: 10.1155/2020/4674235
- Adedeji, M. I. and Adetunji, V. O. (2020). Antibiofilm activities of ginger (Zingiberofficinale) on E. coli O157:H7 isolates from powdered milk in Ibadan, Nigeria. Res. J. Microbiol., 15(3): 90-97 DOI: 10.17311/jm.2020.90.97
- Adegboye, M., Akinpelu, D. and Okoh, A. (2008). The bioactive and phytochemical properties of Garcinia kola (heckel) seed extract on some pathogens. Afr. J. Biotechnol. 7(21): 3934-3938 DOI: 10.4314/ajb.v7i21.59484
- Amala, P. V., Sumithra, T. G., Reshma, K. J., Anusree, V. N., Sayooj, P. and Vijayagopal, P. (2021). Revisiting Substrate Specificity Concept in Microbial Screening Methodologies for Fish Waste Management. Turk. J. Fish. Aquat. Sci. 21(7): 323-332. 2 DOI: 10.4194/1303-2712-v21_7_02
- Amaral, V. C. S., Santos, P. R., Fiori da Silva, A., Santos, A., MachinskiJunioir, M. and Mikcha, J. (2015). Effect of carvacrol and thymol on Salmonella spp. biofilms on polypropylene. Int. J. Food Sci. Tech., 50(12): 2639-2643 DOI: 10.1111/ijfs.12934
- Clinical Laboratory Standard Institute (2020). M100 performance standards for antimicrobial susceptibility testing. 30th ed, Wayne, Pennsylvania, United States of America.
- Ekene, E. and Earnest, O. E. (2014). Garciniakola: a review of its ethnomedicinal, chemical and pharmacological properties. Int. J. Curr. Res. Rev., 6(11): 1-7 https://api.semanticscholar.org/CorpusID:70639553
- Eguale, T., Gebreyes, W., Asrat, D., Alemayehu, H., Gunn, J. S. and Engidawork, E. (2015). Non-typhoidal salmonella serotypes, antimicrobial resistance and coinfection with parasites among patients with diarrhea and other gastrointestinal complaints in Addis Ababa, Ethiopia. BMC Infect Dis., 15:497. DOI: 10.1186/s12879-015-1235-y
- Ejo, M., Garedew, L., Alebachew, Z. and Worku, W. (2016). Prevalence and antimicrobial resistance of Salmonella isolated from animal-origin food items in Gondar, Ethiopia. BiomedRes. Int., 2016:4290506 DOI: 10.1155/2016/4290506
- Fatope, M. O., Ibrahim, H. and Takeda, Y. (1993). Screening of higher plants reputed as pesticides using the brine shrimp lethality assay.Int. J. Pharmacol., 31(4): 250-254 DOI: https://doi.org/10.3109/13880209309082949
- Feasey, N. A., Dougan, G., Kingsley, R. A., Heyderman, R. S. and Gordon, M. A. (2012). Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 379(9835): 2489–2499 DOI: 10.1016/S0140-6736(11)61752-2
- Hakimi, A, R., Ghorban, K. and Dadmanesh, M. (2020). Combined effects of Alliumsativum and Cuminumcyminum essential oils on planktonic and biofilm forms of Salmonella typhimurium isolates. 3 Biotech., 10(7): 315 DOI: 10.1007/s13205-020-02286-2
- Fàbrega, A. and Vila, J. (2013). Salmonellaenterica serovar typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev., 26(2): 308–341. DOI: 10.1128/CMR.00066-12.
- Fan, Q., He, Q., Zhang, T., Song, W., Sheng, Q., Yuan, Y. and Yue, T. (2022). Antibiofilm potential of lactobionic acid against Salmonellatyphimurium. LWT Food Sci. Technol., 162: 0023-6438 DOI: 10.1016/j.lwt.2022.113461
- FAO. (2021). Action Plan on Antimicrobial Resistance 2021–2025. FAO. DOI: 10.4060/cb5545en [Accessed 11th August 2023]
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- Hemmati, F., Rezaee, M. A., Ebrahimzadeh, S., Yousefi, L., Nouri, R., Kafil, H. S. and Gholizadeh, P. (2021). Novel strategies to combat bacterial biofilms. Mol. Biotechnol. 63(7): 569-586 DOI: 10.1007/s12033-021-00325-8
- Hye-Jin, Seo. and Kang, S. S. (2020). Inhibitory effect of bacteriocin produced by Pediococcusacidilactici on the biofilm formation of Salmonellatyphimurium. Food Control. 117: 107361 DOI:10.1016/j.foodcont.2020.107361
- Jaja, I. F., Bhembe, N. L., Green, E., Oguttu, J. and Muchenje, V. (2019). Molecular characterisation of antibiotic-resistant Salmonellaenterica isolates recovered from meat in South Africa. Acta Tropi., 190: 129–136 DOI: 10.1016/j.actatropica.2018.11.003
- Jajere, S. M. (2019). A review of Salmonellaenterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet. World 12(4): 504–521. DOI: 10.14202/vetworld.2019.504-521
- Keerthirathne, T. P., Ross, K., Fallowfield, H. and Whiley, H. (2022). Examination of Australian backyard poultry for Salmonella, Campylobacter and Shigella spp., and related risk factors. Zoonoses Public Health. 69(1): 13–22. DOI: 10.1111/zph.12889
- Maier, B. (2021). How physical interactions shape bacterial biofilms. Annu. Rev. Biophys., 50(1): 401–417 DOI: 10.1146/annurev-biophys-062920-063646
- Kiflu, B., Alemayehu, H., Abdurahaman, M., Negash, Y. and Eguale, T. (2017). Salmonella serotypes and their antimicrobial susceptibility in apparently healthy dogs in Addis Ababa Ethiopia. BMC Vet Res., 13(1): 1–9. DOI: 10.1186/s12917-017-1055-y
- Marami, D., Hailu, K. and Tolera, M. (2018). Prevalence and antimicrobial susceptibility pattern of Salmonella and Shigella species among asymptomatic food handlers working in Haramaya University Cafeterias, Eastern Ethiopia. BMC Res. Notes 11(1): 74 DOI: 10.1186/s13104-018-3189-9
- Morshdy, A. E. M. A., El-Tahlawy, A. S., Qari, S. H., Qumsani, A. T., Bay, D. H., Sami, R., Althubaiti, E. H., Mansour, A. M. A., Aljahani, A. H., Hafez, A. E. E., Mahmoud, A. F. A., El Bayomi, R. M. and Hussein, M. A. (2022). Anti-biofilms' activity of garlic and thyme essential oils against Salmonella Typhimurium. Molecules (Basel, Switzerland) 27(7): 2182 DOI: 10.3390/molecules27072182
- Oboegbulem, S. I. and Okoronkwo, I. (1990). Salmonellae in the African great cane rat (Thryonomysswinderianus). J. Wildl. Dis., 26(1): 119–121. DOI: 10.7589/0090-3558-26.1.119
- Ogbor, O., Ajayi, A., Zautner, A. E. and Smith, S. I. (2019). Antibiotic Susceptibility profiles of Campylobactercoli isolated from poultry farms in Lagos Nigeria – a pilot study. Eur. J. Microbiol. Immunol., 9(2): 2–34. DOI: 10.1556/1886.2019.00007
- Oludairo, O. O., Kwaga J.K.P., Dzikwi A.A. and Kabir J. (2013). The genus Salmonella, isolation and occurrence in wildlife. Int. J. Microbiol. Immunol. Res., 1(5): 047–052 http://hdl.handle.net/123456789/2849
- Opara, M. N. (2010). Grasscutter: the haematology and major parasites. Res. J. Parasitol., 5(4): 214-223 https://scialert.net/abstract/?doi=jp.2010.214.223
- Orum, T. G., Ishola, O. O. and Adebowale, O. O. (2022). Occurrence and antimicrobial susceptibility patterns of Salmonella species from poultry farms in Ibadan, Nigeria. Afr. J. Lab. Med., 11(1): 1606. DOI: 10.4102/ajlm.v11i1.1606
- Okoronkwo, M.O., Suleiman, M.M., Chiezey, N., Udechukwu, C.C., Oyetunde, J.S. and Jolayemi, K.O. (2022). Anti-diarrhoeal effects of Garciniakola (heckel-holl) seed methanolic extract and its fractions in animal model. Sokoto J. Vet. Sci., 20(Special): 1-14 DOI: 10.4314/sokjvs.v20i5.1
- Olatoye, O. and Ogunsemoyin, O. (2016). Prevalence and antibiotics resistance of Campylobacterjejuni in retail chickens in Oyo State, Nigeria. Food Sci. Quality Mgt., 48: 7-11 https://api.semanticscholar.org/CorpusID:55792086
- Sakarikou, C., Kostoglou, D., Simões, M., and Giaouris, E. (2020). Exploitation of plant extracts and phytochemicals against resistant Salmonella spp. in biofilms. Food Res. Int., 128: 108806 DOI: 10.1016/j.foodres.2019.108806
- Salihu, M. D., Junaidu, A. U., Magaji, A. A. and Yakubu, A. S. (2012). Prevalence and antimicrobial resistance of thermophilic Campylobacter isolates from commercial broiler flocks in Sokoto, Nigeria. Res. J. Vet. Sci., 5(2): 51-58. DOI: 10.3923/RJVS.2012.51.58
- Souto, M. S. M., Coura, F. M., Dorneles, E. M., Stynen, A. P., Alves, T. M., Santana, J. A., Pauletti, R. B., Guedes, R. M., Viott, A. M, Heinemann, M. B. and Lage, A. P. (2017). Antimicrobial susceptibility and phylotyping profile of pathogenic Escherichiacoli and Salmonellaenterica isolates from calves and pigs in Minas Gerais, Brazil. Trop. Anim. Health Prod., 49(1): 13–23 DOI: 10.1007/s11250-016-1152-0
- Usmael, B., Abraha, B., Alemu, S., Mummed, B., Hiko, A. and Abdurehman, A. (2022). Isolation, antimicrobial susceptibility patterns, and risk factors assessment of non-typhoidal Salmonella from apparently healthy and diarrheic dogs. BMC Vet. Res. 18(1): 37 DOI: 10.1186/s12917-021-03135-x
- Winfield, M. D. and Groisman, E. A. (2003). Role of nonhost environments in the lifestyles of Salmonella and Escherichiacoli. Appl. Environ. Microbiol., 69(7): 3687–3694 DOI: 10.1128/AEM.69.7.3687-3694.2003
- Wong, G. C. L., Antani, J. D., Lele, P. P., Chen, J., Nan, B., Kuhn, M. J., Persat, A., Bru, J. L., Høyland-Kroghsbo, N. M. and Siryaporn, A. (2021). Roadmap on emerging concepts in the physical biology of bacterial biofilms: from surface sensing to community formation. Phys. Biol., 18(5): 051501. DOI: 10.1088/1478-3975/abdc0e
References
Abdi, R. D., Mengstie, F., Beyi, A. F., Beyene, T., Waktole, H., Mammo, B., Ayana, D. and Abunna, F. (2017). Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC Infec. Dis., 17(1): 352, DOI: 10.1186/s12879-017-2437-2
Abebe, E., Gugsa, G. and Ahmed, M. (2020). Review on major food-borne zoonotic bacterial pathogens. J. Trop. Med., 2020:4674235, DOI: 10.1155/2020/4674235
Adedeji, M. I. and Adetunji, V. O. (2020). Antibiofilm activities of ginger (Zingiberofficinale) on E. coli O157:H7 isolates from powdered milk in Ibadan, Nigeria. Res. J. Microbiol., 15(3): 90-97 DOI: 10.17311/jm.2020.90.97
Adegboye, M., Akinpelu, D. and Okoh, A. (2008). The bioactive and phytochemical properties of Garcinia kola (heckel) seed extract on some pathogens. Afr. J. Biotechnol. 7(21): 3934-3938 DOI: 10.4314/ajb.v7i21.59484
Amala, P. V., Sumithra, T. G., Reshma, K. J., Anusree, V. N., Sayooj, P. and Vijayagopal, P. (2021). Revisiting Substrate Specificity Concept in Microbial Screening Methodologies for Fish Waste Management. Turk. J. Fish. Aquat. Sci. 21(7): 323-332. 2 DOI: 10.4194/1303-2712-v21_7_02
Amaral, V. C. S., Santos, P. R., Fiori da Silva, A., Santos, A., MachinskiJunioir, M. and Mikcha, J. (2015). Effect of carvacrol and thymol on Salmonella spp. biofilms on polypropylene. Int. J. Food Sci. Tech., 50(12): 2639-2643 DOI: 10.1111/ijfs.12934
Clinical Laboratory Standard Institute (2020). M100 performance standards for antimicrobial susceptibility testing. 30th ed, Wayne, Pennsylvania, United States of America.
Ekene, E. and Earnest, O. E. (2014). Garciniakola: a review of its ethnomedicinal, chemical and pharmacological properties. Int. J. Curr. Res. Rev., 6(11): 1-7 https://api.semanticscholar.org/CorpusID:70639553
Eguale, T., Gebreyes, W., Asrat, D., Alemayehu, H., Gunn, J. S. and Engidawork, E. (2015). Non-typhoidal salmonella serotypes, antimicrobial resistance and coinfection with parasites among patients with diarrhea and other gastrointestinal complaints in Addis Ababa, Ethiopia. BMC Infect Dis., 15:497. DOI: 10.1186/s12879-015-1235-y
Ejo, M., Garedew, L., Alebachew, Z. and Worku, W. (2016). Prevalence and antimicrobial resistance of Salmonella isolated from animal-origin food items in Gondar, Ethiopia. BiomedRes. Int., 2016:4290506 DOI: 10.1155/2016/4290506
Fatope, M. O., Ibrahim, H. and Takeda, Y. (1993). Screening of higher plants reputed as pesticides using the brine shrimp lethality assay.Int. J. Pharmacol., 31(4): 250-254 DOI: https://doi.org/10.3109/13880209309082949
Feasey, N. A., Dougan, G., Kingsley, R. A., Heyderman, R. S. and Gordon, M. A. (2012). Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 379(9835): 2489–2499 DOI: 10.1016/S0140-6736(11)61752-2
Hakimi, A, R., Ghorban, K. and Dadmanesh, M. (2020). Combined effects of Alliumsativum and Cuminumcyminum essential oils on planktonic and biofilm forms of Salmonella typhimurium isolates. 3 Biotech., 10(7): 315 DOI: 10.1007/s13205-020-02286-2
Fàbrega, A. and Vila, J. (2013). Salmonellaenterica serovar typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev., 26(2): 308–341. DOI: 10.1128/CMR.00066-12.
Fan, Q., He, Q., Zhang, T., Song, W., Sheng, Q., Yuan, Y. and Yue, T. (2022). Antibiofilm potential of lactobionic acid against Salmonellatyphimurium. LWT Food Sci. Technol., 162: 0023-6438 DOI: 10.1016/j.lwt.2022.113461
FAO. (2021). Action Plan on Antimicrobial Resistance 2021–2025. FAO. DOI: 10.4060/cb5545en [Accessed 11th August 2023]
FAO. (2022). Antimicrobial Resistance. FAO of the United Nations. Available at: https://www.fao.org/one-health/overview/antimicrobial-resistance/en [Accessed 11th August 2023]
Hemmati, F., Rezaee, M. A., Ebrahimzadeh, S., Yousefi, L., Nouri, R., Kafil, H. S. and Gholizadeh, P. (2021). Novel strategies to combat bacterial biofilms. Mol. Biotechnol. 63(7): 569-586 DOI: 10.1007/s12033-021-00325-8
Hye-Jin, Seo. and Kang, S. S. (2020). Inhibitory effect of bacteriocin produced by Pediococcusacidilactici on the biofilm formation of Salmonellatyphimurium. Food Control. 117: 107361 DOI:10.1016/j.foodcont.2020.107361
Jaja, I. F., Bhembe, N. L., Green, E., Oguttu, J. and Muchenje, V. (2019). Molecular characterisation of antibiotic-resistant Salmonellaenterica isolates recovered from meat in South Africa. Acta Tropi., 190: 129–136 DOI: 10.1016/j.actatropica.2018.11.003
Jajere, S. M. (2019). A review of Salmonellaenterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet. World 12(4): 504–521. DOI: 10.14202/vetworld.2019.504-521
Keerthirathne, T. P., Ross, K., Fallowfield, H. and Whiley, H. (2022). Examination of Australian backyard poultry for Salmonella, Campylobacter and Shigella spp., and related risk factors. Zoonoses Public Health. 69(1): 13–22. DOI: 10.1111/zph.12889
Maier, B. (2021). How physical interactions shape bacterial biofilms. Annu. Rev. Biophys., 50(1): 401–417 DOI: 10.1146/annurev-biophys-062920-063646
Kiflu, B., Alemayehu, H., Abdurahaman, M., Negash, Y. and Eguale, T. (2017). Salmonella serotypes and their antimicrobial susceptibility in apparently healthy dogs in Addis Ababa Ethiopia. BMC Vet Res., 13(1): 1–9. DOI: 10.1186/s12917-017-1055-y
Marami, D., Hailu, K. and Tolera, M. (2018). Prevalence and antimicrobial susceptibility pattern of Salmonella and Shigella species among asymptomatic food handlers working in Haramaya University Cafeterias, Eastern Ethiopia. BMC Res. Notes 11(1): 74 DOI: 10.1186/s13104-018-3189-9
Morshdy, A. E. M. A., El-Tahlawy, A. S., Qari, S. H., Qumsani, A. T., Bay, D. H., Sami, R., Althubaiti, E. H., Mansour, A. M. A., Aljahani, A. H., Hafez, A. E. E., Mahmoud, A. F. A., El Bayomi, R. M. and Hussein, M. A. (2022). Anti-biofilms' activity of garlic and thyme essential oils against Salmonella Typhimurium. Molecules (Basel, Switzerland) 27(7): 2182 DOI: 10.3390/molecules27072182
Oboegbulem, S. I. and Okoronkwo, I. (1990). Salmonellae in the African great cane rat (Thryonomysswinderianus). J. Wildl. Dis., 26(1): 119–121. DOI: 10.7589/0090-3558-26.1.119
Ogbor, O., Ajayi, A., Zautner, A. E. and Smith, S. I. (2019). Antibiotic Susceptibility profiles of Campylobactercoli isolated from poultry farms in Lagos Nigeria – a pilot study. Eur. J. Microbiol. Immunol., 9(2): 2–34. DOI: 10.1556/1886.2019.00007
Oludairo, O. O., Kwaga J.K.P., Dzikwi A.A. and Kabir J. (2013). The genus Salmonella, isolation and occurrence in wildlife. Int. J. Microbiol. Immunol. Res., 1(5): 047–052 http://hdl.handle.net/123456789/2849
Opara, M. N. (2010). Grasscutter: the haematology and major parasites. Res. J. Parasitol., 5(4): 214-223 https://scialert.net/abstract/?doi=jp.2010.214.223
Orum, T. G., Ishola, O. O. and Adebowale, O. O. (2022). Occurrence and antimicrobial susceptibility patterns of Salmonella species from poultry farms in Ibadan, Nigeria. Afr. J. Lab. Med., 11(1): 1606. DOI: 10.4102/ajlm.v11i1.1606
Okoronkwo, M.O., Suleiman, M.M., Chiezey, N., Udechukwu, C.C., Oyetunde, J.S. and Jolayemi, K.O. (2022). Anti-diarrhoeal effects of Garciniakola (heckel-holl) seed methanolic extract and its fractions in animal model. Sokoto J. Vet. Sci., 20(Special): 1-14 DOI: 10.4314/sokjvs.v20i5.1
Olatoye, O. and Ogunsemoyin, O. (2016). Prevalence and antibiotics resistance of Campylobacterjejuni in retail chickens in Oyo State, Nigeria. Food Sci. Quality Mgt., 48: 7-11 https://api.semanticscholar.org/CorpusID:55792086
Sakarikou, C., Kostoglou, D., Simões, M., and Giaouris, E. (2020). Exploitation of plant extracts and phytochemicals against resistant Salmonella spp. in biofilms. Food Res. Int., 128: 108806 DOI: 10.1016/j.foodres.2019.108806
Salihu, M. D., Junaidu, A. U., Magaji, A. A. and Yakubu, A. S. (2012). Prevalence and antimicrobial resistance of thermophilic Campylobacter isolates from commercial broiler flocks in Sokoto, Nigeria. Res. J. Vet. Sci., 5(2): 51-58. DOI: 10.3923/RJVS.2012.51.58
Souto, M. S. M., Coura, F. M., Dorneles, E. M., Stynen, A. P., Alves, T. M., Santana, J. A., Pauletti, R. B., Guedes, R. M., Viott, A. M, Heinemann, M. B. and Lage, A. P. (2017). Antimicrobial susceptibility and phylotyping profile of pathogenic Escherichiacoli and Salmonellaenterica isolates from calves and pigs in Minas Gerais, Brazil. Trop. Anim. Health Prod., 49(1): 13–23 DOI: 10.1007/s11250-016-1152-0
Usmael, B., Abraha, B., Alemu, S., Mummed, B., Hiko, A. and Abdurehman, A. (2022). Isolation, antimicrobial susceptibility patterns, and risk factors assessment of non-typhoidal Salmonella from apparently healthy and diarrheic dogs. BMC Vet. Res. 18(1): 37 DOI: 10.1186/s12917-021-03135-x
Winfield, M. D. and Groisman, E. A. (2003). Role of nonhost environments in the lifestyles of Salmonella and Escherichiacoli. Appl. Environ. Microbiol., 69(7): 3687–3694 DOI: 10.1128/AEM.69.7.3687-3694.2003
Wong, G. C. L., Antani, J. D., Lele, P. P., Chen, J., Nan, B., Kuhn, M. J., Persat, A., Bru, J. L., Høyland-Kroghsbo, N. M. and Siryaporn, A. (2021). Roadmap on emerging concepts in the physical biology of bacterial biofilms: from surface sensing to community formation. Phys. Biol., 18(5): 051501. DOI: 10.1088/1478-3975/abdc0e