Safety and immunogenicity study of Multiclade HIV-1 adenoviral vector vaccine alone or as boost following a multiclade HIV-1 DNA vaccine in Africa
We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same H...
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| Published in | PloS one Vol. 5; no. 9; p. e12873 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
21.09.2010
Public Library of Science (PLoS) |
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| Abstract | We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults.
Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1×10(10) or 1×10(11) particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-γ) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-γ ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone.
The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints.
ClinicalTrials.gov NCT00124007. |
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| AbstractList | Background We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults. Methodology/Principal Findings Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1x10.sup.10 or 1x10.sup.11 particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-[gamma]) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-[gamma] ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone. Conclusions/Significance The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints. Trial Registration ClinicalTrials.gov NCT00124007 We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults. Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1x10.sup.10 or 1x10.sup.11 particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-[gamma]) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-[gamma] ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone. The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints. BackgroundWe conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults.Methodology/principal findingsVolunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1×10(10) or 1×10(11) particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-γ) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-γ ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone.Conclusions/significanceThe HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints.Trial registrationClinicalTrials.gov NCT00124007. Background We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults. Methodology/Principal Findings Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1×1010 or 1×1011 particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-γ) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-γ ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone. Conclusions/Significance The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints. Trial Registration ClinicalTrials.gov NCT00124007 We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults. Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1×10(10) or 1×10(11) particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-γ) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-γ ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone. The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints. ClinicalTrials.gov NCT00124007. Background We conducted a double-blind, randomized, placebo-controlled Phase I study of a recombinant replication-defective adenovirus type 5 (rAd5) vector expressing HIV-1 Gag and Pol from subtype B and Env from subtypes A, B and C, given alone or as boost following a DNA plasmid vaccine expressing the same HIV-1 proteins plus Nef, in 114 healthy HIV-uninfected African adults. Methodology/Principal Findings Volunteers were randomized to 4 groups receiving the rAd5 vaccine intramuscularly at dosage levels of 1×1010 or 1×1011 particle units (PU) either alone or as boost following 3 injections of the DNA vaccine given at 4 mg/dose intramuscularly by needle-free injection using Biojector® 2000. Safety and immunogenicity were evaluated for 12 months. Both vaccines were well-tolerated. Overall, 62% and 86% of vaccine recipients in the rAd5 alone and DNA prime - rAd5 boost groups, respectively, responded to the HIV-1 proteins by an interferon-gamma (IFN-γ) ELISPOT. The frequency of immune responses was independent of rAd5 dosage levels. The highest frequency of responses after rAd5 alone was detected at 6 weeks; after DNA prime - rAd5 boost, at 6 months (end of study). At baseline, neutralizing antibodies against Ad5 were present in 81% of volunteers; the distribution was similar across the 4 groups. Pre-existing immunity to Ad5 did not appear to have a significant impact on reactogenicity or immune response rates to HIV antigens by IFN-γ ELISPOT. Binding antibodies against Env were detected in up to 100% recipients of DNA prime - rAd5 boost. One volunteer acquired HIV infection after the study ended, two years after receipt of rAd5 alone. Conclusions/Significance The HIV-1 rAd5 vaccine, either alone or as a boost following HIV-1 DNA vaccine, was well-tolerated and immunogenic in African adults. DNA priming increased the frequency and magnitude of cellular and humoral immune responses, but there was no effect of rAd5 dosage on immunogenicity endpoints. Trial Registration ClinicalTrials.gov NCT00124007 |
| Audience | Academic |
| Author | Muvunyi, Claude M Schmidt, Claudia Dally, Len Smith, Carol Than, Soe Allen, Susan Anzala, Omu Graham, Barney S Bwayo, Job Karita, Etienne Bergin, Philip J Bizimana, Jean Koup, Richard A Adams, Elizabeth M Fast, Patricia Jaoko, Walter Stevens, Gwynneth Thomson, Helen Boaz, Mark J Nabel, Gary J Omosa-Manyonyi, Gloria Farah, Bashir Cox, Josephine H Tarragona-Fiol, Tony Kayitenkore, Kayitesi Bailer, Robert T Loughran, Kelley Komaroff, Wendy Hayes, Peter Ho, Martin Gilmour, Jill |
| AuthorAffiliation | 5 Vaccine Clinical Research Branch (VCRB), Vaccine Research Program (VRP)/Division of AIDS (DAIDS)/National Institute of Allergy and Infectious Diseases (NIAID)/National Institutes of Health (NIH), Bethesda, Maryland, United States of America 7 The EMMES Corporation, Rockville, Maryland, United States of America 1 Kenya AIDS Vaccine Initiative (KAVI), Nairobi, Kenya 4 International AIDS Vaccine Initiative (IAVI), New York, New York, United States of America 3 Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America Queensland Institute of Medical Research, Australia 8 IAVI Human Immunology Laboratory, Imperial College, London, United Kingdom 2 Projet San Francisco (PSF), Rwanda-Zambia HIV Research Project, Kigali, Rwanda 6 Vaccine Research Center (VRC)/NIAID/NIH, Bethesda, Maryland, United States of America |
| AuthorAffiliation_xml | – name: 6 Vaccine Research Center (VRC)/NIAID/NIH, Bethesda, Maryland, United States of America – name: 2 Projet San Francisco (PSF), Rwanda-Zambia HIV Research Project, Kigali, Rwanda – name: 4 International AIDS Vaccine Initiative (IAVI), New York, New York, United States of America – name: 3 Rollins School of Public Health, Emory University, Atlanta, Georgia, United States of America – name: Queensland Institute of Medical Research, Australia – name: 1 Kenya AIDS Vaccine Initiative (KAVI), Nairobi, Kenya – name: 7 The EMMES Corporation, Rockville, Maryland, United States of America – name: 5 Vaccine Clinical Research Branch (VCRB), Vaccine Research Program (VRP)/Division of AIDS (DAIDS)/National Institute of Allergy and Infectious Diseases (NIAID)/National Institutes of Health (NIH), Bethesda, Maryland, United States of America – name: 8 IAVI Human Immunology Laboratory, Imperial College, London, United Kingdom |
| Author_xml | – sequence: 1 givenname: Walter surname: Jaoko fullname: Jaoko, Walter organization: Kenya AIDS Vaccine Initiative (KAVI), Nairobi, Kenya – sequence: 2 givenname: Etienne surname: Karita fullname: Karita, Etienne – sequence: 3 givenname: Kayitesi surname: Kayitenkore fullname: Kayitenkore, Kayitesi – sequence: 4 givenname: Gloria surname: Omosa-Manyonyi fullname: Omosa-Manyonyi, Gloria – sequence: 5 givenname: Susan surname: Allen fullname: Allen, Susan – sequence: 6 givenname: Soe surname: Than fullname: Than, Soe – sequence: 7 givenname: Elizabeth M surname: Adams fullname: Adams, Elizabeth M – sequence: 8 givenname: Barney S surname: Graham fullname: Graham, Barney S – sequence: 9 givenname: Richard A surname: Koup fullname: Koup, Richard A – sequence: 10 givenname: Robert T surname: Bailer fullname: Bailer, Robert T – sequence: 11 givenname: Carol surname: Smith fullname: Smith, Carol – sequence: 12 givenname: Len surname: Dally fullname: Dally, Len – sequence: 13 givenname: Bashir surname: Farah fullname: Farah, Bashir – sequence: 14 givenname: Omu surname: Anzala fullname: Anzala, Omu – sequence: 15 givenname: Claude M surname: Muvunyi fullname: Muvunyi, Claude M – sequence: 16 givenname: Jean surname: Bizimana fullname: Bizimana, Jean – sequence: 17 givenname: Tony surname: Tarragona-Fiol fullname: Tarragona-Fiol, Tony – sequence: 18 givenname: Philip J surname: Bergin fullname: Bergin, Philip J – sequence: 19 givenname: Peter surname: Hayes fullname: Hayes, Peter – sequence: 20 givenname: Martin surname: Ho fullname: Ho, Martin – sequence: 21 givenname: Kelley surname: Loughran fullname: Loughran, Kelley – sequence: 22 givenname: Wendy surname: Komaroff fullname: Komaroff, Wendy – sequence: 23 givenname: Gwynneth surname: Stevens fullname: Stevens, Gwynneth – sequence: 24 givenname: Helen surname: Thomson fullname: Thomson, Helen – sequence: 25 givenname: Mark J surname: Boaz fullname: Boaz, Mark J – sequence: 26 givenname: Josephine H surname: Cox fullname: Cox, Josephine H – sequence: 27 givenname: Claudia surname: Schmidt fullname: Schmidt, Claudia – sequence: 28 givenname: Jill surname: Gilmour fullname: Gilmour, Jill – sequence: 29 givenname: Gary J surname: Nabel fullname: Nabel, Gary J – sequence: 30 givenname: Patricia surname: Fast fullname: Fast, Patricia – sequence: 31 givenname: Job surname: Bwayo fullname: Bwayo, Job |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/20877623$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2010 Public Library of Science 2010. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2010 |
| Copyright_xml | – notice: COPYRIGHT 2010 Public Library of Science – notice: 2010. This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: This is an open-access article distributed under the terms of the Creative Commons Public Domain declaration which stipulates that, once placed in the public domain, this work may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. 2010 |
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| DOI | 10.1371/journal.pone.0012873 |
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| Discipline | Sciences (General) Public Health |
| DocumentTitleAlternate | Phase I HIV-Vaccine Study |
| EISSN | 1932-6203 |
| Editor | Doolan, Denise L. |
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| Notes | Current address: WHO-UNAIDS HIV Vaccine Initiative (HVI), Initiative for Vaccine Research (IVR), World Health Organization (WHO), Geneva, Switzerland Current address: Department of Clinical Biology, Faculty of Medicine, National University of Rwanda, Butare, Rwanda Conceived and designed the experiments: ST BSG JG GJN PF. Performed the experiments: WJ EK KK GSOM BF OA CMM JB TTF PJB PH GS JC. Analyzed the data: BSG RAK RTB CS LD MH MB JC JG PF. Contributed reagents/materials/analysis tools: RAK RTB JG GJN. Wrote the paper: BSG CS LD MB JC CS PF. Director of the Rwanda Zambia HIV Research Group: SAA. Medical monitoring: EA. Data manager: KL. Project Manager: WK. Director of African Laboratory Operations: GS. African Clinical Program Manager: HT. Principal Investigator at KAVI: JJB. Current address: Sanofi Pasteur, Swiftwater, Pennsylvania, United States of America Current address: Pfizer Inc., New York, New York, United States of America Current address: Division of Biostatistics, Office of Surveillance and Biometrics, Center for Devices and Radiological Health, Food and Drug Administration, Rockville, Maryland, United States of America |
| OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2943475/ |
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| SubjectTerms | Acquired immune deficiency syndrome Adenoviridae - genetics Adenoviridae - immunology Adenoviruses Adolescent Adult Adults AIDS AIDS vaccines AIDS Vaccines - adverse effects AIDS Vaccines - immunology Antibodies Antibodies, Viral - immunology Antigens Biological response modifiers Deoxyribonucleic acid DNA DNA vaccines Dosage Double-Blind Method Drug-Related Side Effects and Adverse Reactions Enzyme-linked immunosorbent assay Epidemiology gag Gene Products, Human Immunodeficiency Virus - adverse effects gag Gene Products, Human Immunodeficiency Virus - genetics gag Gene Products, Human Immunodeficiency Virus - immunology Genetic research Genetic Vectors - adverse effects Genetic Vectors - genetics Genetic Vectors - immunology Health aspects HIV HIV antigens HIV infections HIV Infections - immunology HIV Infections - prevention & control HIV Infections - virology HIV-1 - classification HIV-1 - genetics HIV-1 - immunology Human immunodeficiency virus Humans Immune response Immune response (humoral) Immune system Immunity Immunization, Secondary Immunogenicity Immunoglobulins Immunology Immunology/Immune Response Infections Infectious diseases Infectious Diseases/HIV Infection and AIDS Interferon Laboratories Lymphocytes Male Medical research Middle Aged Nef protein pol Gene Products, Human Immunodeficiency Virus - adverse effects pol Gene Products, Human Immunodeficiency Virus - genetics pol Gene Products, Human Immunodeficiency Virus - immunology Priming Proteins Public health Public Health and Epidemiology/Immunization Randomization Safety Safety and security measures Vaccines Vaccines, DNA - adverse effects Vaccines, DNA - immunology Young Adult γ-Interferon |
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| Title | Safety and immunogenicity study of Multiclade HIV-1 adenoviral vector vaccine alone or as boost following a multiclade HIV-1 DNA vaccine in Africa |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/20877623 https://www.proquest.com/docview/1292356360 https://pubmed.ncbi.nlm.nih.gov/PMC2943475 https://doaj.org/article/e14cd23e1bda4c33ac138fcbe3751b52 http://dx.doi.org/10.1371/journal.pone.0012873 |
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