Quantitative and Qualitative Evaluation of Microorganism Profile Identified in Bioburden Analysis in a Biopharmaceutical Facility in Brazil: Criteria for Classification and Management of Results

Josiane Machado Vieira Mattoso; Luciana Veloso da Costa; Bruna de Almeida do Vale; Cristhiane Falavina dos Reis; Joyce Modesto de Andrade; Lygia Maria Paulo da Silva Braga; Greice Maria Silva da Conceição; Paulo Borges Mathias Costa; Igor Barbosa da Silva; Letícia de Alencar Pereira Rodrigues; Jeancarlo Pereira dos Anjos; Marcelo Luiz Lima Brandão

doi:10.5731/pdajpst.2023.012883

References

1.↵
World Health Organization. Annex 3: WHO Good Manufacturing Practices for Pharmaceutical Products: Main Principles. WHO Technical Report Series 961; WHO: Geneva, 2011.
2.↵
U.S. Pharmacopeial Convention [1116]. Microbiological Control and Monitoring of Aseptic Processing Environments. USP 43–NF 38, USP: Rockville, MD, 2021.
3.↵
1. Eissa M. E.
Distribution of Bacterial Contamination in Non-Sterile Pharmaceutical Materials and Assessment of Its Risk to the Health of the Final Consumers Quantitatively. Beni-Suef Univ. J. Basic Appl. Sci. 2016, 5 (3), 217–230.
OpenUrl
4.↵
European Commission, EudraLex—The Rules Governing Medicinal Products in the European Union, Volume 4: Good Manufacturing Practice for Medicinal Products for Human and Veterinary Use, Annex 1 - Manufacture of Sterile Medicinal Products. European Commission: Brussels, 2022.
5.↵
1. Bain D.,
2. Hardy D.,
3. Bell B. L.,
4. Forng R.-Y.,
5. Knight M.,
6. Bawa A.,
7. Ramsey S.,
8. Arbesser-Rastburg C.,
9. Paul M.,
10. Ton C.,
11. Leira F.,
12. Roman C.,
13. McFarland K.,
14. Phillips D.,
15. Stuckey J.,
16. Bauer C.,
17. Calvo A. J.
Microbial Monitoring For Biological Drug Substance Manufacturing: An Industry Perspective. PDA J. Pharm. Sci. Technol. 2015, 69 (3), 451–460.
OpenUrl FREE Full Text
6.↵
1. Sandle T.
Improving Microbiological Assurance for Bioburden Tests. Eur. Pharm. Rev. 2016, 21 (3), 41–44.
OpenUrl
7.↵
1. Eissa M.
Bioburden Control in the Biopharmaceutical Industry. BioPharm Int. 2017, 30 (9), 24–27.
OpenUrl
8.↵
European Medicines Agency. Guideline on the Sterilisation of the Medicinal Product, Active Substance, Excipient and Primary Container. EMA/CHMP/CVMP/QWP/850374/2015, EMA: London, 2019.
9.↵
1. Tidswel E. C.,
2. Boone K.
Environmental and Personnel Monitoring Programs—A Risk-Based Case Study of Cutibacterium acnes. PDA J. Pharm. Sci. Technol. 2020, 74 (4), 408–422.
OpenUrl Abstract/FREE Full Text
10.↵
Agência Nacional de Vigilância Sanitária. Farmacopeia Brasileira, 6a Edição—Volume II: Produtos Biológicos. ANVISA: Brasíl, 2019.
11.↵
1. Parte A. C.,
2. Sardà Carbasse J.,
3. Meier-Kolthoff J. P.,
4. Reimer L. C.,
5. Göker M.
List of Prokaryotic Names with Standing in Nomenclature (LPSN) Moves to the DSMZ. Int. J. Syst. Evol. Microbiol. 2020, 70 (11), 5607–5612.
OpenUrl CrossRef PubMed
12.↵
1. Shukla A. A.,
2. Gottschalk U.
Single-Use Disposable Technologies for Biopharmaceutical Manufacturing. Trends Biotechnol. 2013, 31 (3), 147–154.
OpenUrl CrossRef PubMed
13.↵
1. Repetto R.,
2. Levy R.
PDA Single-Use Systems Cross-Organizational Workshop-Meeting Summary, May 14, 2014-PDA Global Headquarters, Bethesda, MD. PDA J. Pharm. Sci. Technol. 2015, 69 (2), 317–325.
OpenUrl Abstract/FREE Full Text
14.↵
1. Clontz L.
Microbial Limit and Bioburden Tests: Validation Approaches and Global Requirements, 2nd ed; CRC Press: Boca Raton, FL, 2009.
15.↵
1. Jimenez L.
Microbial Diversity in Pharmaceutical Product Recalls and Environments. PDA J. Pharm. Sci. Technol. 2007, 61 (5), 383–399.
OpenUrl Abstract/FREE Full Text
16.↵
1. Kremer T.,
2. Patel R.
Correlation between Environmental Monitoring and Product Bioburden. Biomed. Instrum. Technol. 2019, 53 (s2), 32–37.
OpenUrl PubMed
17.↵
1. da Costa L. V.,
2. de Miranda R. V. D S. L.,
3. Reis C. M. F. D.,
4. de Andrade J. M.,
5. Cruz F. V.,
6. Frazão A. M.,
7. Fonseca E. L. D.,
8. Ramos J. N.,
9. Brandão M. L. L.,
10. Vieira V. V.
MALDI-TOF MS Database Expansion for Identification of Bacillus and Related Genera Isolated from a Pharmaceutical Facility. J. Microbiol. Methods 2022, 203, 106625.
OpenUrl PubMed
18.↵
1. Stamatoski B.,
2. Ilievska M.,
3. Babunovska H.,
4. Sekulovski N.,
5. Panov S.
Optimized Genotyping Method for Identification of Bacterial Contaminants in Pharmaceutical Industry. Acta Pharm. 2016, 66 (2), 289–295.
OpenUrl PubMed
19.↵
1. Braga L. M. P. S.,
2. Reis C. M. F.,
3. Andrade J. M.,
4. Miranda R. V. S. L.,
5. Costa L. V.,
6. Moreira F. M.,
7. Maltoso J. M. V.,
8. Silva I. B.,
9. Santos H. A. M.,
10. Brandão M. L. L.
Misidentification of Curtobacterium, Leifsonia, Microbacterium, Pseudarthrobacter and Paenibacillus as Cronobacter spp. Isolated from a Pharmaceutical Industry, In Annals of The Symposium: Vaccines, Biopharmaceuticals, In Vitro Diagnosis, Management, Other Related Themes, Proceedings of the 6th International Symposium on Immunobiological, Rio de Janeiro, Brazil, May 3–5, 2022; Instituto de Tecnologia em Imunobiológicos: Rio de Janeiro, Brazil, 2022; p 95.
20.↵
1. Costa L. V. D.,
2. Miranda R. V. D S. L. D.,
3. Fonseca E. L. D.,
4. Gonçalves N. P.,
5. Reis C. M. F. D.,
6. Frazão A. M.,
7. Cruz F. V.,
8. Brandão M. L. L.,
9. Ramos J. N.,
10. Vieira V. V.
Assessment of VITEK^® 2, MALDI-TOF MS and Full Gene 16S rRNA Sequencing for Aerobic Endospore-Forming Bacteria Isolated from a Pharmaceutical Facility. J. Microbiol. Methods 2022, 194, 106419.
OpenUrl PubMed
21.↵
1. Moreira F. M.,
2. Lage R. V. S.,
3. Costa P. V.,
4. Reis C. M. F.,
5. Braga L. M. P. S.,
6. Nascimento L. G.,
7. Maltoso J. M. V.,
8. Silva I. B.,
9. Santos H. A. M.,
10. Brandão M. L. L.,
11. Costa L. V.
Identification of Filamentous Fungi in a Pharmaceutical Industry using Matrix-Assisted Laser Desorption Ionization - Time of Flight Mass Spectrometry (MALDI-TOF MS). Abstracts of 31st Congresso Brasileiro de Microbiologia, Online, October, 22–24 2021; Sociedade Brasileira de Microbiologia: São Paulo, Brazil, 2021.
22.↵
1. Watson S. W.,
2. Novitsky T. J.,
3. Quinby H. L.,
4. Valois F. W.
Determination of Bacterial Number and Biomass in the Marine Environment. Appl. Environ. Microbiol. 1977, 33 (4), 940–946.
OpenUrl Abstract/FREE Full Text
23.↵
1. McIntyre C. A.,
2. Reinin G.
Reduction in Endotoxin Levels After Performing the Prepare for Aseptic Sort Procedure on the BD FACSAria II Flow Cytometer; BD Biosciences Application Note; BD Biociences: San Jose, CA, 2019.
24.↵
1. Magalhães P. O.,
2. Lopes A. M.,
3. Mazzola P. G.,
4. Rangel-Yagui C.,
5. Penna T. C. V.,
6. Pessoa A. Jr.
Methods of Endotoxin Removal from Biological Preparations: A Review. J. Pharm. Pharm. Sci. 2007, 10 (3), 388–404.
OpenUrl PubMed
25.↵
1. Evenson M. L.,
2. Hinds M. W.,
3. Bernstein R. S.,
4. Bergdoll M. S.
Estimation of Human Dose of Staphylococcal Enterotoxin A from a Large Outbreak of Staphylococcal Food Poisoning Involving Chocolate Milk. Int. J. Food Microbiol. 1988, 7 (4), 311–316.
OpenUrl CrossRef PubMed
26.↵
1. Asao T.,
2. Kumeda Y.,
3. Kawai T.,
4. Shibata T.,
5. Oda H.,
6. Haruki K.,
7. Nakazawa H.,
8. Kozaki S.
An Extensive Outbreak of Staphylococcal Food Poisoning Due to Low-Fat Milk in Japan: Estimation of Enterotoxin A in the Incriminated Milk and Powdered Skim Milk. Epidemiol. Infect. 2003, 130 (1), 33–40.
OpenUrl CrossRef PubMed Web of Science
27.↵
1. Simar S. R.,
2. Hanson B. M.,
3. Arias C. A.
Techniques in Bacterial Strain Typing: Past, Present, and Future. Curr Opin Infect Dis 2021, 34 (4), 339–345.
OpenUrl CrossRef PubMed

In This Issue

Download PDF

Article Alerts

Email Article

Citation Tools

Cited By...

No citing articles found.

Google Scholar

More in this TOC Section

Show more Research

Keywords

[1] 1.↵
World Health Organization. Annex 3: WHO Good Manufacturing Practices for Pharmaceutical Products: Main Principles. WHO Technical Report Series 961; WHO: Geneva, 2011.

[2] 2.↵
U.S. Pharmacopeial Convention [1116]. Microbiological Control and Monitoring of Aseptic Processing Environments. USP 43–NF 38, USP: Rockville, MD, 2021.

[3] 3.↵
Eissa M. E.
Distribution of Bacterial Contamination in Non-Sterile Pharmaceutical Materials and Assessment of Its Risk to the Health of the Final Consumers Quantitatively. Beni-Suef Univ. J. Basic Appl. Sci. 2016, 5 (3), 217–230.
OpenUrl

[4] Eissa M. E.

[5] 4.↵
European Commission, EudraLex—The Rules Governing Medicinal Products in the European Union, Volume 4: Good Manufacturing Practice for Medicinal Products for Human and Veterinary Use, Annex 1 - Manufacture of Sterile Medicinal Products. European Commission: Brussels, 2022.

[6] 5.↵
Bain D.,
Hardy D.,
Bell B. L.,
Forng R.-Y.,
Knight M.,
Bawa A.,
Ramsey S.,
Arbesser-Rastburg C.,
Paul M.,
Ton C.,
Leira F.,
Roman C.,
McFarland K.,
Phillips D.,
Stuckey J.,
Bauer C.,
Calvo A. J.
Microbial Monitoring For Biological Drug Substance Manufacturing: An Industry Perspective. PDA J. Pharm. Sci. Technol. 2015, 69 (3), 451–460.
OpenUrl FREE Full Text

[7] Bain D.,

[8] Hardy D.,

[9] Bell B. L.,

[10] Forng R.-Y.,

[11] Knight M.,

[12] Bawa A.,

[13] Ramsey S.,

[14] Arbesser-Rastburg C.,

[15] Paul M.,

[16] Ton C.,

[17] Leira F.,

[18] Roman C.,

[19] McFarland K.,

[20] Phillips D.,

[21] Stuckey J.,

[22] Bauer C.,

[23] Calvo A. J.

[24] 6.↵
Sandle T.
Improving Microbiological Assurance for Bioburden Tests. Eur. Pharm. Rev. 2016, 21 (3), 41–44.
OpenUrl

[25] Sandle T.

[26] 7.↵
Eissa M.
Bioburden Control in the Biopharmaceutical Industry. BioPharm Int. 2017, 30 (9), 24–27.
OpenUrl

[27] Eissa M.

[28] 8.↵
European Medicines Agency. Guideline on the Sterilisation of the Medicinal Product, Active Substance, Excipient and Primary Container. EMA/CHMP/CVMP/QWP/850374/2015, EMA: London, 2019.

[29] 9.↵
Tidswel E. C.,
Boone K.
Environmental and Personnel Monitoring Programs—A Risk-Based Case Study of Cutibacterium acnes. PDA J. Pharm. Sci. Technol. 2020, 74 (4), 408–422.
OpenUrl Abstract/FREE Full Text

[30] Tidswel E. C.,

[31] Boone K.

[32] 10.↵
Agência Nacional de Vigilância Sanitária. Farmacopeia Brasileira, 6a Edição—Volume II: Produtos Biológicos. ANVISA: Brasíl, 2019.

[33] 11.↵
Parte A. C.,
Sardà Carbasse J.,
Meier-Kolthoff J. P.,
Reimer L. C.,
Göker M.
List of Prokaryotic Names with Standing in Nomenclature (LPSN) Moves to the DSMZ. Int. J. Syst. Evol. Microbiol. 2020, 70 (11), 5607–5612.
OpenUrl CrossRef PubMed

[34] Parte A. C.,

[35] Sardà Carbasse J.,

[36] Meier-Kolthoff J. P.,

[37] Reimer L. C.,

[38] Göker M.

[39] 12.↵
Shukla A. A.,
Gottschalk U.
Single-Use Disposable Technologies for Biopharmaceutical Manufacturing. Trends Biotechnol. 2013, 31 (3), 147–154.
OpenUrl CrossRef PubMed

[40] Shukla A. A.,

[41] Gottschalk U.

[42] 13.↵
Repetto R.,
Levy R.
PDA Single-Use Systems Cross-Organizational Workshop-Meeting Summary, May 14, 2014-PDA Global Headquarters, Bethesda, MD. PDA J. Pharm. Sci. Technol. 2015, 69 (2), 317–325.
OpenUrl Abstract/FREE Full Text

[43] Repetto R.,

[44] Levy R.

[45] 14.↵
Clontz L.
Microbial Limit and Bioburden Tests: Validation Approaches and Global Requirements, 2nd ed; CRC Press: Boca Raton, FL, 2009.

[46] Clontz L.

[47] 15.↵
Jimenez L.
Microbial Diversity in Pharmaceutical Product Recalls and Environments. PDA J. Pharm. Sci. Technol. 2007, 61 (5), 383–399.
OpenUrl Abstract/FREE Full Text

[48] Jimenez L.

[49] 16.↵
Kremer T.,
Patel R.
Correlation between Environmental Monitoring and Product Bioburden. Biomed. Instrum. Technol. 2019, 53 (s2), 32–37.
OpenUrl PubMed

[50] Kremer T.,

[51] Patel R.

[52] 17.↵
da Costa L. V.,
de Miranda R. V. D S. L.,
Reis C. M. F. D.,
de Andrade J. M.,
Cruz F. V.,
Frazão A. M.,
Fonseca E. L. D.,
Ramos J. N.,
Brandão M. L. L.,
Vieira V. V.
MALDI-TOF MS Database Expansion for Identification of Bacillus and Related Genera Isolated from a Pharmaceutical Facility. J. Microbiol. Methods 2022, 203, 106625.
OpenUrl PubMed

[53] da Costa L. V.,

[54] de Miranda R. V. D S. L.,

[55] Reis C. M. F. D.,

[56] de Andrade J. M.,

[57] Cruz F. V.,

[58] Frazão A. M.,

[59] Fonseca E. L. D.,

[60] Ramos J. N.,

[61] Brandão M. L. L.,

[62] Vieira V. V.

[63] 18.↵
Stamatoski B.,
Ilievska M.,
Babunovska H.,
Sekulovski N.,
Panov S.
Optimized Genotyping Method for Identification of Bacterial Contaminants in Pharmaceutical Industry. Acta Pharm. 2016, 66 (2), 289–295.
OpenUrl PubMed

[64] Stamatoski B.,

[65] Ilievska M.,

[66] Babunovska H.,

[67] Sekulovski N.,

[68] Panov S.

[69] 19.↵
Braga L. M. P. S.,
Reis C. M. F.,
Andrade J. M.,
Miranda R. V. S. L.,
Costa L. V.,
Moreira F. M.,
Maltoso J. M. V.,
Silva I. B.,
Santos H. A. M.,
Brandão M. L. L.
Misidentification of Curtobacterium, Leifsonia, Microbacterium, Pseudarthrobacter and Paenibacillus as Cronobacter spp. Isolated from a Pharmaceutical Industry, In Annals of The Symposium: Vaccines, Biopharmaceuticals, In Vitro Diagnosis, Management, Other Related Themes, Proceedings of the 6th International Symposium on Immunobiological, Rio de Janeiro, Brazil, May 3–5, 2022; Instituto de Tecnologia em Imunobiológicos: Rio de Janeiro, Brazil, 2022; p 95.

[70] Braga L. M. P. S.,

[71] Reis C. M. F.,

[72] Andrade J. M.,

[73] Miranda R. V. S. L.,

[74] Costa L. V.,

[75] Moreira F. M.,

[76] Maltoso J. M. V.,

[77] Silva I. B.,

[78] Santos H. A. M.,

[79] Brandão M. L. L.

[80] 20.↵
Costa L. V. D.,
Miranda R. V. D S. L. D.,
Fonseca E. L. D.,
Gonçalves N. P.,
Reis C. M. F. D.,
Frazão A. M.,
Cruz F. V.,
Brandão M. L. L.,
Ramos J. N.,
Vieira V. V.
Assessment of VITEK^® 2, MALDI-TOF MS and Full Gene 16S rRNA Sequencing for Aerobic Endospore-Forming Bacteria Isolated from a Pharmaceutical Facility. J. Microbiol. Methods 2022, 194, 106419.
OpenUrl PubMed

[81] Costa L. V. D.,

[82] Miranda R. V. D S. L. D.,

[83] Fonseca E. L. D.,

[84] Gonçalves N. P.,

[85] Reis C. M. F. D.,

[86] Frazão A. M.,

[87] Cruz F. V.,

[88] Brandão M. L. L.,

[89] Ramos J. N.,

[90] Vieira V. V.

[91] 21.↵
Moreira F. M.,
Lage R. V. S.,
Costa P. V.,
Reis C. M. F.,
Braga L. M. P. S.,
Nascimento L. G.,
Maltoso J. M. V.,
Silva I. B.,
Santos H. A. M.,
Brandão M. L. L.,
Costa L. V.
Identification of Filamentous Fungi in a Pharmaceutical Industry using Matrix-Assisted Laser Desorption Ionization - Time of Flight Mass Spectrometry (MALDI-TOF MS). Abstracts of 31st Congresso Brasileiro de Microbiologia, Online, October, 22–24 2021; Sociedade Brasileira de Microbiologia: São Paulo, Brazil, 2021.

[92] Moreira F. M.,

[93] Lage R. V. S.,

[94] Costa P. V.,

[95] Reis C. M. F.,

[96] Braga L. M. P. S.,

[97] Nascimento L. G.,

[98] Maltoso J. M. V.,

[99] Silva I. B.,

[100] Santos H. A. M.,

[101] Brandão M. L. L.,

[102] Costa L. V.

[103] 22.↵
Watson S. W.,
Novitsky T. J.,
Quinby H. L.,
Valois F. W.
Determination of Bacterial Number and Biomass in the Marine Environment. Appl. Environ. Microbiol. 1977, 33 (4), 940–946.
OpenUrl Abstract/FREE Full Text

[104] Watson S. W.,

[105] Novitsky T. J.,

[106] Quinby H. L.,

[107] Valois F. W.

[108] 23.↵
McIntyre C. A.,
Reinin G.
Reduction in Endotoxin Levels After Performing the Prepare for Aseptic Sort Procedure on the BD FACSAria II Flow Cytometer; BD Biosciences Application Note; BD Biociences: San Jose, CA, 2019.

[109] McIntyre C. A.,

[110] Reinin G.

[111] 24.↵
Magalhães P. O.,
Lopes A. M.,
Mazzola P. G.,
Rangel-Yagui C.,
Penna T. C. V.,
Pessoa A. Jr.
Methods of Endotoxin Removal from Biological Preparations: A Review. J. Pharm. Pharm. Sci. 2007, 10 (3), 388–404.
OpenUrl PubMed

[112] Magalhães P. O.,

[113] Lopes A. M.,

[114] Mazzola P. G.,

[115] Rangel-Yagui C.,

[116] Penna T. C. V.,

[117] Pessoa A. Jr.

[118] 25.↵
Evenson M. L.,
Hinds M. W.,
Bernstein R. S.,
Bergdoll M. S.
Estimation of Human Dose of Staphylococcal Enterotoxin A from a Large Outbreak of Staphylococcal Food Poisoning Involving Chocolate Milk. Int. J. Food Microbiol. 1988, 7 (4), 311–316.
OpenUrl CrossRef PubMed

[119] Evenson M. L.,

[120] Hinds M. W.,

[121] Bernstein R. S.,

[122] Bergdoll M. S.

[123] 26.↵
Asao T.,
Kumeda Y.,
Kawai T.,
Shibata T.,
Oda H.,
Haruki K.,
Nakazawa H.,
Kozaki S.
An Extensive Outbreak of Staphylococcal Food Poisoning Due to Low-Fat Milk in Japan: Estimation of Enterotoxin A in the Incriminated Milk and Powdered Skim Milk. Epidemiol. Infect. 2003, 130 (1), 33–40.
OpenUrl CrossRef PubMed Web of Science

[124] Asao T.,

[125] Kumeda Y.,

[126] Kawai T.,

[127] Shibata T.,

[128] Oda H.,

[129] Haruki K.,

[130] Nakazawa H.,

[131] Kozaki S.

[132] 27.↵
Simar S. R.,
Hanson B. M.,
Arias C. A.
Techniques in Bacterial Strain Typing: Past, Present, and Future. Curr Opin Infect Dis 2021, 34 (4), 339–345.
OpenUrl CrossRef PubMed

[133] Simar S. R.,

[134] Hanson B. M.,

[135] Arias C. A.

Main menu

User menu

Search

Quantitative and Qualitative Evaluation of Microorganism Profile Identified in Bioburden Analysis in a Biopharmaceutical Facility in Brazil: Criteria for Classification and Management of Results

References

In This Issue

Citation Manager Formats

Related Articles

Cited By...

More in this TOC Section

Similar Articles

Keywords

Readers

Author/Reviewer Information

Parenteral Drug Association, Inc.

Main menu

User menu

Search

Quantitative and Qualitative Evaluation of Microorganism Profile Identified in Bioburden Analysis in a Biopharmaceutical Facility in Brazil: Criteria for Classification and Management of Results

References

In This Issue

Citation Manager Formats

Jump to section

Related Articles

Cited By...

More in this TOC Section

Similar Articles

Keywords

Readers

Author/Reviewer Information

Parenteral Drug Association, Inc.