Student or educator? Sign up with your school email and get 6 months of Pro free.
CoChat
Sign Up
Cited by 961

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Multiplex PCR: Optimization and Application in Diagnostic Virology

Open access
Elnifro, Elfath M., Ashshi, Ahmed M., Cooper, Robert J., Klapper, Paul E.·2000·Clinical Microbiology Reviews
DOI 10.1128/cmr.13.4.559
Open this paper in CoChat — free account

Abstract

SUMMARY: PCR has revolutionized the field of infectious disease diagnosis. To overcome the inherent disadvantage of cost and to improve the diagnostic capacity of the test, multiplex PCR, a variant of the test in which more than one target sequence is amplified using more than one pair of primers, has been developed. Multiplex PCRs to detect viral, bacterial, and/or other infectious agents in one reaction tube have been described. Early studies highlighted the obstacles that can jeopardize the production of sensitive and specific multiplex assays, but more recent studies have provided systematic protocols and technical improvements for simple test design. The most useful of these are the empirical choice of oligonucleotide primers and the use of hot start-based PCR methodology. These advances along with others to enhance sensitivity and specificity and to facilitate automation have resulted in the appearance of numerous publications regarding the application of multiplex PCR in the diagnosis of infectious agents, especially those which target viral nucleic acids. This article reviews the principles, optimization, and application of multiplex PCR for the detection of viruses of clinical and epidemiological importance.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1128/cmr.13.4.559

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Show all 1 references

Research works printed but not linked: 125

  1. Adleberg J. M. Wittwer C. Use of the polymerase chain reaction in the diagnosis of ocular disease. Curr. Opin. Ophthalmol. 6 1995 80 85 · DOI
  2. 10.1128/CDLI.5.2.219-224.1998 · DOI
  3. Beards G. Graham C. Pillay D. Investigation of vesicular rashes for HSV and HZV by PCR. J. Med. Virol. 54 1998 155 157 · DOI
  4. 10.3109/10409239109114071 · DOI
  5. 10.4269/ajtmh.1998.58.102 · DOI
  6. Bertram S. Hufert F. T. van Lunzen J. von Laer D. Coinfection of individual leukocytes with human cytomegalovirus and human immunodeficiency virus is a rare event in vivo. J. Med. Virol. 49 1996 283 288 · DOI
  7. 10.1086/515603 · DOI
  8. Birch D. E. Kolmodin L. Wong J. Zangenberg G. A. Zoccoli M. A. McKinney N. Young K. K. Y. Simplified hot start PCR. Nature 381 1996 445 446 · DOI · Paper page
  9. 10.1093/nar/25.16.3235 · DOI · Paper page
  10. 10.1128/JCM.37.2.283-289.1999 · DOI
  11. 10.1128/jcm.35.12.3192-3197.1997 · DOI
  12. 10.1016/S0166-0934(97)00035-9 · DOI
  13. Casas I. Pozo F. Trallero G. Echevarria J. M. Tenorio A. Viral diagnosis of neurological infection by RT multiplex PCR: a search for entero- and herpesviruses in a prospective study. J. Med. Virol. 57 1999 145 151 · DOI
  14. Cassinotti P. Siegl G. A nested-PCR assay for the simultaneous amplification of HSV-1, HSV-2, and HCMV genomes in patients with presumed herpetic CNS infection. J. Virol. Methods 71 1998 105 114 · DOI
  15. Cassinotti P. Mietz H. Siegl G. Suitability and clinical application of a multiplex nested PCR assay for the diagnosis of herpes simplex virus infections. J. Med. Virol. 50 1996 75 81 · doi:10.1002/(sici)1096-9071(199609)50:1<75::aid-jmv13>3.0.co;2-x
  16. Caudai C. Padula M. G. Bettini V. Valensin P. E. Detection of HCV and GBV-C/HGV infection by multiplex PCR in plasma samples of transfused subjects. J. Virol. Methods 70 1998 79 83 · DOI
  17. Cha R. S. Thilly W. G. Specificity, efficiency, and fidelity of PCR. PCR Methods Appl. 3 1993 S18 S29 · DOI · Paper page
  18. Chamberlain J. S. Chamberlain J. R. Optimization of multiplex PCRs The polymerase chain reaction. Mullis K. B. Ferre F. Gibbs R. A. 1994 38 46 Birkhauser Boston Mass · DOI
  19. Chamberlain J. S. Gibbs R. A. Ranier J. E. Nguyen P. N. Caskey C. T. Multiplex PCR for the diagnosis of Duchenne muscular dystrophy PCR protocols: a guide to methods and applications. Gelfand D. H. Innis M. A. Shinsky J. J. White T. J. 1989 272 281 Academic Press San Diego Calif · DOI · Paper page
  20. 10.1093/nar/16.23.11141 · DOI · Paper page
  21. Chou Q. Russel M. Birch D. E. Raymond J. Bloch W. Prevention of pre-PCR mis-priming and primer dimerization improves low-copy-number amplifications. Nucleic Acids Res. 11 1992 1717 1723 · DOI · Paper page
  22. Cinque P. Vago L. Marenzi R. Giudici B. Weber T. Corradini R. Ceresa D. Lazzarin A. Linde A. Herpes simplex virus infections of the central nervous system in human immunodeficiency virus-infected patients: clinical management by polymerase chain reaction assay of cerebrospinal fluid. Clin. Infect. Dis. 27 1998 303 309 · DOI
  23. Clavel C. Rihet S. Masure M. Chypre C. Boulanger J. C. Quereux C. Birembaut P. DNA-EIA to detect high and low risk HPV genotypes in cervical lesions with E6/E7 primer mediated multiplex PCR. J. Clin. Pathol. 51 1998 38 43 · DOI
  24. Della N. G. Molecular biology in ophthalmology: a review of principles and recent advances. Arch. Ophthalmol. 114 1996 457 463 · DOI
  25. Dieffenbach C. W. Lowe T. M. J. Dveksler G. S. General concepts for PCR primer design. PCR Methods Appl. 3 1993 S30 S37 · DOI · Paper page
  26. 10.1128/JCM.36.5.1388-1391.1998 · DOI
  27. Edwards M. C. Gibbs R. A. Multiplex PCR: advantages, development, and applications. PCR Methods Appl. 3 1994 S65 S75 · DOI · Paper page
  28. 10.1128/jcm.33.6.1442-1447.1995 · DOI
  29. 10.1128/jcm.35.8.2076-2082.1997 · DOI
  30. Elnifro E. M. Cooper R. J. Klapper P. E. Bailey A. S. Tullo A. B. Diagnosis of viral chlamydial keratoconjunctivitis: which laboratory test? Br. J. Ophthalmol. 83 1999 622 627 · DOI
  31. Emmanuel P. J. Polymerase chain reaction from bench to bedside. Applications for infectious disease. J. Fla. Med. Assoc. 80 1993 627 630
  32. Fan J. Henrickson K. J. Savatski L. L. Rapid simultaneous diagnosis of infections with respiratory syncytial viruses A and B, influenza viruses A and B, and human parainfluenza virus types 1, 2, and 3 by multiplex quantitative reverse transcription-polymerase chain reaction enzyme hybridization assay (Hexaplex). Clin. Infect. Dis. 26 1998 1397 1402 · DOI · Paper page
  33. Garcia L. Tercero J. C. Legido B. Ramos J. A. Alemany J. Sanz M. Rapid detection of Actinobacillus actinomycetemcomitans,Prevotella intermedia and Porphyromona gingivalis by multiplex PCR. J. Periodontal Res. 33 1998 59 64 · DOI
  34. 10.1016/S0166-0934(98)00101-3 · DOI
  35. 10.1128/JCM.37.1.1-7.1999 · DOI · Paper page
  36. Harmon K. M. Ransom G. M. Wesley I. V. Differentiation of Campylobacter jejuni and Campylobacter coli by polymerase chain reaction. Mol. Cell. Probes 11 1997 195 200 · DOI
  37. Harris E. Appropriate transfer of molecular technology. Asia Pacific Technol. Monitor 13 1996 29 33
  38. 10.1128/JCM.36.7.1989-1995.1998 · DOI
  39. Harrison T. J. The polymerase chain reaction—a time of transition from research to routine. J. Clin. Pathol. 51 1998 491 492 · DOI
  40. Hassan-Walker A. F. Cope A. V. Griffiths P. D. Emery V. C. Transcription of the human cytomegalovirus natural killer decoy gene, UL18, in vitro and in vivo. J. Gen. Virol. 79 1998 2113 2116 · DOI
  41. 10.1128/jcm.35.11.2854-2858.1997 · DOI
  42. 10.2144/97233rr01 · DOI · Paper page
  43. Hengen P. N. Optimizing multiplex and LA-PCR with betaine. Trends Biol. Sci. 22 1997 225 226 · DOI
  44. 10.1016/S0928-0197(96)00255-3 · DOI
  45. Hewlett I. K. Ruta M. Cristiano K. Hawthorne C. A. Epstein J. S. Co-amplification of multiple regions of the HIV-1 genome by the polymerase chain reaction: potential use in multiple diagnosis. Oncogene 4 1989 1149
  46. Hu K. O. Yu C. H. Lee S. Villamil F. G. Vierling J. M. Simultaneous detection of both hepatitis B virus DNA and hepatitis C virus RNA using a combined one-step polymerase chain reaction technique. Hepatology 21 1995 901 907
  47. Jackson J. B. Polymerase chain reaction in transfusion medicine. Transfusion 30 1990 51 · DOI
  48. Jackson R. Morris D. J. Cooper R. J. Bailey A. S. Klapper P. E. Cleator G. M. Multiplex polymerase chain reaction for adenovirus and herpes simplex virus in eye swabs. J. Virol. Methods 56 1996 41 48 · DOI
  49. 10.1016/S0166-0934(98)00086-X · DOI
  50. Jin L. Richards A. Brown D. W. G. Development of a dual target-PCR for detection and characterization of measles virus in clinical specimens. Mol. Cell. Probes 10 1996 191 200 · DOI
  51. 10.1128/AEM.64.5.1743-1749.1998 · DOI
  52. Kebelmann-Betzing C. Seeger K. Dragon S. Schmitt G. Moricke A. Schild T. A. Henze G. Beyermann B. Advantages of a new Taq DNA polymerase in multiplex PCR and time-release PCR. BioTechniques 24 1998 154 158 · DOI
  53. Klapper P. E. Jungkind D. L. Fenner T. Antinozzi R. Schirm J. Blanckmeister C. Multicenter international work flow study of an automated polymerase chain reaction instrument. Clin. Chem. 44 1998 1737 1739 · DOI
  54. 10.1038/339237a0 · DOI · Paper page
  55. Lazarus P. Caruana S. Typing of common human papilloma virus strains by multiplex PCR. Anal. Biochem. 243 1996 198 201 · DOI
  56. Linz U. Delling U. Rübsamen-Waigmann H. Systematic studies on parameters influencing the performance of the polymerase chain reaction. J. Clin. Chem. Clin. Biochem. 28 1990 5 13
  57. Livache T. Bazin H. Mathis G. Conducting polymers on microelectronic devices as tools for biological analyses. Clin. Chim. Acta 278 1998 171 176 · DOI
  58. Mahony J. B. Jang D. Chong S. Luinstra K. E. Sellors J. W. Tyndall M. Chernesky M. Detection of Chlamydia trachomatis,Neisseria gonorrhoeae,Ureaplasma urealyticum, and Mycoplasma genitalium in first-void urine specimens by multiplex polymerase chain reaction. Mol. Diagn. 2 1997 161 168 · DOI
  59. 10.1128/jcm.33.11.3049-3053.1995 · DOI
  60. Markoulatos P. Samara V. Siafakas N. Plakokefalos E. Spyrou N. Moncany M. L. Development of a quadriplex polymerase chain reaction for human cytomegalovirus detection. J. Clin. Lab. Anal. 13 1999 99 105 · DOI
  61. 10.1016/0166-0934(95)00019-Q · DOI
  62. 10.1128/JCM.37.4.950-953.1999 · DOI
  63. Mitrani-Rosenbaum S. Tsvieli R. Lavie O. Boldes R. Anteby E. Shimonovitch S. Lazarovitch T. Friedmann A. Simultaneous detection of three common sexually transmitted agents by polymerase chain reaction. Am. J. Obstet. Gynecol. 171 1994 784 790 · DOI
  64. Mitsuhashi M. Technical report: part 2. Basic requirements for designing optimal PCR primers. J. Clin. Lab. Anal. 10 1996 285 293 · doi:10.1002/(sici)1098-2825(1996)10:5<285::aid-jcla9>3.0.co;2-7
  65. Morse S. A. Trees D. L. Htun Y. Radebe F. Orle K. A. Dangor Y. Beck-Sague C. M. Schmid S. Fehler G. Weiss J. B. Ballard R. C. Comparison of clinical diagnosis and standard laboratory and molecular methods for the diagnosis of genital ulcer disease in Lesotho: association with human immunodeficiency virus infection. J. Infect. Dis. 175 1997 583 589 · DOI · Paper page
  66. Moschettini D. De Milito A. Catucci M. Marconi A. Rinina C. Bianchi-Bandinelli M. L. Valensin P. E. Detection of human herpesvirus 6 and 7 in heart transplant recipients by multiplex polymerase chain reaction method. Eur. J. Clin. Microbiol. Infect. Dis. 17 1998 117 119 · DOI
  67. 10.1093/nar/23.8.1411 · DOI · Paper page
  68. Myeroson D. Lingenfelter P. A. Gleaves C. A. Meyers J. D. Bowden R. A. Diagnosis of cytomegalovirus pneumonia by polymerase chain reaction with archived frozen lung tissue and bronchoalveolar lavage fluid. Am. J. Clin. Pathol. 100 1993 407 413 · DOI
  69. Nadin-Davis S. A. Huang W. Wandeler A. I. The design of strain-specific polymerase chain reaction for discrimination of the raccoon rabies virus strain from indigenous rabies viruses of Ontario. J. Virol. Methods 57 1996 1 14 · DOI
  70. Nedjar S. Mitchell F. Biswas R. Simultaneous amplification and detection of specific hepatitis B virus and hepatitis C virus genomic sequences in serum samples. J. Med. Virol. 42 1994 212 216 · DOI
  71. Nicodème P. Steyaert J. Selecting optimal oligonucleotide primers for multiplex PCR. Intelligent Syst. Mol. Biol. 51 1997 210 213
  72. 10.1128/jcm.34.1.49-54.1996 · DOI · Paper page
  73. 10.1128/JCM.36.11.3149-3154.1998 · DOI
  74. Pizzighella S. Pisoni G. Bevilacqua F. Vaona A. Simultaneous polymerase chain reaction detection and restriction typing for the diagnosis of human genital papillomavirus infection. J. Virol. Methods 55 1995 245 256 · DOI
  75. 10.1128/AEM.64.10.3724-3730.1998 · DOI · Paper page
  76. Pozo F. Tenorio A. Detection and typing of lymphotropic herpesviruses by multiplex polymerase chain reaction. J. Virol. Methods 79 1999 9 19 · DOI
  77. Pring-Akerblom P. Trijssenaar F. E. J. Adrian T. Hoyer H. Multiplex polymerase chain reaction for subgenus-specific detection of human adenovirus in clinical samples. J. Med. Virol. 58 1999 87 92 · doi:10.1002/(sici)1096-9071(199905)58:1<87::aid-jmv14>3.0.co;2-r
  78. 10.1101/gr.5.1.91 · DOI
  79. Rajeev B. Biswas J. Molecular biologic techniques in ophthalmic pathology. Indian J. Ophthalmol. 46 1998 3 13
  80. 10.1128/JCM.37.5.1352-1355.1999 · DOI
  81. 10.1128/jcm.35.3.691-696.1997 · DOI
  82. 10.1021/bi00052a019 · DOI · Paper page
  83. 10.1128/jcm.31.5.1095-1102.1993 · DOI
  84. Reubel G. H. Crabb B. S. Studdert M. J. Diagnosis of equine gammaherpesvirus 2 and 5 infections by polymerase chain reaction. Arch. Virol. 140 1995 1049 1060 · DOI
  85. Rithidech K. N. Dunn J. J. Gordon C. R. Combining multiplex and touchdown PCR to screen murine microsatellite polymorphisms. BioTechniques 23 1997 36 45 · DOI
  86. 10.1128/jcm.35.1.268-269.1997 · DOI
  87. Robertson J. M. Walsh-Weller J. An introduction to PCR primer design and optimisation of amplification reactions. Methods Mol. Biol. 98 1998 121 154
  88. Rochelle P. A. Leon R. D. Stewart M. H. Wolfe R. L. Comparison of primers and optimization of PCR conditions for detection of Cryptosporidium parvum and Giardia lamblia in water. J. Clin. Microbiol. 63 1997 106 114
  89. 10.1006/viro.1997.8990 · DOI
  90. Roux K. H. Optimization and troubleshooting in PCR. PCR Methods Appl. 4 1995 S185 S194 · DOI
  91. Ruano G. Brash D. E. Kidd K. K. PCR: the first few cycles. Amplifications 7 1991 1 4
  92. Sevall J. S. Detection of parvovirus B19 by dot-blot and polymerase chain reaction. Mol. Cell. Probes 4 1990 237 246 · DOI
  93. Sherlock J. Cirigliano V. Petrou M. Tutschek B. Adinolfi M. Assessment of diagnostic quantitative fluorescent multiplex polymerase chain reaction assays performed on single cells. Ann. Hum. Genet. 62 1998 9 23 · DOI
  94. Shuber A. P. Grondin V. J. Klinger K. W. A simplified procedure for developing multiplex PCRs. Genome Res. 5 1995 488 493 · DOI
  95. Shuber A. P. Skoletsky J. Stern R. Handelin B. L. Efficient 12-mutation testing in the CFTR gene: a general model for complex mutation analysis. Hum. Mol. Genet. 2 1993 153 158 · DOI
  96. Soler C. Allibert P. Chardonnet Y. Cros P. Mandrand B. Thivolet J. Detection of human papillomavirus types 6, 11, 16 and 18 in mucosal and cutaneous lesions by the multiplex polymerase chain reaction. J. Virol. Methods 35 1991 143 157 · DOI
  97. 10.1128/JCM.36.10.2990-2995.1998 · DOI · Paper page
  98. Sunzeri F. J. Lee T. H. Bronlee R. G. Busch M. P. Rapid simultaneous detection of multiple retroviral DNA sequences using the polymerase chain reaction and capillary DNA chromatography. Blood 77 1991 879 886 · DOI
  99. 10.1128/aem.62.2.625-630.1996 · DOI · Paper page
  100. Taylor G. R. Robinson P. The polymerase chain reaction: from functional genomics to high-school practical classes. Curr. Opin. Biotechnol. 9 1998 35 42 · DOI
  101. Tenorio A. Echevarria J. E. Casas I. Echevarria J. M. Tabares E. Detection and typing of human herpesviruses by multiplex polymerase chain reaction. J. Virol. Methods 44 1993 261 269 · DOI
  102. Vandenvelde C. Verstraete M. Van Beers D. Fast multiplex polymerase chain reaction on boiled clinical samples for rapid viral diagnosis. J. Virol. Methods 30 1990 215 227 · DOI
  103. Vangrysperre W. De Clercq K. Rapid and sensitive polymerase chain reaction based detection and typing of foot-and-mouth disease virus in clinical samples and cell culture isolates, combined with a simultaneous differentiation with other genomically and/or symptomatically related viruses. Arch. Virol. 141 1996 331 344 · DOI
  104. Vesy C. J. Greenson J. K. Papp A. C. Snyder P. J. Qualman S. J. Prior T. W. Evaluation of celiac disease biopsies for adenovirus 12 and using a multiplex polymerase chain reaction. Mod. Pathol. 6 1993 61 64
  105. 10.1073/pnas.96.11.6394 · DOI · Paper page
  106. 10.1002/(SICI)1098-2825(1996)10:6<312::AID-JCLA2>3.0.CO;2-8 · doi:10.1002/(sici)1098-2825(1996)10:6<312::aid-jcla2>3.0.co;2-8
  107. 10.1093/sysbio/43.2.250 · DOI · Paper page
  108. 10.1101/gr.1.4.241 · DOI · Paper page
  109. 10.1021/ac970642d · DOI · Paper page
  110. Wattel E. Mariotti M. Agis F. Gordien E. Prou O. Courouce A. M. Rouger P. Wain-Hobson S. Chen I. S. Lefrere J. J. Human T lymphotropic virus (HTLV) type I and II DNA amplification in HTLV-I/II-seropositive blood donors of the French West Indies. J. Infect. Dis. 165 1992 369 372 · DOI
  111. Williams J. F. Optimization strategies for the polymerase chain reaction. BioTechniques 7 1989 762 769
  112. 10.1128/aem.63.10.3741-3751.1997 · DOI · Paper page
  113. 10.1016/0166-0934(93)90138-H · DOI
  114. Winn-Deen E. S. Automation of molecular genetic methods. Part 2: DNA amplification techniques. J. Clin. Ligand Assay 19 1996 21 26
  115. 10.1128/jcm.31.5.1148-1154.1993 · DOI
  116. 10.1128/CMR.5.4.370 · DOI
  117. 10.1136/jcp.48.2.101 · DOI
  118. 10.1128/jcm.35.6.1579-1581.1997 · DOI · Paper page
  119. 10.1089/dna.1991.10.233 · DOI · Paper page
  120. 10.1016/0168-1702(91)90107-7 · DOI
  121. Yourno J. A method for nested PCR with single closed reaction tubes. PCR Methods Appl. 2 1992 60 65 · DOI
  122. Zheng P. S. Li S. R. Iwasaka T. Song J. Gui M. H. Sugimori H. Simultaneous detection by consensus multiplex PCR of high- and low-risk and other types of human papilloma virus in clinical samples. Gynecol. Oncol. 58 1995 179 183 · DOI
  123. Zimmermann K. Schogl D. Plaimauer B. Mannhalter J. W. Quantitative multiple competitive PCR of HIV-1 DNA in a single reaction tube. BioTechniques 21 1996 480 484 · DOI
  124. 10.1128/jcm.35.10.2623-2627.1997 · DOI
  125. 10.1128/JCM.36.6.1544-1548.1998 · DOI

Cited by

See all 961

Metadata

Authors
Elnifro, E. M., Ashshi, A. M., Cooper, R. J., & Klapper, P. E.
Venue
Clinical Microbiology Reviews
Publisher
American Society for Microbiology
Published
2000-10
Volume
13
Issue
4
Pages
559-570
ISSN
  • 0893-8512 (ISSN-L)
  • 1098-6618
DOI
10.1128/cmr.13.4.559
OpenAlex
W2137089963
Cited by
961
References
1
FWCI
2.48
Type
journal article
Language
en
Open access
green
Licence
journals.asm.org/non-commercial-tdm-license (tdm)

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

How to cite

Cite CoChat for the checks on this page, and the paper for its own findings.

This page
CoChat. (2026). Citation check: Multiplex PCR: Optimization and Application in Diagnostic Virology. https://app.cochat.ai/papers/10.1128/cmr.13.4.559
The paper
Elnifro, E. M., Ashshi, A. M., Cooper, R. J., & Klapper, P. E. (2000). Multiplex PCR: Optimization and Application in Diagnostic Virology. Clinical Microbiology Reviews. https://doi.org/10.1128/cmr.13.4.559

Data sources

Bibliographic data: Semantic Scholar, OpenAlex, Crossref.

Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).

Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.