Evaluation of rapid low-cost colorimetric methods for diagnosis of multidrug-resistant tuberculosis in limited-resource settings

I would like to express my immense gratitude to my advisor and mentor, Dr. Hassan Azzazy. I thank him not only for his support, knowledge opportunities, encouragement, and science he taught me, but most of all for teaching me how to think big and take on challenges effectively. I am privileged to be able to call myself his student, and for all that he taught me, I am forever in his debt. I would like to acknowledge the support and funding the Youssef Jameel Science and Technology Research Center (YJ-STRC) has provided me during the course of my enrollment in the Masters Program. I would like to thank Dr. Moustafa Abdel Fadeel and members of NAMRU-3 who have welcomed me into their facilities and spared no effort help me out, and provided me with the needed samples for this work. I have learnt a great deal from my time there and met people whom I will always value. I thank Dr. Momtaz Wasfy, and his TB laboratory members Mr. Bassem Abdel Rahman and Mr. Mohamed Abdel Maksoud. They have been more than helpful and have always been available to help me out despite their busy schedule.

[1]  P. Andersen,et al.  The success and failure of BCG — implications for a novel tuberculosis vaccine , 2005, Nature Reviews Microbiology.

[2]  J. Musser,et al.  Sequence-Based Identification ofMycobacterium Species Using the MicroSeq 500 16S rDNA Bacterial Identification System , 2000, Journal of Clinical Microbiology.

[3]  S. Cole,et al.  Differential Effects of Prior Exposure to Environmental Mycobacteria on Vaccination with Mycobacterium bovis BCG or a Recombinant BCG Strain Expressing RD1 Antigens , 2005, Infection and Immunity.

[4]  R. Cooksey,et al.  Molecular identification of mutations associated with anti-tuberculosis drug resistance among strains of Mycobacterium tuberculosis. , 2009, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[5]  M. Dimairo,et al.  Diagnostic accuracy of commercial urinary lipoarabinomannan detection in African tuberculosis suspects and patients. , 2009, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[6]  P. Vandamme,et al.  A new rapid and simple colorimetric method to detect pyrazinamide resistance in Mycobacterium tuberculosis using nicotinamide. , 2006, The Journal of antimicrobial chemotherapy.

[7]  F. Portaels,et al.  Multicenter study of MTT and resazurin assays for testing susceptibility to first-line anti-tuberculosis drugs. , 2005, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[8]  Hansjakob Furrer,et al.  Effect of Mutation and Genetic Background on Drug Resistance in Mycobacterium tuberculosis , 2012, Antimicrobial Agents and Chemotherapy.

[9]  T D McHugh,et al.  Prospective evaluation of BDProbeTec strand displacement amplification (SDA) system for diagnosis of tuberculosis in non-respiratory and respiratory samples. , 2004, Journal of medical microbiology.

[10]  R. Wilkinson,et al.  The clinical consequences of strain diversity in Mycobacterium tuberculosis. , 2008, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[11]  W. Lester Treatment of drug-resistant tuberculosis. , 1971, Disease-a-month : DM.

[12]  C. Leung,et al.  Management of multidrug‐resistant tuberculosis: Update 2007 , 2007, Respirology.

[13]  D. Spandidos,et al.  Molecular diagnostic tools in mycobacteriology. , 2008, Journal of microbiological methods.

[14]  S. Kaufmann,et al.  Mycobacterium tuberculosis: success through dormancy. , 2012, FEMS microbiology reviews.

[15]  M. Pai,et al.  Microscopic-observation drug susceptibility and thin layer agar assays for the detection of drug resistant tuberculosis: a systematic review and meta-analysis. , 2010, The Lancet. Infectious diseases.

[16]  M. Pai,et al.  Diagnosis of multidrug-resistant tuberculosis and extensively drug-resistant tuberculosis: Current standards and challenges. , 2008, The Canadian journal of infectious diseases & medical microbiology = Journal canadien des maladies infectieuses et de la microbiologie medicale.

[17]  Peter Eaton,et al.  Gold nanoparticles for the development of clinical diagnosis methods , 2008, Analytical and bioanalytical chemistry.

[18]  N. Pollock,et al.  Identification of Mycobacterium tuberculosis Ornithine Carboamyltransferase in Urine as a Possible Molecular Marker of Active Pulmonary Tuberculosis , 2008, Clinical and Vaccine Immunology.

[19]  D. Moore,et al.  Alternative methods of diagnosing drug resistance--what can they do for me? , 2011, The Journal of infectious diseases.

[20]  M. Drancourt,et al.  Diagnosis of pulmonary tuberculosis in a microbiological laboratory. , 2011, Medecine et maladies infectieuses.

[21]  Rosella Centis,et al.  INVITED REVIEW SERIES: TUBERCULOSIS , 2010 .

[22]  E. Stella,et al.  Comparison of the Performances of Two In-House Rapid Methods for Antitubercular Drug Susceptibility Testing , 2008, Antimicrobial Agents and Chemotherapy.

[23]  S. Franzblau,et al.  Rapid and simple MTT method for rifampicin and isoniazid susceptibility testing of Mycobacterium tuberculosis. , 2002, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[24]  L. Lindquist,et al.  Sputum concentration improves diagnosis of tuberculosis in a setting with a high prevalence of HIV. , 2000, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[25]  A. Aseffa,et al.  Evaluation of a direct colorimetric assay for rapid detection of rifampicin resistant Mycobacterium tuberculosis , 2005 .

[26]  N. Pollock,et al.  Identification and characterization of Mycobacterium tuberculosis antigens in urine of patients with active pulmonary tuberculosis: an innovative and alternative approach of antigen discovery of useful microbial molecules , 2008, Clinical and experimental immunology.

[27]  Anandi Martin,et al.  Rapid detection of rifampicin and isoniazid resistance in Mycobacterium tuberculosis by the direct thin-layer agar method. , 2008, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[28]  Pratibha Sharma,et al.  Evaluation of nitrate reduction assay, resazurin microtiter assay and microscopic observation drug susceptibility assay for first line antitubercular drug susceptibility testing of clinical isolates of M. tuberculosis. , 2012, Journal of microbiological methods.

[29]  J. O’Grady,et al.  New and improved diagnostics for detection of drug-resistant pulmonary tuberculosis , 2011, Current opinion in pulmonary medicine.

[30]  J. Caminero,et al.  Management of multidrug-resistant tuberculosis: an update , 2010, Therapeutic advances in respiratory disease.

[31]  D. Berg,et al.  Rapid, Efficient Detection and Drug Susceptibility Testing of Mycobacterium tuberculosis in Sputum by Microscopic Observation of Broth Cultures , 2000, Journal of Clinical Microbiology.

[32]  D. van Soolingen Molecular epidemiology of tuberculosis and other mycobacterial infections: main methodologies and achievements , 2001, Journal of internal medicine.

[33]  C. Griffiths,et al.  Diagnosis of active and latent tuberculosis: summary of NICE guidance , 2012, BMJ : British Medical Journal.

[34]  F. Portaels,et al.  Evaluation of the resazurin assay for the detection of multidrug-resistant Mycobacterium tuberculosis in Madagascar. , 2007, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[35]  F. Portaels,et al.  Thin-layer agar for detection of resistance to rifampicin, ofloxacin and kanamycin in Mycobacterium tuberculosis isolates. , 2009, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[36]  Evaluation of the Cobas TaqMan MTB Test for Direct Detection of Mycobacterium tuberculosis Complex in Respiratory Specimens , 2010, Journal of Clinical Microbiology.

[37]  Pedro Barquinha,et al.  Gold on paper-paper platform for Au-nanoprobe TB detection. , 2012, Lab on a chip.

[38]  A. R. Escombe,et al.  Microscopic-Observation Drug-Susceptibility Assay for the Diagnosis of TB , 2008 .

[39]  S. Kalantri,et al.  New tools and emerging technologies for the diagnosis of tuberculosis: Part II. Active tuberculosis and drug resistance , 2006, Expert review of molecular diagnostics.

[40]  F. Q. Falconi,et al.  Comparison of the VersaTREK system and Löwenstein-Jensen medium for the recovery of mycobacteria from clinical specimens , 2008, Scandinavian journal of infectious diseases.

[41]  A. Van Deun,et al.  Diagnosis of drug-resistant tuberculosis: reliability and rapidity of detection. , 2010, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[42]  E. Lemma,et al.  Evaluation of Microscopic Observation Drug Susceptibility Assay for Detection of Multidrug-Resistant Mycobacterium tuberculosis , 2007, Journal of Clinical Microbiology.

[43]  F. Portaels,et al.  Colorimetric redox-indicator methods for the rapid detection of multidrug resistance in Mycobacterium tuberculosis: a systematic review and meta-analysis. , 2007, The Journal of antimicrobial chemotherapy.

[44]  G. Roberts,et al.  Evaluation of Gen-Probe Amplified Mycobacterium Tuberculosis Direct Test by Using Respiratory and Nonrespiratory Specimens in a Tertiary Care Center Laboratory , 2002, Journal of Clinical Microbiology.

[45]  V. Lorian Bailey & Scott's Diagnostic Microbiology , 1990 .

[46]  F. Portaels,et al.  Rapid and Inexpensive Detection of Multidrug-Resistant Mycobacterium tuberculosis with the Nitrate Reductase Assay Using Liquid Medium and Direct Application to Sputum Samples , 2008, Journal of Clinical Microbiology.

[47]  A. Kilic Advances in the Diagnosis of Mycobacterium tuberculosis and Detection of Drug Resistance , 2013 .

[48]  Alimuddin Zumla,et al.  Urine for the diagnosis of tuberculosis: current approaches, clinical applicability, and new developments , 2010, Current opinion in pulmonary medicine.

[49]  T. Shinnick,et al.  Association of specific mutations in katG, rpoB, rpsL and rrs genes with spoligotypes of multidrug-resistant Mycobacterium tuberculosis isolates in Russia. , 2007, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[50]  M. Joloba,et al.  Direct Nitrate Reductase Assay versus Microscopic Observation Drug Susceptibility Test for Rapid Detection of MDR-TB in Uganda , 2011, PloS one.

[51]  Jacques Theron,et al.  Selection and Application of ssDNA Aptamers to Detect Active TB from Sputum Samples , 2012, PloS one.

[52]  P. Baptista,et al.  Gold-nanoparticle-probe-based assay for rapid and direct detection of Mycobacterium tuberculosis DNA in clinical samples. , 2006, Clinical chemistry.

[53]  R. Prasad,et al.  Multi-drug resistant tuberculosis: an iatrogenic problem. , 2010, Bioscience trends.

[54]  M. Joloba,et al.  Mycobacterium tuberculosis spoligotypes and drug susceptibility pattern of isolates from tuberculosis patients in peri-urban Kampala, Uganda , 2008, BMC infectious diseases.

[55]  B. Barrell,et al.  Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence , 1998, Nature.

[56]  Robert H. Gilman,et al.  Rapid, Low-Technology MIC Determination with Clinical Mycobacterium tuberculosis Isolates by Using the Microplate Alamar Blue Assay , 1998, Journal of Clinical Microbiology.

[57]  J. Palomino,et al.  Multicentre laboratory validation of the colorimetric redox indicator (CRI) assay for the rapid detection of extensively drug-resistant (XDR) Mycobacterium tuberculosis. , 2011, The Journal of antimicrobial chemotherapy.

[58]  M. Amicosante,et al.  Evaluation of the BDProbeTec strand displacement amplification assay in comparison with the AMTD II direct test for rapid diagnosis of tuberculosis. , 2004, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[59]  F. Portaels,et al.  The nitrate reductase assay for the rapid detection of isoniazid and rifampicin resistance in Mycobacterium tuberculosis: a systematic review and meta-analysis. , 2008, The Journal of antimicrobial chemotherapy.

[60]  F. Portaels,et al.  Resazurin Microtiter Assay Plate: Simple and Inexpensive Method for Detection of Drug Resistance in Mycobacterium tuberculosis , 2002, Antimicrobial Agents and Chemotherapy.

[61]  J. Palomino Molecular detection, identification and drug resistance detection in Mycobacterium tuberculosis. , 2009, FEMS immunology and medical microbiology.

[62]  M. Thakur,et al.  Global tuberculosis control report. , 2001, The National medical journal of India.

[63]  Tanya Parish,et al.  Mycobacteria Protocols , 2009, Methods in Molecular Biology.

[64]  J. O’Grady,et al.  Tuberculosis diagnostics and biomarkers: needs, challenges, recent advances, and opportunities. , 2012, The Journal of infectious diseases.

[65]  N. Kalyan,et al.  Rapid, inexpensive MIC determination of Mycobacterium tuberculosis isolates by using microplate nitrate reductase assay. , 2005, Diagnostic microbiology and infectious disease.

[66]  K. Steingart,et al.  Commercial Serological Antibody Detection Tests for the Diagnosis of Pulmonary Tuberculosis: A Systematic Review , 2007, PLoS medicine.

[67]  A. Fathy,et al.  Genotypic detection of rifampicin and isoniazid resistant Mycobacterium tuberculosis strains by DNA sequencing: a randomized trial , 2009, Annals of Clinical Microbiology and Antimicrobials.

[68]  A. Orcau,et al.  Characterization of mutations in streptomycin-resistant Mycobacterium tuberculosis clinical isolates in the area of Barcelona. , 2010, The Journal of antimicrobial chemotherapy.

[69]  M. Siedner,et al.  Inter- and Intra-Assay Reproducibility of Microplate Alamar Blue Assay Results for Isoniazid, Rifampicin, Ethambutol, Streptomycin, Ciprofloxacin, and Capreomycin Drug Susceptibility Testing of Mycobacterium tuberculosis , 2008, Journal of Clinical Microbiology.

[70]  Falk Hildebrand,et al.  Origin, Spread and Demography of the Mycobacterium tuberculosis Complex , 2008, PLoS pathogens.

[71]  F. Portaels,et al.  Rapid culture-based methods for drug-resistance detection in Mycobacterium tuberculosis. , 2008, Journal of microbiological methods.

[72]  R. Chaisson,et al.  Diagnostic Accuracy of a Urine Lipoarabinomannan Test for Tuberculosis in Hospitalized Patients in a High HIV Prevalence Setting , 2009, Journal of acquired immune deficiency syndromes.

[73]  M. Schoenfisch,et al.  Analytical chemistry of nitric oxide. , 2009, Annual review of analytical chemistry.

[74]  K. Carroll,et al.  of Tuberculosis in Low-Prevalence Settings Laboratory in Diagnosis and Management Role of the Clinical Mycobacteriology , 2011 .

[75]  S. Hoffner,et al.  Rapid and Inexpensive Drug Susceptibility Testing of Mycobacterium tuberculosis with a Nitrate Reductase Assay , 2002, Journal of Clinical Microbiology.

[76]  S. Cole,et al.  Mechanisms of drug resistance in Mycobacterium tuberculosis. , 1994, Immunobiology.

[77]  G. Sandhu,et al.  Tuberculosis: Current Situation, Challenges and Overview of its Control Programs in India , 2011, Journal of global infectious diseases.

[78]  G. Nataraj,et al.  Rapid antibiotic susceptibility testing of Mycobacterium tuberculosis: its utility in resource poor settings. , 2006, Indian journal of medical microbiology.

[80]  L. P. Ormerod Multidrug-resistant tuberculosis (MDR-TB): epidemiology, prevention and treatment. , 2005, British medical bulletin.

[81]  M. Joloba,et al.  Direct susceptibility testing for multi drug resistant tuberculosis: A meta-analysis , 2009, BMC infectious diseases.

[82]  J. Nkengasong,et al.  Laboratory Diagnosis of Tuberculosis in Resource-Poor Countries: Challenges and Opportunities , 2011, Clinical Microbiology Reviews.

[83]  R. Brosch,et al.  Pathogenicity in the tubercle bacillus: molecular and evolutionary determinants , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[84]  G. Cangelosi,et al.  Drug Resistance Assays for Mycobacterium tuberculosis , 2009 .

[85]  I. Khan,et al.  Microplate nitrate reductase assay versus Alamar Blue assay for MIC determination of Mycobacterium tuberculosis. , 2005, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[86]  Enrico Tortoli,et al.  Evaluation of INNO-LiPA MYCOBACTERIA v2: Improved Reverse Hybridization Multiple DNA Probe Assay for Mycobacterial Identification , 2003, Journal of Clinical Microbiology.

[87]  S. Abbott,et al.  16S rRNA Gene Sequencing for Bacterial Identification in the Diagnostic Laboratory: Pluses, Perils, and Pitfalls , 2007, Journal of Clinical Microbiology.

[88]  Zhong-yi Hu,et al.  Interferon-gamma release assays for the diagnosis of extrapulmonary tuberculosis: a systematic review and meta-analysis. , 2012, FEMS immunology and medical microbiology.

[89]  E. Böttger,et al.  Differentiation of Mycobacterium species by direct sequencing of amplified DNA. , 1990, Journal of general microbiology.

[90]  J. Palomino,et al.  Molecular basis and mechanisms of drug resistance in Mycobacterium tuberculosis: classical and new drugs. , 2011, The Journal of antimicrobial chemotherapy.

[91]  B. Bjorvatn,et al.  Rapid Colorimetric Method for Testing Susceptibility of Mycobacterium tuberculosis to Isoniazid and Rifampin in Liquid Cultures , 2003, Journal of Clinical Microbiology.

[92]  E. Böttger,et al.  Tuberculosis: drug resistance, fitness, and strategies for global control , 2008, European Journal of Pediatrics.

[93]  Zhi-ping Zhang,et al.  Multiplex Detection of Mutations in Clinical Isolates of Rifampin-Resistant Mycobacterium tuberculosis by Short Oligonucleotide Ligation Assay on DNA Chips , 2004, Journal of Clinical Microbiology.

[94]  Karin Weyer,et al.  Viewpoint TB diagnostics: what does the world really need? , 2011, The Journal of infectious diseases.

[95]  L. O’Connor Diagnostic Bacteriology Protocols , 2006, Methods in Molecular Biology™.

[96]  C. Saltini Chemotherapy and diagnosis of tuberculosis. , 2006, Respiratory medicine.

[97]  C. Spreadbury Mycobacteria, Molecular Biology and Virulence , 2001 .

[98]  P. Woo,et al.  Guidelines for interpretation of 16S rRNA gene sequence-based results for identification of medically important aerobic Gram-positive bacteria. , 2009, Journal of medical microbiology.

[99]  J. Palomino,et al.  Tuberculosis 2007; from basic science to patient care , 2007 .

[100]  F. Portaels,et al.  Rapid drug resistance detection in Mycobacterium tuberculosis: a review of colourimetric methods. , 2007, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[101]  Wilbert Bitter,et al.  Type VII secretion — mycobacteria show the way , 2007, Nature Reviews Microbiology.

[102]  G. Kahlmeter,et al.  Evaluation of wild-type MIC distributions as a tool for determination of clinical breakpoints for Mycobacterium tuberculosis. , 2009, The Journal of antimicrobial chemotherapy.

[103]  F. Portaels,et al.  Practical handbook for the phenotypic and genotypic identification of mycobacteria , 2004 .

[104]  H. McShane,et al.  Tuberculosis vaccines: progress and challenges. , 2011, Trends in pharmacological sciences.

[105]  B. Robertson,et al.  Mycobacterium tuberculosis Lineage Influences Innate Immune Response and Virulence and Is Associated with Distinct Cell Envelope Lipid Profiles , 2011, PloS one.

[106]  J. Palomino,et al.  Multicentre study of nitrate reductase assay for rapid detection of rifampicin-resistant M. tuberculosis. , 2009, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[107]  E. Böttger The ins and outs of Mycobacterium tuberculosis drug susceptibility testing. , 2011, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[108]  Suhail Ahmad,et al.  Recent advances in the diagnosis and treatment of multidrug-resistant tuberculosis. , 2009, Respiratory medicine.

[109]  M. Pai,et al.  Blinded evaluation of commercial urinary lipoarabinomannan for active tuberculosis: a pilot study. , 2009, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[110]  Y. Balabanova,et al.  Diagnosis of tuberculosis and drug resistance: what can new tools bring us? , 2012, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[111]  G. Kahlmeter,et al.  Challenging a dogma: antimicrobial susceptibility testing breakpoints for Mycobacterium tuberculosis. , 2012, Bulletin of the World Health Organization.

[112]  N. Smith,et al.  Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis , 2009, Nature Reviews Microbiology.

[113]  Nancy A Knechel Tuberculosis: pathophysiology, clinical features, and diagnosis. , 2009, Critical care nurse.

[114]  John W. Wilson,et al.  Update on the treatment of tuberculosis. , 2008, American family physician.

[115]  Z LEVNTAL,et al.  [History of tuberculosis]. , 1957, Medicinski glasnik.

[116]  M. Pai,et al.  Bacteriophage assays for rifampicin resistance detection in Mycobacterium tuberculosis: updated meta-analysis. , 2010, The international journal of tuberculosis and lung disease : the official journal of the International Union against Tuberculosis and Lung Disease.

[117]  D. Mitchison The diagnosis and therapy of tuberculosis during the past 100 years. , 2005, American journal of respiratory and critical care medicine.

[118]  S. Kalantri,et al.  New tools and emerging technologies for the diagnosis of tuberculosis: Part I. Latent tuberculosis , 2006, Expert review of molecular diagnostics.

[119]  Priscille Brodin,et al.  Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti , 2002, Molecular microbiology.

[120]  J. Sáez-Nieto,et al.  Molecular characterization of isoniazid-resistant Mycobacterium tuberculosis clinical strains isolated in the Philippines. , 2004, International journal of antimicrobial agents.

[121]  Zeinab H. Helal,et al.  Unexpectedly High Proportion of Ancestral Manu Genotype Mycobacterium tuberculosis Strains Cultured from Tuberculosis Patients in Egypt , 2009, Journal of Clinical Microbiology.

[122]  M. Perkins,et al.  Fluorescence versus conventional sputum smear microscopy for tuberculosis: a systematic review. , 2006, The Lancet. Infectious diseases.

[123]  D. Alland,et al.  A detailed analysis of 16S ribosomal RNA gene segments for the diagnosis of pathogenic bacteria. , 2007, Journal of microbiological methods.

[124]  B. Marston,et al.  Interferon-Gamma Release Assays for the Diagnosis of Latent Tuberculosis Infection in HIV-Infected Individuals: A Systematic Review and Meta-Analysis , 2011, Journal of acquired immune deficiency syndromes.

[125]  J. Palomino,et al.  Current developments and future perspectives for TB diagnostics. , 2012, Future microbiology.