Best Practices in the Management of Clostridioides difficile Infection in Developing Nations
Abstract
:1. Introduction
2. CDI in Developing Nations: Under-Recognized, Under-Measured
2.1. Current Epidemiology
2.1.1. Africa
2.1.2. Asia
2.1.3. Latin America
2.1.4. Europe
2.2. Limited Awareness
2.3. A High-Risk Environment: Aging Population, Inadequate Antibiotic Stewardship
3. Limited Diagnostic Capabilities
3.1. State of the Art in CDI Diagnostics
3.2. A Paucity of Clinical Microbiology Infrastructure
3.3. Unexpected Opportunities
4. Challenges of Treatment
4.1. Metronidazole, Always Available but No Longer SOC
4.2. Oral Vancomycin: Creative Solutions
4.3. Challenges to Fecal Microbiota Transplantation
4.4. Challenges to Introducing Newer Therapeutics: Monoclonal Antibodies, Newer Antibiotics, Bacteriophage
4.5. Opportunity: Enhanced Antimicrobial Stewardship
5. Key Facts
Author Contributions
Funding
Conflicts of Interest
Abbreviations/Acronyms
CDI | Clostridioides difficile infection |
rCDI | Recurrent Clostridioides difficile infection |
HA-CDI | Healthcare-associated CDI |
CA-CDI | Community-associated CDI |
GDH | Glutamate dehydrogenase |
EIA | Enzyme immunoassay |
PCR | Polymerase chain reaction |
NAAT | Nucleic acid amplification test |
SOC | Standard of care |
FMT | Fecal microbiota transplantation |
LBPs | Live biotherapeutics products |
ASPs | Antimicrobial Stewardship Programs |
Appendix A
Country | CDI Rate | CDI Diagnosis Tests | Population | Publication Year/Reference |
---|---|---|---|---|
ASIA | ||||
Bangladesh | 8.7% | GDH + Toxin A/B EIA (C. Diff Quik Chek Complete® assay) + Toxigenic culture | Adults 18 years with diarrhea (≥3 loose stools in a 24 h period) | 2020 [51] |
10% | Culture in CCFA + Toxin A/B latex agglutination (C. difficile Oxoid Latex Reagent) + Toxin A/B PCR | Adults 18 years with hospital-acquired diarrhea | 2018 [113] | |
Iran | 15.9%/15.5% a | Culture in CCFA + Gram stain + 16srDNA PCR + Toxin A/B PCR | Inpatients and outpatients with diarrhea | 2020 [53] |
21% | Toxin A/B EIA + Antigen EIA | Patient with hospital-acquired diarrhea (≥3 loose stools in a 24 h period occurring ≥48 h after admission) | 2015 [81] | |
6.1% | Culture in CCFA + API 20A system (bioMerieux, Marcy l’Etoile, France) | Patients with hospital-acquired diarrhea | 2009 [114] | |
5.3% | Toxin A/B EIA (Premier Toxin A/B, Generic Assays, Inc., Blankenfelde-Mahlow, Germany) | Patients with diarrhea | 2011 [59] | |
21% | Culture in CDMN agar (Oxoid) + Toxin A/B PCR | Aliquots of stool from hospitalized patients with diarrhea (≥3 watery/unformed/loose stools in ≥24 h) | 2012 [115] | |
India | 17% | Toxin A/B EIA (Ridascreen kit) | Inpatient and outpatients with diarrhea | 2011 [116] |
17.5% | Toxin A/B EIA | Hospitalized patients with diarrhea | 2014 [117] | |
62.5% b | Culture in CCFA + Toxin A/B latex agglutination | Hospitalized patients with diarrhea | 2012 [118] | |
15.7%/10.9% a (toxigenic strains) | Robertson’s cooked meat media + Toxin A/B PCR | Patient >2 years old with diarrhea developed after >72 h of admission. | 2015 [56] | |
4%/16% c | GDH + Toxin A/B (C. Diff Quik Chek Complete® assay) | Inpatients and outpatients with diarrhea and recent history of antibiotic exposure and/or antiulcer drug | 2017 [119] | |
25% | Toxin A/B latex agglutination | Stool samples of all-age-group patients | 2002 [120] | |
8.57% | Toxin A/B PCR (Cepheid Xpert™ C. difficile assay or Biofire FilmArray® Gastrointestinal Panel) | Stool samples of inpatients with diarrhea | 2023 [121] | |
Lao | 7.1%/4.2% d | Culture in Chrom ID C. difficile agar (bioMerieux, Marcy l’Etoile, France) + Toxin latex agglutination (Oxoid C. difficile latex test kit, United Kingdom) confirmed by toxin A/B PCR | Hospitalized patient with unformed stools | 2017 [54] |
Pakistan | 29.18% | Culture in CCFA | Hospitalized patient who developed diarrhea after ≥2 days of taking antibiotics with fecal leukocytosis. | 2012 [60] |
Philippines | 43.6% | Toxin A/B ELISA (TechLab®, Blacksburg, VA, USA) | Adult patients aged ≥18 years who were scheduled for colonoscopy or sigmoidoscopy | 2012 [122] |
Cambodia | 3.75% | Toxin A (Oxoid Toxin Detection kit) | HIV-positive adult patients with chronic diarrhea (>3 loose stools daily for ≥3 days) | 2006 [123] |
China | 9.54% | Culture + Toxin B (TechLab®, Blacksburg, VA, USA) | Adult patient with diarrhea | 2008 [124] |
12.58% | Culture in CCFA + Vitek® Anaerobe Identification Card (bioMérieux, Inc., Salt Lake City, UT, USA) + CCCNA culture followed by ribotype PCR | Stool sample of adult hospitalized patients | 2011 [125] | |
14.29% | Culture in CCFA + Vitek 2® Anaerobe Identification Card (bioMérieux, Marcy l’Etoile, France) + Toxin A/B PCR | Hospitalized patient aged > 18 years with diarrhea (≥3 watery/loose stools in ≥24 h) | 2018 [126] | |
30.58% | Culture in CCFA + RAPID ID 32 A (bioMérieux, Marcy l’Etoile, France) + Toxin A/B PCR (Cepheid Xpert™ C. difficile assay, Sunnyvale, CA, USA) | Hospitalized patient aged ≥ 18 years with diarrhea (≥3 watery/loose stools in ≥24 h) and antibiotic used ≥4 weeks prior to onset of diarrhea | 2014 [127] | |
Indonesia | 1.3% | Premier C. difficile toxin A EIA (Meridian Diagnostic Inc.) | Outpatients and inpatients with diarrhea | 2002 [128] |
25% | GDH + Toxin A/B (C. Diff Quik Chek Complete® assay) | Elderly hospitalized patient with hepatocellular carcinoma | 2014 [129] | |
14.7% | Culture on C. difficile selective agar (bioMerieux, Marcy l’Etoile, France) or chromogenic agar (CHROMagar) + MALDI-TOF mass spectrometry (Biotyper, Bruker Daltonics, Bremen, Germany) + Toxin A/B EIA + Toxin A/B PCR | Patients with diarrhea and without diarrhea (controls) | 2018 [130] | |
10.9% | GDH + Toxin A/B (C. Diff Quik Chek Complete® assay) followed by Culture + Toxin A/B PCR | Stool samples from patient with diarrhea | 2017 [131] | |
Jordan | 9.7% | Toxin A EIA (Culturette, Brand Toxin CD kit, Becton-Dickinson) + Culture on CCFA + API 20A system (bioMérieux, Marcy l’Etoile, France) | Hospitalized patients aged ≥ 2 years with diarrhea. | 2001 [132] |
19.2% | Culture on CCFA + Remel RapiID ANA II system + Toxin A/B PCR | Stool samples from hospitalized patients aged ≥ 40 years and admitted ≥3 days with or without diarrhea | 2009 [133] | |
Vietnam | 9% | Toxin A/B PCR + Multiplexed NAAT (TAG gastrointestinal pathogen assay, Luminex Molecular Diagnostics) | Stool samples from hospitalized patients admitted with diarrhea (≥3 watery/loose stools in ≥24 h) | 2016 [134] |
AFRICA | ||||
Egypt | 20.4% (Pediatric: 17.89%/Adult: 27%) | Culture in CCFA + Gram stain + API 20A system (bioMérieux, Marcy l’Etoile, France) + Toxin A/B EIA confirmed by Toxin A/B PCR | Adult and pediatric patients with antibiotic-associated diarrhea | 2020 [61] |
24% | Culture in Columbia blood agar + Toxin A/B EIA (Ridascreen kit) | Patients with antibiotic-associated diarrhea | 2007 [135] | |
13.7% | Culture on C. difficile agar (Oxoid) + C. difficile identification latex agglutination test (Oxoid) | Hospitalized patients with healthcare-associated diarrhea (>3 unformed stools for 24 h) | 2017 [136] | |
Côte d’Ivoire | 5.88% b | GDH (Clostridium K-SeT, Coris BioConcept) confirmed in CLO culture (BioMerieux, Marcy l’Etoile, France) with MALDI-TOF and toxin A/B PCR | Patients aged ≥1 year presenting with persistent diarrhea (≥2 weeks) and patients without any gastrointestinal symptoms | 2015 [137] |
Ghana | 4.5% | GDH + Toxin A/B (C. Diff Quik Chek Complete® assay) + Culture C. difficile agar base (Oxoid) confirmed by MALDI-TOF | Hospitalized patients with diarrhea | 2016 [138] |
Nigeria | 15% | Toxin A/B EIA (Inverness Medical Professional Diagnostics) | Hospitalized patients with >2 witnessed watery bowel movement for ≥48 h or outpatients with loose stools greater than twice their regular frequencies e | 2011 [57] |
2.6% | Toxin A/B EIA (Meridian Immunocard, Meridian Bioscience) | Hospitalized patients with diarrhea | 2016 [58] | |
Kenya | 33.8%/25.5% f | Culture in toxigenic culture confirmed by toxin A/B PCR and toxin A/B ELISA (TechLab®, Blacksburg, VA, USA) | Hospitalized patients aged ≤ 5 years presenting with diarrhea | 2019 [139] |
92.4%/90.5% f | Culture in toxigenic culture confirmed by toxin A/B PCR and toxin A/B EIA | Hospitalized patients with diarrhea | 2018 [14] | |
Malawi | 13.3% g | Toxin A/B ELISA (TechLab®, Blacksburg, VA, USA)) | Hospitalized patients with and without diarrhea (≥3 loose stools per day) | 2014 [140] |
Tanzania | 6.4%/2.8% h | Culture on chromogenic agar (CHROMagar, Paris, France) + GDH + Toxin A/B (C. Diff Quik Chek Complete® assay) confirmed by toxin A/B PCR | Patients with and without diarrhea | 2015 [141] |
Zambia | 10% | Culture on CCFA + C. difficile latex agglutination + Toxin A/B ELISA confirmed by tpi gene PCR | Stool samples of patients with acute or persistent diarrhea | 2020 [142] |
Zimbabwe | 8.6% | Culture in toxigenic culture + Toxin A/B EIA | Stool samples of outpatients with diarrhea | 2014 [143] |
Botswana | 4.2% | Multiplexed NAAT (TAG gastrointestinal pathogen assay, Luminex Molecular Diagnostics) | Hospitalized patients aged < 13 years presenting with diarrhea | 2016 [144] |
Algeria | 6.9% | Culture on CLO (bioMérieux, Marcy l’Etoile, France) with cefoxitin, cyclosporine, and sodium taurocholate + Gram stain + API 20A system (bioMérieux, Marcy l’Etoile, France) confirmed by toxin A/B multiplex PCR | Hospitalized patients with diarrhea after admission | 2018 [52] |
Cameroon | 27.3% | GDH + Toxin A/B EIA (C. Diff Quik Chek Complete® assay) | Inpatients and outpatients with diarrhea | 2020 [145] |
South Africa | 22% | Culture on chromogenic agar (CHROMagar, Paris, France) + Toxin A/B PCR | Patients aged >18 years with diarrhea | 2016 [146] |
13.7% | Toxin B PCR (GeneXpert C. difficile) confirmed by culture on CCEYA + Toxin A/B multiplex PCR | Stool samples of patients with diarrhea | 2016 [147] | |
44.8% | Toxin A/B PCR | Hospitalized patients aged >18 years with diarrhea | 2018 [148] | |
9.2% | Toxin A EIA | Hospitalized patients aged >18 years who developed diarrhea after admission | 2013 [149] | |
LATIN AMERICA | ||||
Brazil | 27.8% b | Culture in CCFA + Bacterial cytotoxicity on VERO tissue culture + Toxin A/B PCR | Stool samples of pediatric patients aged 0–5 years with and without diarrhea | 2003 [150] |
4.17% | Toxin B PCR (BD Diagnostics) and stool culture | Stool samples of hospitalized patients aged 18 years or older with hospital stay of at least 5 days | 2012 [151] | |
8% | Toxin A/B EIA (Premier Toxins A & B, Meridian Bioscience, Cincinnati, OH, USA) + Culture in CLO agar (bioMerieux, Marcy l’Etoile, France) and/or toxin B PCR | Hospitalized adults with diarrhea (≥3 loose stools over 24 h period) | 2014 [152] | |
5.41% | Toxin A/B ELISA (Ridascreen C. difficile Toxin A/B, R-Biopharm) OR Culture in CCFA + tpi PCR + Toxin A/B PCR | Stool samples of hospitalized patients with diarrhea | 2014 [153] | |
48% | Toxin A/B EIA (ProSpect C. difficile Toxin A/B Microplate Assay, Remel) + Culture in CCFA + RapID ANA II system (Remel) and tpi gene PCR | Stool samples of hospitalized cancer patients aged >18 years with diarrhea (≥3 liquid stools over 24 h period) | 2017 [154] | |
4.51%/8.49%/15% i | GDH + Toxin A/B EIA (C. Diff Quik Chek Complete® assay) + Toxin B PCR (Cepheid Xpert) | Stool samples of hospitalized patients | 2020 [155] | |
Mexico | 5.43% | Toxin A Vidas II EIA (BioMerieux, Durham, UK) | Stool samples from all patients tested for toxin A with exclusion of repetition | 2009 [156] |
48.2% | Toxin A/B EIA | Hospitalized patients with liquid stools for >12 h after 24 h of admission | 2018 [157] | |
20.7% | Toxin A/B EIA | Patients who developed diarrhea (>3 unformed stools in 24 h) during hospital stay or within three days after hospital discharge | 2019 [158] | |
96%/91.3% j | Toxin A/B EIA immunocard (Meridian Bioscience) OR Toxin A/B PCR (Cepheid Xpert) | Patients who developed diarrhea (≥3 loose stools in the preceding 24 h) | 2017 [80] | |
18.2% | Toxin A/B immunochromatography (CerTest kit) | Stool samples of inpatients or outpatients | 2021 [159] | |
Paraguay | 19.7% | Toxin A/B PCR | Stool samples of hospitalized patients | 2020 [22] |
Colombia | 13.8% | Toxin A/B ELISA OR toxin B/binary toxin PCR (GeneXpert) | Hospitalized patients aged >18 years with >3 liquid stools and no laxative used | 2017 [19] |
13.95% | Toxin A/B PCR (Cepheid Xpert) | Hospitalized patients with >3 decreased consistency stools for at least 48 h and received antibiotics for at least 48 h within 90 days prior to onset of diarrhea | 2017 [20] | |
9.7% | Toxin A/B EIA immunocard (Meridian Bioscience, Cincinnati, OH, USA) or MiniVidas (bioMerieux, Marcy l’Etoile, France) | Hospitalized patient with suspicion of CDI and received at least one dose of antibiotic within 6 weeks prior to onset of symptoms | 2017 [21] | |
Peru | 35.3% | Toxin A/B ELISA (Remel) | Hospitalized patient aged >14 years with diarrhea ≥72 h after admission. | 2007 [17] |
11.2% | GDH (Rida Quik C. difficile) + Toxin A/B EIA (RIDA SCREEN C. difficile A & B) arbitrated by toxin A/B PCR (Cepheid Xpert) | Hospitalized patients aged > 18 years with ≥3 unformed stools 48 h after admission and received antibiotics for at least 48 h within 90 days prior to onset of diarrhea | 2020 [18] | |
EUROPE | ||||
North Macedonia | 13.2% | GDH and toxin A/B detection by immunochromatographic detection | Stool samples received collected 2016–2020 from symptomatic patients | 2024 [23] |
Bulgaria | 3.3% | C. difficile antigen and toxin by immunochromatographic method | Hospitalized patients with acute diarrhea with ≥3 unformed stools per day | 2022 [26] |
Bosnia and Herzegovina | 35.08% | Toxin A/B ELISA | Hospitalized patients with clinical symptoms and signs suggested for CDI | 2013 [28] |
Continent/ Reference | Ribotypes (RT) |
---|---|
Africa [13] |
|
Europe [24,25] |
|
Asia [78,160] |
|
Latin America [16,21,161,162,163] |
|
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CDI | IDSA/SHEA | ESCMID a | South African Society of Clinical Microbiology b | Taiwan Guidelines | Mexican Consensus |
---|---|---|---|---|---|
Primary episode, non-severe | Preferred regimen: SOC c FDX | ||||
Alternative regimen: SOC c VAN | Preferred regimen: SOC c VAN | ||||
Alternative regimen: SOC c MET d | Preferred regimen: SOC MET | Alternative regimen: SOC MET d | |||
Primary episode, severe e | Preferred regimen: SOC FDX | ||||
Alternative regimen: SOC VAN | Preferred regimen: SOC VAN | Preferred regimen: VAN 125–250 mg qid for 14 days | |||
Oral administration not possible f: Rectal or nasoduodenal delivery +/− adjunctive IV MET 500 mg tid | Alternative regimen: TEC 200 mg bid for 10 days | ||||
First recurrence | SOC FDX OR FDX EPX g | SOC FDX (if primary episode was treated with VAN or MET) | SOC FDX (if VAN was used for primary episode) | SOC FDX (if VAN was used for primary episode in a patient without risk factors h) | |
Alternative regimen: VAN prolonged ta-pered and pulsed regimen i OR SOC VAN | SOC VAN OR SOC FDX + BEZ 10 mg/kg IV once (if primary episode treated with FDX) | SOC VAN (if MET was used for primary episode) | SOC VAN (if MET was used for primary episode in a patient without risk factors h) | SOC VAN (if MET was used for primary episode) | |
Adjunctive therapy: BEZ 10 mg/kg IV once after SOC | VAN prolonged tapered and pulsed regimen (if FDX or BEZ are unavailable) | VAN prolonged tapered and pulsed regimen (if standard VAN was used in primary episode) | TEC 100–200 mg bid for 10 days (if VAN was used for primary episode in a patient without risk factors). Patient with risk factors h,j: VAN extended-regimen k OR FDX EPX g | VAN prolonged tapered and pulsed regimen (if SOC VAN was used in primary episode) | |
Second or subsequent recurrence | SOC FDX | SOC FDX + BEZ 10 mg/kg IV once OR SOC FDX followed by FMT | SOC FDX | FDX EPX if it was not previously used | |
VAN tapered and pulsed regimen OR SOC VAN followed by RAX 400 mg tid for 20 days | SOC VAN followed by FMT OR SOC VAN + BEZ 10 mg/kg IV once | VAN prolonged tapered and pulsed regimen | VAN extended regimen k | VAN tapered and pulsed regimen OR VAN 125 mg qid for 10–14 days followed by RAX (unavailable in Mexico) 400 mg tid for 20 days | |
Adjunctive therapy: BEZ 10 mg/kg IV once after SOC | Alternative regimen: VAN tapered and pulsed regimen (if FDX, BEZ, and FMT are unavailable) | TEC 100–200 mg bid for 10–14 days if it was not previously used | |||
FMT | FMT | FMT (for third and subsequent recurrence) | FMT | FMT | |
Fulminant CDI l | VAN 500 mg qid PO or NGT + IV MET 500 mg tid | SOC VAN OR SOC FDX + surgical consultation | VAN 500 mg qid PO or NGT + IV MET 500 mg tid | VAN 125–500 mg qid PO or NGT + IV MET 500 mg tid | VAN 250–500 mg qid PO or NGT + IV MET 500 mg tid |
If ileus present: Consider adding rectal VAN 500 mg in 100 mL NaCl qid as retention enema. | If ileus present: Consider adding rectal VAN 500 mg in 100 mL NaCl qid as retention enema. | VAN 125–500 mg qid PO or NGT plus VAN 0.25–1 g bid-qid per rectum | If ileus or abdominal distention: VAN 500 mg qid rectal |
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Mendo-Lopez, R.; Alonso, C.D.; Villafuerte-Gálvez, J.A. Best Practices in the Management of Clostridioides difficile Infection in Developing Nations. Trop. Med. Infect. Dis. 2024, 9, 185. https://doi.org/10.3390/tropicalmed9080185
Mendo-Lopez R, Alonso CD, Villafuerte-Gálvez JA. Best Practices in the Management of Clostridioides difficile Infection in Developing Nations. Tropical Medicine and Infectious Disease. 2024; 9(8):185. https://doi.org/10.3390/tropicalmed9080185
Chicago/Turabian StyleMendo-Lopez, Rafael, Carolyn D. Alonso, and Javier A. Villafuerte-Gálvez. 2024. "Best Practices in the Management of Clostridioides difficile Infection in Developing Nations" Tropical Medicine and Infectious Disease 9, no. 8: 185. https://doi.org/10.3390/tropicalmed9080185