Typhoid diagnosis and associated prevailing drug resistance in Mbale city, Uganda

SAMUEL GIDUDU; Jesca Nakavuma; Dennis Muhanguzi; Francis Mutebi; Herbert Itabangi; Jacob Iramiot

doi:10.12688/f1000research.109968.2

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Research Article

Revised

Typhoid diagnosis and associated prevailing drug resistance in Mbale city, Uganda

[version 2; peer review: 1 approved, 1 approved with reservations]

SAMUEL GIDUDU ¹, Jesca Nakavuma¹, Dennis Muhanguzi¹, Francis Mutebi¹, Herbert Itabangi², Jacob Iramiot²

SAMUEL GIDUDU ¹, Jesca Nakavuma¹, [...] Dennis Muhanguzi¹, Francis Mutebi¹, Herbert Itabangi², Jacob Iramiot²

PUBLISHED 26 Feb 2024

Author details Author details

¹ Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda
² Department of Microbiology and Immunology, Faculty of Health Sciences, Busitema University, Mbale, Uganda

SAMUEL GIDUDU
Roles: Conceptualization, Data Curation, Formal Analysis, Funding Acquisition, Investigation, Methodology, Project Administration, Resources, Software, Writing – Original Draft Preparation, Writing – Review & Editing

Jesca Nakavuma
Roles: Supervision, Writing – Review & Editing

Dennis Muhanguzi
Roles: Supervision, Writing – Review & Editing

Francis Mutebi
Roles: Supervision, Writing – Review & Editing

Herbert Itabangi
Roles: Writing – Review & Editing

Jacob Iramiot
Roles: Writing – Review & Editing

OPEN PEER REVIEW

REVIEWER STATUS

This article is included in the Emerging Diseases and Outbreaks gateway.

Abstract

Background

The study aimed at determining the predictive values of Widal’s test against culture and the antimicrobial sensitivity profile of Salmonella typhi (S. typhi) isolates from patients attending private health facilities in Mbale city, Uganda. This was to provide evidence-based information to policy implementers for guideline enforcement.

Methods

This was a quantitative cross-sectional study in which 172 participants were recruited. Blood and stool samples collected were cultured; and to each stool sample the following tests were done; Xylose Lysine Deoxycholate (XLD), Salmonella Shigella agar (SSA), and MacConkey. Isolates suggestive for S. typhi were examined with triple sugar iron (TSI) and SIM (Sulphur, indole, and motile) and antibiotic sensitivity test (Ciprofloxacin, Imipenem, Ceftriaxone, Chloramphenicol and Augmentin for sensitivity testing) conducted with Mueller Hinton respectively. Generated data was entered in the Epidemiological information (Epi Info) software (version 7) and analyzed using the contingency table to determine the sensitivity, specificity, positive predictive value and the negative predictive value. The analysis was then presented in form of graphs and tables.

Results

The positive predictive value (PPV) for Widal’s test was 6.8% while the negative predictive value (NPV) was 100%. Three isolates were sensitive to Ciprofloxacin (3, 100%) and Imipenem (3, 100%), intermediate to Ceftriaxone (2, 67%) and resistant to Chloramphenicol (2, 67%) and Augmentin (2, 67%).

Conclusion

In comparison with culture, Widal’s test is highly sensitive (100%) with a low specificity of 76% and PPV (6.8%) and NPV (100%). It should therefore be followed up with a more specific confirmatory test. S. typhi was highly sensitive to both Ciprofloxacin and Imipenem; and resistant Chloramphenicol and Augmentin.

Keywords

Typhoid fever, Widal's test

Corresponding author: SAMUEL GIDUDU

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2024 GIDUDU S et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

How to cite: GIDUDU S, Nakavuma J, Muhanguzi D et al. Typhoid diagnosis and associated prevailing drug resistance in Mbale city, Uganda [version 2; peer review: 1 approved, 1 approved with reservations]. F1000Research 2024, 11:319 (https://doi.org/10.12688/f1000research.109968.2) First published: 17 Mar 2022, 11:319 (https://doi.org/10.12688/f1000research.109968.1) Latest published: 26 Feb 2024, 11:319 (https://doi.org/10.12688/f1000research.109968.2)

Revised Amendments from Version 1

The second version supersedes the first version following revision of the manuscript. Changes have been made in captions of figures, title of tables, additional information on how sensitivity, specificity, positive predictive value and negative predictive value were calculated. Added included explanations/justifications on why both blood and stool were considered in this study; and what gap was to be filled by this paper's findings. We also included possible reasons why findings of this study were disagreeing with other study's findings.

See the authors' detailed response to the review by Letemichael Negash Welekidan

Introduction

The global burden of typhoid fever was estimated at 17 million cases with 178,000 deaths in 2015 with more cases being reported in South Asia, South East Asia, and Sub-Saharan Africa.¹ Whereas typhoid fever appears to be less common or under ascertained in Africa compared to Asia, more recent studies confirm that typhoid fever incidence is high in some parts of Africa.²

The prevalence of the fever in Uganda was reported to be 7.6% during the February, 2015 disease outbreak that started from Kampala City³ and by the month of December 2015, the cases were reported by nearly all districts in Uganda with central region reporting the highest numbers followed by Northern, Western and Eastern respectively. In Mbale specifically, the prevalence of typhoid fever was reported at 1.3%.⁴

The recommended diagnosis for typhoid fever in Uganda is by use of culture, rapid antibody tests, Polymerase Chain Reaction (PCR) and relative leukopenia tests and not Widal’s test⁵; and the antibiotics used for treatment include Ciprofloxacin, Chloramphenicol, Ceftriaxone, and or Amoxicillin depending on the fever’s severity.⁵ Private health facilities in Mbale city are still depending on the Widal’s test that is no longer recommended to diagnose typhoid fever which isn’t the case in public health facilities. The test is not recommended because of its low positive predictive value (60%) and low negative predictive value (75.2%).⁶ The non-compliance to the diagnostic guidelines of diagnosing typhoid fever is causing inappropriate drug prescription and multidrug resistance development against antibiotics like ampicillin, chloramphenicol and ciprofloxacin.⁷

Since accurate diagnosis is crucial to the management of typhoid fever,⁷ the research aimed at determining the predictive values of Widal’s test against culture and the antimicrobial sensitivity profile of S. typhi isolates from patients attending private health facilities in Mbale city, Uganda; and give information about how typhoid fever is being managed in private health facilities, act as a basis for developing or re-enforcing policies on typhoid fever management, and also act as a reference to other researchers adventuring in the same field of study.

Methods

Ethical considerations

This study was approval by the Mbale regional referral hospital research ethical committee (MRRH REC) with a reference of MRRH-REC IN-COM 006/2018 before data collection. MRRH REC is accredited by UNST with a registration number of UG-REC-011. Permission was sought from Mbale city authorities and private health facility authorities before conducting the study. A written consent was sought from the participants prior to recruitment into the study. Codes instead of names were used as sample identification numbers for confidentiality purposes. Results obtained were availed to the clinicians and the research participants for health management purposes. The S. typhi isolates and the data summary was kept safely in the Mbale regional referral hospital microbiology laboratory.

Patients and samples

This was a quantitative cross-sectional study that recruited 172 patients clinically suspected for typhoid fever and seeking treatment from private clinics in Mbale city between December, 2017 to January, 2018. A systematic sampling technique was used to identify and enroll four participants (every 1st, 3rd, 5th and 7th) from each private health facility into the study. The sample size was used to obtain the number of private facilities to be enrolled into the study (i.e., sample size/number of expected participants per facility). The study included typhoid suspects seeking diagnosis and treatment in private health facilities during the period of study and consented in writing to participate in the study. Those who were on antibiotics within one month of the study were excluded. Both blood samples (10 ml and 2 ml) and stool samples (2 g) were collected from the research participants for study and treatment purposes.

Specimen collection/sampling procedure

Using a vacuum extraction blood-sampling system, 10 mls of blood was aseptically collected from the research participant and dispensed directly into BD blood culture bottle. 2 ml syringe was used to aseptically collect 2 ml of blood from the research participant, discarded the needle, opened the plan vacutainer tube to dispense the 2 ml volume of collected blood; this was used for Widal’s test by the laboratory staff at the private health facility as routine. The private health facility continued with their usual technique of tile rocking as they observed for agglutination while performing the Widal’s screening test using serum as a sample. To widen the scope of the investigation, and following orientation, research participant scooped 2 g of fresh stool samples using the spoon in the clean leak-proof containers that were free from disinfectant or detergent residue and recapped with tight-fitting, leak-proof lids; and delivered to the private health facility laboratory where it was inoculated into a Cary Blair media for transportation to the microbiology laboratory for culture. Both blood and stool samples including the request form were triple packaged and transported to the microbiology Laboratory Unit at Microbiology Department in Mbale regional referral hospital. Other information collected from the research participants included demographic data such age and gender and the Widal’s test result at the private health facility.

Blood and stool culture and sensitivity

BD blood culture bottles inoculated with blood samples were inserted into the Bactec machine for incubation set at 37°C for up to seven days. While, Stool samples were inoculated on XLD, SS agar (placed in the incubator set at 37°C for 24 hours) and MacConkey was first placed into anerobic gar before placing it in the incubator to limit the background of environmental flora and allow only S. typhi to grow. Gram reaction testing, triple iron sugar (TSI), and SIM biochemical testing were performed on isolates for identification purposes. The susceptibility of each bacteria to each antibiotic disk (Ciprofloxacin, Ceftriaxone, Azithromycin, Amoxiclave, Imipenem and Chloramphenicol) was done using the disc diffusion method and results recorded as resistant (R), Intermediate (I) and Sensitive (S).

Data management and analysis

Data generated from the study was entered in the Epidemiological information (Epi Info) software (version 7) and analyzed using the contingency table to determine the sensitivity, specificity, positive predictive value (PPV) and the negative predictive value (NPV). Sensitivity was calculated as number of research participants with culture positive and Widal reactive test results divided by total number of those with culture positive results and multiplied by 100. Specificity was calculated as number of research participants with culture negative and Widal non-reactive test results divided by total number of those with culture positive results and multiplied by 100. PPV was calculated as number of research participants with Widal reactive and culture positive test results divided by the total number of those with Widal reactive test results and multiplied by 100. The NPV was calculated as number of research participants with Widal non-reactive and culture negative test results divided by the total number of those with Widal non-reactive test results and multiplied by 100. The analysis was then presented in form of graphs and tables.

Safety and environment

The personal protective equipment (examination gloves, lab coats and closed shoes) was put on during sample collection and sample processing procedures. The media (except blood culture broth) were prepared aseptically, and incubated to rule out contamination. All Laboratory procedures were done following the standard operation procedures (SOPs) guide lines of the Mbale regional referral hospital microbiology laboratory.

Results

Demographic characteristics of research participants

A total of 172 participants, 55% female and 45% male, aged between <17 to >50 years were enrolled for the study. Majority of the participants were aged between 18 and 34 years and few were those above 50 years of age (Figure 1).

Figure 1. Description of participants by age and gender.

Comparison of Widal’s test with bacterial culture

Occurrence of S. typhi positive participants

Out of the 172 Widal’s tests that were done in the private health facility, 44 (25.6%) were reactive and 128 (74.4%) were non-reactive. When compared to the gold standard, culture had 3 (1.7%) S. typhi isolates and 169 (98.3%) did not have any significant growth (Table 1).

Table 1. Culture and Widal’s test results.

Widal’s test results	Culture results
Widal’s test results	Positive	Negative	Total
Reactive	3 (6.8%)	41 (93.2%)	44 (25.6%)	PPV = 6.8%
Non-reactive	00	128 (100%)	128 (74.4%)	NPV = 100%
Total	3 (1.7%)	169 (98.3%)	172 (100%)
	Sensitivity = 100%	Specificity = 76%

The samples were drawn from 43 private health facilities of which only three (7%) had S. typhi isolated from their referred samples (Figure 2).

Figure 2. Description of private health facilities by culture test result.

S. typhi was isolated more from the male participants (67%, 2/3) as compared to the female counterparts (33%, 1/3). These isolates were mainly obtained from two age groups namely 18-34 years and 35-49 years with more amongst the 18-34 years age group (67%, 2/3). The S. typhi was isolated from three (03) stool samples and none from blood samples.

Diagnostic accuracy study

This study showed the Widal’s test diagnostic accuracy to be as follows: sensitivity (100%), specificity (76%), positive predictive value (6.8%) and negative predictive value (100%) (Table 1).

The antimicrobial sensitivity profiles

Drug sensitivity patterns

This study showed that the drugs i.e., Chloramphenicol and Augmentin demonstrated resistance each at 67% (2/3). Those that were highly sensitive included Ciprofloxacin and Imipenem each at 100% (3/3). Ceftriaxone 67% (2/3) was intermediate (Table 2).

Table 2. Antibiotic sensitivity pattern.

Antibiotic	Resistance	Sensitivity	Intermediate
Ciprofloxacin (CIP)	00	03	00
Imipenem (IPM)	00	03	00
Augmentin (AUG)	02	01	00
Chloramphenicol (C)	02	00	01
Ceftriaxone (CRO)	00	01	02

Discussion

This study revealed Widal’s test PPV as 6.8% suggestive of a possibility of not all participants with reactive Widal’s test result had typhoid fever.⁸^,⁹ This finding was similar to most of studies reviewed whose PPV was below 60% with exception of Minjibir (2020) whose PPV was 68.2%.⁶^,¹⁰^–¹⁵ Widal’s test may not be not dependable for diagnosis of typhoid fever.¹⁴ This study revealed Widal’s test NPV as 100% suggestive of a possibility of all participants with non-reactive Widal’s test result as not having typhoid fever.⁸^,⁹ This finding was similar to most of the studies reviewed whose NPV was above 90% with exception of Mengist (2017) and Mawazo (2019) who obtained 75.2% and 89.7% respectively.⁶^,¹⁰^–¹⁵ The difference with Mengist (2017) and Mawazo (2019) could be because of different brand of Widal’s test reagent used. Therefore, the Widal’s test result can serve as a good indicator of the absence of typhoid fever.¹¹ This study revealed that the Widal’s test had a sensitivity of 100%. This indicated that, the Widal’s test had the ability to rule out the presence of typhoid fever and this surpasses that of Widal’s test acceptable of 70%.¹⁶ This finding was similar to most of studies with exception of Yousif (2018) whose value was 26.5%.⁶^,¹⁰^–¹⁵ This study also revealed that the Widal’s test has a specificity of 76%. This indicated that Widal’s test had the ability to identify positive cases although with a high false positive rate of 93.2% (41/44). This was so probably because typhoid fever is uncommon among the participants hence giving a large proportion of false positive test results and this explains partly why this study’s positive predictive value was low (6.8%).¹⁷ This finding was similar to most of the studies reviewed whose value was above 70% specificity with exception of Deksissa and Gebremedhin (2019), Mawazo (2019) and Muthoni (2016) whose values were 44.4%, 18.3% and 47.7% respectively.⁶^,¹⁰^–¹⁵ The difference could be due to different brand of Widal’s test reagent used. As described by many scholars, false diagnosis of typhoid fever can lead to an inappropriate treatment which eventually leads to antibiotic resistance development, a serious threat to the global public health which if not addressed in time, may lead to mortality.¹⁸^,¹⁹ This study described the antibiotic sensitivity profile of S. typhi. Chloramphenicol was 67% (2/3) resistant, a finding was similar to Wasihum et al (2015) and Deksissa and Gebremedhi (2019) who reported 76.1% and 20% resistance respectively.¹¹^,²⁰ Augmentin was 67% (2/3) resistant, a finding similar to Wasihum et al (2015) and; Deksissa and Gebremedhi (2019) also reported 2.6% and 100% resistance.¹¹^,²¹ This study’s finding was however contrary to Chaudhary et al (2016) who reported Augmentin as 94.3% sensitive.¹⁰ This study also revealed that Ciprofloxacin was 100% (3/3) sensitive which finding was contrary to Wasihum et al (2015) who reported (76.1%).²¹ This study’s finding of Ceftriaxone being 67% (2/3) intermediate was contrary to Deksissa and Gebremedhi (2019) who reported 100% sensitivity.¹¹

Limitations

The limitation of this study was the very few S. typhi isolates since this did not provide adequate information on the antibiotic resistance profile of Mbale city. Future studies would increase the scope and study to obtain more S. typhi isolates such that adequate information on the antibiotic profile is obtained.

Conclusion

In comparison with culture, the gold standard, Widal’s test is highly sensitive (100%) with a high negative predictive value (100%) but low specificity (76%) and PPV (6.8%) S. typhi was highly sensitive to both Ciprofloxacin and Imipenem; and resistant Chloramphenicol and Augmentin. This urgent need for policy implementers to enforce adherence to Uganda Clinical Guidelines on typhoid fever diagnosis in Mbale city.

Impact statement

This study is significant in that, it gives information about how typhoid fever is being managed in private health facilities, act as a basis to develop or re-enforce policies on typhoid fever management, and act as a reference to other researchers adventuring in the same field of study. Inappropriate typhoid diagnosis in Mbale city private health facilities could lead to inappropriate antibiotic prescription, antibiotic resistance development and death. Conducting this comparative study and determining the antimicrobial sensitivity profile will provide information on typhoid fever management in private health facilities in Mbale city.

Data availability

The data that support the findings of this study are available on request from the corresponding author, [SG]. The data are not publicly available because they contain information that could compromise the privacy of research participants. If the reader needs access to the said data, they could do so by writing an email to the corresponding author, [SG] detailing justification for the primary data source request.

Acknowledgements

The author(s) would like to thank Makerere University for technical support while conducting the study; and with permission, the author(s) acknowledges the administrative support from Rt. Rev. Patrick Gidudu, DR. Can. Hannah Gidudu, Rev. Prof. Dr. Jeanette Meadway and Mr. John Meadway that facilitated the study. The views expressed in the submitted article are author(s) own and not an official position of the institution.

References

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2. Crump JA: Progress in Typhoid Fever Epidemiology. Clin. Infect. Dis. 2019 Feb 15 [cited 2021 Feb 23]; 68(Supplement_1): S4–S9. PubMed Abstract | Publisher Full Text Reference Source
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5. Ministry of health Uganda: Uganda Clinical Guidelines. Ministry of health Uganda; 2016 [cited 2017 Mar 10]; 1142. Reference Source
6. Mengist HM, Tilahun K, Mihiretie H: Diagnostic Value of Widal Test in the Diagnosis of Typhoid Fever: A Systematic Review. J. Med. Microb. Diagn. 2017 Feb 6 [cited 2018 May 11]; 06(01). Reference Source
7. Kabwama SN, Bulage L, Nsubuga F, et al.: A large and persistent outbreak of typhoid fever caused by consuming contaminated water and street-vended beverages: Kampala, Uganda, January - June 2015. BMC Public Health. 2017; 17(1): 241–320. Publisher Full Text Reference Source
8. Attia J: Moving beyond sensitivity and specificity: Using likelihood ratios to help interpret diagnostic tests. Vol. 26, Australian Prescriber. NPS MedicineWise. 2003 [cited 2018 May 11]; p. 111–113. Publisher Full Text Reference Source
9. Bentley ERLO: Positive and Negative Predictive Value of Diagnostic Tests: Introduction. Graduate Entry Medical School, University of Nottingham.2014 [cited 2018 May 11]. Reference Source
10. Chaudhary P, Sharma V, Chaudhary A, et al.: Comparative Study of Blood Culture and Widal Agglutination Test from the Patients Suspected of Enteric Fever. Br. Microbiol. Res. J. 2016 Jan 10 [cited 2021 Feb 24]; 16(5): 1–9. Publisher Full Text Reference Source
11. Deksissa T, Gebremedhin EZ: A cross-sectional study of enteric fever among febrile patients at Ambo hospital: Prevalence, risk factors, comparison of Widal test and stool culture and antimicrobials susceptibility pattern of isolates. BMC Infect. Dis. 2019 Mar 27 [cited 2021 Feb 24]; 19(1): 288. PubMed Abstract | Publisher Full Text
12. Minjibir AA, Diso SU, Ibrahim IS, et al.: Comparative Study of Widal test Against Stool Culture in Diagnosis of Typhoid Fever Suspected Cases in Kano, Northern Nigeria. South Asian Res. J. Eng. Tech. 2020 [cited 2021 Feb 24]; 2(5): 39–44. Publisher Full Text Reference Source
13. Mawazo A, Bwire GM, Matee MIN: Performance of Widal test and stool culture in the diagnosis of typhoid fever among suspected patients in Dar es Salaam, Tanzania. BMC. Res. Notes. 2019 Jun 5 [cited 2021 Feb 24]; 12(1): 316. PubMed Abstract | Publisher Full Text
14. Muthoni GC: Performance of Widal’s test and Stool culture as diagnostic methods for Salmonella typhi infectionin Chuka General Hospital, Tharaka Nithi County.2016 [cited 2021 Feb 24]. Reference Source
15. Yousif TAT: Comparison of Widal Test In Diagnosis of Typhoid Fever with Blood Culture and Immuno chromatographic Test among Patients in Wad Medani Teaching Hospital, Gezira State, Sudan (2012-2017).2018 Feb 13 [cited 2021 Feb 24]. Reference Source
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Version 2

VERSION 2 PUBLISHED 17 Mar 2022

Author details Author details

Jesca Nakavuma
Roles: Supervision, Writing – Review & Editing

Dennis Muhanguzi
Roles: Supervision, Writing – Review & Editing

Francis Mutebi
Roles: Supervision, Writing – Review & Editing

Herbert Itabangi
Roles: Writing – Review & Editing

Jacob Iramiot
Roles: Writing – Review & Editing

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

Article Versions (2)

version 2

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Published: 26 Feb 2024, 11:319

https://doi.org/10.12688/f1000research.109968.2

version 1

Published: 17 Mar 2022, 11:319

https://doi.org/10.12688/f1000research.109968.1

© 2024 GIDUDU S et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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GIDUDU S, Nakavuma J, Muhanguzi D et al. Typhoid diagnosis and associated prevailing drug resistance in Mbale city, Uganda [version 2; peer review: 1 approved, 1 approved with reservations]. F1000Research 2024, 11:319 (https://doi.org/10.12688/f1000research.109968.2)

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Version 2

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PUBLISHED 26 Feb 2024

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Reviewer Report 11 Sep 2024

Samuel Kariuki, Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya

Approved with Reservations

https://doi.org/10.5256/f1000research.163031.r319885

The study aimed at determining the predictive values of Widal’s test against culture and the antimicrobial sensitivity profile of Salmonella Typhi (S. Typhi) isolates from patients attending private health facilities in Mbale, Uganda. Overall, this paper presents data on an important subject of the growing threat of drug-resistant typhoid fever in endemic settings such as Mbale, and the growing challenge of poor diagnosis that results from lack of adequate laboratory resources (infrastructure and materials). The result from use of poor and often non-specific rapid tests is over-diagnosis of typhoid fever, leading to excessive use of antimicrobials, a key driver for AMR. There are a number of important concerns that the authors need to address:

ABSTRACT
Comment: Proper nomenclature is Salmonella enterica as a species, and Typhi serovar; thus Salmonella Typhi with only Genus name italicized.

Comment: Augmentin: proper antibiotic name - Amoxicillin-clavulanic acid.

INTRODUCTION
Line: Since accurate diagnosis is crucial to the management of typhoid fever,7 the research aimed at determining the predictive values of Widal’s test against culture and the antimicrobial sensitivity profile of S. typhi isolates from patients attending private health facilities in Mbale city, Uganda
Comment: Replace “crucial to” with “crucial for”
Line: act as a basis for developing or re-enforcing policies on typhoid fever management, and also act as a reference to other researchers adventuring in the same field of study.
Comment: Replace “other researchers adventuring in the same field” with “seeking to work in same field of study.”

METHODS
Line: This study was approval by the Mbale regional referral hospital research ethical committee (MRRH REC) with a reference of MRRH-REC IN-COM 006/2018, before data collection.
Comment: Delete “before data collection”
Line: Both blood samples (10 ml and 2 ml) and stool samples (2 g) were collected from the research participants for study and treatment purposes.
Comment: Why were two different volumes of blood taken?

RESULTS
Line: Figure 2. Description of private health facilities by culture test result.
Comment: This figure has very little data to show, you can omit and just do a sentence on the finding

DISCUSSION
Line: The information on antimicrobial resistance profiles of just 3 isolates to be compared and contrasted with other studies gives an impression of overrated outcomes! Authors should be cautious of making conclusions on this, unless they can refer to other previous more detailed AMR data from the same settings

LIMITATIONS
Line: The limitation of this study was the very few S. typhi isolates [SK3] [SK4] since this did not provide adequate information on the antibiotic resistance profile of Mbale city
Comment: This limitation on the small number of isolates analysed is a crucial one in interpretation of the results; 3 isolates is such a small number! Authors should also state where the 3 isolates came from, as they may be all be from same facility or ward? Just to also note that the Widal test has long been discontinued in many clinical labs, essentially due to its poor performance in sensitivity and specificity. This study reinforce these previous findings, and should engage policy at Ministry of Health in Mbale and the region in enforcing change in diagnostic approaches in private labs still using the test.

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Epidemiology, genomics of Enteric pathogens and AMR

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report 09 Apr 2024

Letemichael Negash Welekidan, Food safety, Norwegian University of Life Sciences, Oslo, Norway

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https://doi.org/10.5256/f1000research.163031.r250262

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Author Response 21 Jun 2024

Samuel GIDUDU, Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

21 Jun 2024

Author Response

Thank you for your review.
Competing Interests: No competing interests
Thank you for your review.
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Author Response 21 Jun 2024

Samuel GIDUDU, Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

21 Jun 2024

Author Response

Thank you for your review.
Competing Interests: No competing interests
Thank you for your review.
Thank you for your review.
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Version 1

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Reviewer Report 03 Oct 2023

Letemichael Negash Welekidan, Food safety, Norwegian University of Life Sciences, Oslo, Norway

Approved with Reservations

https://doi.org/10.5256/f1000research.121530.r204934

Summary of the paper:

The article tried to evaluate widal test as a diagnostic test for typhoid fever in private clinics in Mbale, Uganda. The paper mentioned that widal test is not recommended in Uganda for diagnosing typhoid fever due to low positive and negative predictive values but the private clinic in Uganda still uses it. This paper aimed at evaluating widal test and antimicrobial susceptibility test for Salmonella typhi (S.typhi), the causative agent of typhoid fever.

The result showed the the sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) of widal test and the antimicrobial susceptibility pattern of S.typhi.

Questions:

If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding?
What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper.
You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear?
What software do you used for analysis of drug susceptibility profile (DST) and participant's data?
In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that
How did you calculate the sensitivity, specificity, PPV and NPV?
I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile
Figure captions should be at the bottom of the figure, make corrections to your figure captions.
Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile
In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.
In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear.
There are spelling errors
Over all the paper looks shallow so try to enrich it to make it a good paper.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Partly
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Microbiologist

CITE

Report a concern

Author Response 13 Apr 2024

Samuel GIDUDU, Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

13 Apr 2024

Author Response
1. If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill
... Continue reading
If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding? The gap to be filled is providing evidence-based information to the policy implementer in order to enforce appropriate diagnostic technique for Typhoid fever in Mbale city

What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper. This been made clearer in the newer vision of the article. As quick response, we only retrieved Widal test results from the private health facility. and collected samples for Culture and Sensitivity. Also to mention. We did not interfere with the procedure used at the private health facility but rather requested them to also collect blood for culture in addition to their routine method of Widal testing.

You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear? This been made clearer in the newer vision of the article. As quick response, We cultured both blood and stool to widen the scope of investigation of typhoid fever.

What software do you used for analysis of drug susceptibility profile (DST) and participant's data? We did not use a software to do the analysis but rather a contingency table that was generated from Epidemiological information (Epi Info) software (version 7).

In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that: This has been corrected to read <17 to >50. all persons below 17 years were summed up

How did you calculate the sensitivity, specificity, PPV and NPV? We used stardard formulas to calculate these. The formulas have been included in the newer version of the manuscript

I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile: This have been addressed in the newer version of the manuscript

Figure captions should be at the bottom of the figure, make corrections to your figure captions. This have been addressed in the newer version of the manuscript

Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile This have been addressed in the newer version of the manuscript

In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.This have been addressed in the newer version of the manuscript

In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear. This have been addressed in the newer version of the manuscript

There are spelling errors. This have been addressed in the newer version of the manuscript

Over all the paper looks shallow so try to enrich it to make it a good paper. This have been addressed in the newer version of the manuscript
If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding? The gap to be filled is providing evidence-based information to the policy implementer in order to enforce appropriate diagnostic technique for Typhoid fever in Mbale city

What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper. This been made clearer in the newer vision of the article. As quick response, we only retrieved Widal test results from the private health facility. and collected samples for Culture and Sensitivity. Also to mention. We did not interfere with the procedure used at the private health facility but rather requested them to also collect blood for culture in addition to their routine method of Widal testing.

You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear? This been made clearer in the newer vision of the article. As quick response, We cultured both blood and stool to widen the scope of investigation of typhoid fever.

What software do you used for analysis of drug susceptibility profile (DST) and participant's data? We did not use a software to do the analysis but rather a contingency table that was generated from Epidemiological information (Epi Info) software (version 7).

In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that: This has been corrected to read <17 to >50. all persons below 17 years were summed up

How did you calculate the sensitivity, specificity, PPV and NPV? We used stardard formulas to calculate these. The formulas have been included in the newer version of the manuscript

I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile: This have been addressed in the newer version of the manuscript

Figure captions should be at the bottom of the figure, make corrections to your figure captions. This have been addressed in the newer version of the manuscript

Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile This have been addressed in the newer version of the manuscript

In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.This have been addressed in the newer version of the manuscript

In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear. This have been addressed in the newer version of the manuscript

There are spelling errors. This have been addressed in the newer version of the manuscript

Over all the paper looks shallow so try to enrich it to make it a good paper. This have been addressed in the newer version of the manuscript
Competing Interests: No competing interests Close
Report a concern
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COMMENTS ON THIS REPORT

Author Response 13 Apr 2024

Samuel GIDUDU, Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

13 Apr 2024

Author Response
1. If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill
... Continue reading
If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding? The gap to be filled is providing evidence-based information to the policy implementer in order to enforce appropriate diagnostic technique for Typhoid fever in Mbale city

What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper. This been made clearer in the newer vision of the article. As quick response, we only retrieved Widal test results from the private health facility. and collected samples for Culture and Sensitivity. Also to mention. We did not interfere with the procedure used at the private health facility but rather requested them to also collect blood for culture in addition to their routine method of Widal testing.

You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear? This been made clearer in the newer vision of the article. As quick response, We cultured both blood and stool to widen the scope of investigation of typhoid fever.

What software do you used for analysis of drug susceptibility profile (DST) and participant's data? We did not use a software to do the analysis but rather a contingency table that was generated from Epidemiological information (Epi Info) software (version 7).

In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that: This has been corrected to read <17 to >50. all persons below 17 years were summed up

How did you calculate the sensitivity, specificity, PPV and NPV? We used stardard formulas to calculate these. The formulas have been included in the newer version of the manuscript

I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile: This have been addressed in the newer version of the manuscript

Figure captions should be at the bottom of the figure, make corrections to your figure captions. This have been addressed in the newer version of the manuscript

Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile This have been addressed in the newer version of the manuscript

In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.This have been addressed in the newer version of the manuscript

In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear. This have been addressed in the newer version of the manuscript

There are spelling errors. This have been addressed in the newer version of the manuscript

Over all the paper looks shallow so try to enrich it to make it a good paper. This have been addressed in the newer version of the manuscript
If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding? The gap to be filled is providing evidence-based information to the policy implementer in order to enforce appropriate diagnostic technique for Typhoid fever in Mbale city

What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper. This been made clearer in the newer vision of the article. As quick response, we only retrieved Widal test results from the private health facility. and collected samples for Culture and Sensitivity. Also to mention. We did not interfere with the procedure used at the private health facility but rather requested them to also collect blood for culture in addition to their routine method of Widal testing.

You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear? This been made clearer in the newer vision of the article. As quick response, We cultured both blood and stool to widen the scope of investigation of typhoid fever.

What software do you used for analysis of drug susceptibility profile (DST) and participant's data? We did not use a software to do the analysis but rather a contingency table that was generated from Epidemiological information (Epi Info) software (version 7).

In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that: This has been corrected to read <17 to >50. all persons below 17 years were summed up

How did you calculate the sensitivity, specificity, PPV and NPV? We used stardard formulas to calculate these. The formulas have been included in the newer version of the manuscript

I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile: This have been addressed in the newer version of the manuscript

Figure captions should be at the bottom of the figure, make corrections to your figure captions. This have been addressed in the newer version of the manuscript

Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile This have been addressed in the newer version of the manuscript

In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.This have been addressed in the newer version of the manuscript

In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear. This have been addressed in the newer version of the manuscript

There are spelling errors. This have been addressed in the newer version of the manuscript

Over all the paper looks shallow so try to enrich it to make it a good paper. This have been addressed in the newer version of the manuscript
Competing Interests: No competing interests Close
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Version 2

VERSION 2 PUBLISHED 17 Mar 2022

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Letemichael Negash Welekidan, Norwegian University of Life Sciences, Oslo, Norway
Samuel Kariuki, Kenya Medical Research Institute, Nairobi, Kenya

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11 Sep 2024 | for Version 2

Samuel Kariuki, Centre for Microbiology Research, Kenya Medical Research Institute, Nairobi, Kenya

3 Views Cite this report Responses(0)

Approved With Reservations

Is the work clearly and accurately presented and does it cite the current literature?

Yes
Is the study design appropriate and is the work technically sound?

Yes
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Yes
Are all the source data underlying the results available to ensure full reproducibility?

Yes
Are the conclusions drawn adequately supported by the results?

Partly

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Epidemiology, genomics of Enteric pathogens and AMR

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Reviewer Report

7 Views

09 Apr 2024 | for Version 2

Letemichael Negash Welekidan, Food safety, Norwegian University of Life Sciences, Oslo, Norway

7 Views Cite this report Responses(1)

Approved

I do not have any further comments.

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Microbiologist

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report

16 Views

03 Oct 2023 | for Version 1

Letemichael Negash Welekidan, Food safety, Norwegian University of Life Sciences, Oslo, Norway

16 Views Cite this report Responses(1)

Approved With Reservations

If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding?
What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper.
You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear?
What software do you used for analysis of drug susceptibility profile (DST) and participant's data?
In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that
How did you calculate the sensitivity, specificity, PPV and NPV?
I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile
Figure captions should be at the bottom of the figure, make corrections to your figure captions.
Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile
In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.
In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear.
There are spelling errors
Over all the paper looks shallow so try to enrich it to make it a good paper.

Is the work clearly and accurately presented and does it cite the current literature?

Partly
Is the study design appropriate and is the work technically sound?

Partly
Are sufficient details of methods and analysis provided to allow replication by others?

Partly
If applicable, is the statistical analysis and its interpretation appropriate?

Partly
Are all the source data underlying the results available to ensure full reproducibility?

Partly
Are the conclusions drawn adequately supported by the results?

Yes

Competing Interests

No competing interests were disclosed.

Reviewer Expertise

Microbiologist

Respond to this report

Responses (1)

Author Response

13 Apr 2024

Samuel GIDUDU, Department of Biomolecular Resources and Biolaboratory Sciences; School of Biosecurity; Biotechnical and Laboratory Science; College of Veterinary Medicine Animal Resources and Biosecurity, Makerere University, Kampala, Uganda

If widal test is not recommended by the ministry of health of Uganda due to its low PPV and NPV, so what gap are you going to fill from this paper's finding? The gap to be filled is providing evidence-based information to the policy implementer in order to enforce appropriate diagnostic technique for Typhoid fever in Mbale city
What technique and what sample have you used for the widal test and how you performed? I could not find it in the paper. This been made clearer in the newer vision of the article. As quick response, we only retrieved Widal test results from the private health facility. and collected samples for Culture and Sensitivity. Also to mention. We did not interfere with the procedure used at the private health facility but rather requested them to also collect blood for culture in addition to their routine method of Widal testing.
You have cultured both blood and stool samples, what was the purpose to culture both the samples and how did you present the results for both samples is not clear? This been made clearer in the newer vision of the article. As quick response, We cultured both blood and stool to widen the scope of investigation of typhoid fever.
What software do you used for analysis of drug susceptibility profile (DST) and participant's data? We did not use a software to do the analysis but rather a contingency table that was generated from Epidemiological information (Epi Info) software (version 7).
In the result part, it is written that participant age range is 17-50 but figure-1 shows also <17 years. Make a correction or justify it why you put it like that: This has been corrected to read <17 to >50. all persons below 17 years were summed up
How did you calculate the sensitivity, specificity, PPV and NPV? We used stardard formulas to calculate these. The formulas have been included in the newer version of the manuscript
I suggest reorder the table numbers and correct its citation on the text, and text should be before the table and correct the table for antimicrobial susceptibility profile: This have been addressed in the newer version of the manuscript
Figure captions should be at the bottom of the figure, make corrections to your figure captions. This have been addressed in the newer version of the manuscript
Use one suitable subtitle under the result part; e.g you used: Comparison of widal test with bacterial culture and under it Occurrence of S.typhi positive participants and same comment for the antimicrobial sensitivity profile This have been addressed in the newer version of the manuscript
In the discussion part you did not justify or reason out for the disagreement between your study and other studies when applicable.This have been addressed in the newer version of the manuscript
In your introduction it is written that widal test is not recommended by the ministry of health of Uganda but you concluded that widal test should be followed by specific confirmatory test. As the ministry of health is recommended already these specific tests that you are referring for as primary diagnostics, so are you recommending to the policy makers to use widal test or recommending for what they have already recommend? Make it clear. This have been addressed in the newer version of the manuscript
There are spelling errors. This have been addressed in the newer version of the manuscript
Over all the paper looks shallow so try to enrich it to make it a good paper. This have been addressed in the newer version of the manuscript

View more View less

Competing Interests

No competing interests

Alongside their report, reviewers assign a status to the article:

Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested

Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.

Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions

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[11] 11. Deksissa T, Gebremedhin EZ: A cross-sectional study of enteric fever among febrile patients at Ambo hospital: Prevalence, risk factors, comparison of Widal test and stool culture and antimicrobials susceptibility pattern of isolates. BMC Infect. Dis. 2019 Mar 27 [cited 2021 Feb 24]; 19(1): 288. PubMed Abstract | Publisher Full Text

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[13] 13. Mawazo A, Bwire GM, Matee MIN: Performance of Widal test and stool culture in the diagnosis of typhoid fever among suspected patients in Dar es Salaam, Tanzania. BMC. Res. Notes. 2019 Jun 5 [cited 2021 Feb 24]; 12(1): 316. PubMed Abstract | Publisher Full Text

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[16] 16. TULIP diagnostics: Widal Antigen Set/Antigens for Slide and Tube Tests.2012 [cited 2021 Feb 25]; 1–2. Reference Source

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[19] 19. Watkins RR, Bonomo RA: Overview: Global and Local Impact of Antibiotic Resistance. Vol. 30, Infectious Disease Clinics of North America. Elsevier.2016 [cited 2018 Sep 20]; p. 313–322. Reference Source

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[21] 21. Wasihun AG, Wlekidan LN, Gebremariam SA, et al.: Diagnosis and Treatment of Typhoid Fever and Associated Prevailing Drug Resistance in Northern Ethiopia. Int. J. Infect. Dis. 2015 Jun 1; 35: 96–102. Publisher Full Text

Typhoid diagnosis and associated prevailing drug resistance in Mbale city, Uganda

Abstract

Background

Methods

Results

Conclusion

Keywords

Revised Amendments from Version 1

Introduction

Methods

Ethical considerations

Patients and samples

Specimen collection/sampling procedure

Blood and stool culture and sensitivity

Data management and analysis

Safety and environment

Results

Demographic characteristics of research participants

Figure 1. Description of participants by age and gender.

Comparison of Widal’s test with bacterial culture

Table 1. Culture and Widal’s test results.

Figure 2. Description of private health facilities by culture test result.

The antimicrobial sensitivity profiles

Table 2. Antibiotic sensitivity pattern.

Discussion

Limitations

Conclusion

Impact statement

Data availability

Acknowledgements

References

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