PONE-D-20-22153

The Human Health Burden of nontyphoidal Salmonella and Vibrio parahaemolyticus Foodborne Gastroenteritis in Shanghai, East China

PLOS ONE

Dear Dr. Chen,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The Academic Editor would like to apologize to the authors for the long duration of the review process; it was due to the unavailability of multiple reviewers with expertise in the field of surveillance and epidemiology who were invited by the editor to handle the manuscript but could not accept the invitation. Review comments have been timely provided by only one invited reviewer and are attached in the present letter. In order to provide the authors with a timely decision, this manuscript proceeded to the next stage of the editorial process, based on the evaluation provided by one external reviewer and the academic editor herself.

Editor’s comments

Although the Academic Editor is not an epidemiologist, raised comments regarding the overall approach of the presented study from a food microbiology perspective, its scientific soundness as well as the quality of the manuscript are summarized below. According to the editor’s opinion, the manuscript should be subject to minor revisions before its publication in PLOS ONE is considered. Beyond the more specific comments that are following, a general a comment is an overall cross-check with regard to English grammar/syntax (maybe a review by an English expert/native speaker should be considered).  

- Title: both in the manuscript’s title and throughout the manuscript, please use the species name “Salmonella enterica” (or S. enterica after first mentioning) instead of the genus name (i.e. Salmonella). The genus Salmonella includes two species (i.e. Salmonella enterica and Salmonella bongori) and only S. enterica is regarded as a foodborne pathogen for humans.

- L24-25: please revise to “…cases for non-typhoidal salmonellosis and V. parahaemolyticus infection, respectively, illustrating that bacterial gastroenteritis due to these two pathogens poses a substantial health burden”

- L27: revise to “…and the data actually reported for foodborne diseases…”

- L45: I would suggest using “relative” instead of “proportionate”

- L48: please correct to “the Netherlands”

- L53: please revise to “…for precisely estimating foodborne disease burden and monitoring the impact…”

- L58-59: please revise to “…among patients provides important basic data for estimating foodborne disease burden”

- L64: the phrase “foodborne pathogenic infections” is rather specific for such a general statement; I would suggest using “foodborne illness severity” instead.

- L92: correct to “eight sentinel hospitals”

- L94-95: please correct to “Rectal swabs or stool specimens from patients with diarrhea were collected from the sentinel hospitals…”

- L96: revise to “non-typhoidal S. enterica and V. parahaemolyticus by the laboratories of the Chinese Center for Disease Control and Prevention”; in general, be consistent using the same single (and not multiple) terms throughout the manuscript, e.g. “non-typhoidal” (instead of “non-typhoid”  or “nontyphoidal”), “foodborne” (instead of “food-borne”), etc.

- L98: please correct to “…were representative of the community samples”

- L99-103: revise to “For S. enterica detection, specimens were enriched in selenite broth, followed by surface plating (or plating) on Bismuth sulfite agar and xylose-lysine-desoxycholate (XLD) agar. With reference to V. parahaemolyticus detection, specimens were enriched in alkaline peptone water, followed by surface plating (or streaking) on thiosulfate citrate bile salts sucrose agar or CHROMagar Vibrio agar”. Moreover, were specific ISO protocols applied for these selective enrichment procedures? If so, please refer to the specific protocols (as in-text citations with the corresponding additions in the references’ list).     

- L107-113: it would be better for the reader (particularly a non-expert in epidemiology) if definitions of M1, M2 and M3 are provided in brief

- L111: please change to “Then, the number of submitted stool specimens was divided by…”

- L112: by “laboratory performing test for pathogens” you refer to “laboratory pathogen testing”? If so, consider using the second (simpler) term both here and wherever else applicable in the manuscript’s text.

- L114: change to “It was assumed that the laboratory testing sensitivity was 87.5%...”; in general, use third person (and not “we”) when providing descriptions pertinent to the Materials and Methods and/or Results section of the manuscript.

- L117: please revise to “Figure 1 shows the pyramid of the burden of pathogen-specific foodborne gastroenteritis”

- L118-119: please revise to “…were modeled using the Pert distribution. The estimation model was developed using @RISK…”

- L120: please revise to “The number of positive specimens tested was multiplied with M to estimate the number of sportive samples in the surveillance area”

- L123: please correct to “…were assessed”

- L124: revise to “Pyramid of the burden of pathogen-specific gastroenteritis”. Also, is this the appropriate place in the manuscript’s text for a figure caption (and the same applies for Fig. 2 caption in L157-158)?

- L125-126: please revise to “…non-typhoidal salmonellosis and Vibrio parahaemolyticus infection…”; please use the same phrase when referring to the infection (gastroenteritis) caused by these two pathogens throughout the manuscript for simplification and consistency reasons.

- Table 1: in the last line (referring to M4) and the last column (referring to the distribution) please use a decimal digit for all three numbers (namely, 1.0, 1.1 and 2.0).

- L129-135: please revise as following recommended: “Since there are no data on the proportion…on data published by Hald et al. [23]…and were multiplied by the number of illnesses to obtain foodborne non-typhoidal salmonellosis [23], while the proportion based on US research was used to obtain…The estimated pathogen-specific numbers of foodborne illness cases were compared with the routinely reported numbers of foodborne outbreak cases so as to calibrate the surveillance data”. Please keep in mind that “data” is plural (singular form the Latin word “datum”), and proceed with all required grammar corrections when using this term throughout the manuscript.

- L138: change to “…the National Institute for Nutrition and Food Safety…”

- L149-150: please revise to “…36.9% (95% CI 26.5-47.2) visited a doctor, and among them 34.4% (95% CI 17.0-51.9) submitted a stool specimen”

- L155-156: please correct to “…(Fig. 2), while more information regarding the two studied bacterial species was not collected”

- L157-158: please revise the Figure 2 caption to “Month-wise isolation rate for non-typhoidal Salmonella enterica and Vibrio parahaemolyticus in Shanghai, east China, 2010-2011”

- L165: please correct to “Among people seeking medical care, 34.4%...”

- L168: please correct to “Considering that the number of stool specimens tested in the surveillance area was 4,548…”

- L170: change to “…laboratory confirmed salmonellosis or V. parahaemolyticus infection…”; also to what does “respectively” refer to? (a single percentage, namely 71%, is mentioned herein).

- Table 2: I would suggest moving the percentage symbol (%) in the first (from the second) column of the table in parentheses (wherever applicable), e.g., “AGI incidence per person-year (%)”. Moreover, spell out the AGI abbreviation (either in the title or in a footnote). Finally prefer using “laboratory pathogen testing” in the place of the vaguer “laboratory perming test for pathogens”

- L174-178: please revise to “The estimated cases in the surveillance area during the 12-month study 1,349 cases (95% CI…) of salmonellosis and 3,408 cases (95% CI…) of V. parahaemolyticus infection (Table 3). Considering the population of the surveillance area, the annual incidence estimated by the model developed herein was 101 (95% CI…) cases for salmonellosis abd 256 (95% CI…) cases for V. parahaemolyticus infection per 100,000 population”

- Table 3: Revise the title to “Estimated health burden of non-typhoidal salmonellosis and Vibrio parahaemolyticus infection in Shanghai, east Chine, 2010-2011. Also make the following changes:

1.  Non-typhoidal Salmonella enterica (in 1^st column)

2. Estimated foodborne illness cases per 100,000 population (95% CI) (in 4^th and 6^th column)

3. Reported foodborne illness outbreak cases per 100,000 population (in 7^th column)

General comment: avoid using the general term “illness” and try to be consistent and specific by using the term “foodborne illness”; also choose whether you prefer to use “illness” or “disease” and be consistent throughout the manuscript.

- L184: correct to “from a population survey”

- L184-185: revise to “…surveillance, the burden of foodborne gastroenteritis in Shanghai was estimated to be 13,310…”

- L187: revise to “This indicates that AGI caused by these two pathogens poses a substantial burden…”

- L197: revise to “…as determined from a literature review…”

- L210: what about the distinction between outbreak and sporadic cases? Is this possible based on the analysis performed in the present study? I think that a pertinent comment would add value to the Discussion section of the manuscript.

- L215: revise to “…the China National Center…”

- L218” revise to “…estimating the burden…”

- L223-226: please consider revising to “In order to more accurately determine and prioritize food safety issue in China, and to evaluate and quantify the burden of foodborne diseases outbreaks, it is necessary…

- L241-245: please revise to “In conclusion, the estimated large number of salmonellosis and V. parahaemolyticus infection cases occurring every year in the surveillance area, indicates that these two pathogens pose a substantial health burden in Shanghai, east China, After considering the differences among distinct pathogens, these methods can also be applied in a similar manner to assess the burden of additional foodborne pathogens”

- L246: change “infection” to “infections”

- L248: revise to “…in order to provide improved data support…”

- References: please cross-check references with regard to accuracy and conformance to the PLOS ONE format/style

- Figure 2: correct the legends’ text to “Non-typhoidal Salmonella enterica” and “Vibrio parahaemolyticus” 

Please submit your revised manuscript by Oct 08 2020 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Alexandra Lianou, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

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Comments to the Author

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Reviewer #1: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

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Reviewer #1: Yes

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Reviewer #1: Yes

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5. Review Comments to the Author

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Reviewer #1: 1. The Introduction provides justification for conducting a national health burden assessment but does not explain why a local (Shanghai) health burden assessment was conducted. Please explain why a local and not a national health burden assessment was conducted and why Salmonella and Vibrio parahaemolyticus were selected for the assessment.

2. What is the difference between a primary, secondary, and tertiary hospital? Other readers may have similar questions. Therefore, it might be a good idea to include the answer to this question in the manuscript.

3. Is the testing sensitivity the same as the false negative rate? It seems that a range from 50 to 100% is not realistic because no test is perfect and a test with such a low sensitivity of 50% would not be used. It would be a good idea to better explain the basis for these estimates of uncertainty.

4. When I multiply the most likely values for M1, M2, M3, and M4 for the pert distributions in Table 1, I get 51 but the text says the overall multiplier is 71. Why are these values not similar? Other readers may have the same question. Perhaps it would be good to explain in more detail how 71 and its 95% CI were obtained.

5. It is my understanding, based on human feeding trials (McCullough & Eisele, 1951a, 1951b, 1951c, 1951d), that an infection occurs when a patient is shedding the pathogen but not showing symptoms of disease, whereas an illness occurs when a patient is shedding the pathogen and showing symptoms of the disease. In the present study, the incidence of people showing symptoms of gastrointestinal disease was a basis for the calculation of health burden. Thus, the health burden assessment was for illness and not infection. Yet, throughout the paper both terms are used interchangeably, which is a bit confusing. To do a health burden assessment for infection, data would be needed for the incidence of people that test positive for the pathogen but do not show symptoms of illness. That kind of data was not collected in the present study. Thus, I think that it is not appropriate to talk about a health burden assessment for infection when it is actually a health burden assessment for illness.

6. The sentence starting on line 153 seems to be missing its beginning. Thus, its meaning is not clear. Please clarify this sentence.

7. When a person is exposed to a foodborne pathogen, their peak response falls on a continuum from no infection to infection (asymptomatic) to illness (symptomatic) to severe illness (hospital) to death. Where the peak response falls on this continuum depends on the outcome of the interaction between the pathogen, host, and food (disease triangle). Consequently, if two communities had the same illness rate but one community had more high-risk individuals, the illness rate would be a poor indicator of health burden because the severity of illness would higher in the community with more high-risk individuals. Therefore, I think the current manuscript could be improved by estimating a health burden that takes severity of illness into account.

8. Overall, I think this is a very good paper that will be a good addition to the scientific literature. My comments are mainly suggestions that if adopted could improve the manuscript. My main suggestions are to justify conducting a local health burden assessment, to focus the health burden assessment on illness and not infection, and to consider severity of illness in the prediction of health burden.

I hope this review is helpful,

References

McCullough, N. B., & Eisele, C. W. (1951a). Experimental human salmonellosis. I. Pathogenicity of strains of Salmonella meleagridis and Salmonella anatum obtained from spray-dried whole egg. Journal of Infectious Disease, 88, 278-289.

McCullough, N. B., & Eisele, C. W. (1951b). Experimental human salmonellosis. III. Pathogenicity of strains of Salmonella newport, Salmonella derby, and Salmonella bareilly obtained from spray-dried whole egg. Journal of Infectious Disease, 89, 209-213.

McCullough, N. B., & Eisele, C. W. (1951c). Experimental human salmonellosis. IV. Pathogenicity of strains of Salmonella pullorum obtained from spray-dried whole egg. Journal of Infectious Disease, 89, 259-265.

McCullough, N. B., & Eisele, C. W. (1951d). Experimental human salmonellosis: II. Immunity studies following experimental illness with Salmonella meleagridis and Salmonella anatum. Journal of Immunology, 66, 595-608.

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Reviewer #1: No

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The Human Health Burden of non-typhoidal Salmonella enterica and Vibrio parahaemolyticus Foodborne Gastroenteritis in Shanghai, East China

PONE-D-20-22153R1

Dear Dr. Chen,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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Kind regards,

Alexandra Lianou, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

All comments raised have been sufficiently addressed in the revised manuscript.

Reviewers' comments: