Association between the proportion of laparoscopic approaches for digestive surgeries and the incidence of consequent surgical site infections, 2009–2019: A retrospective observational study based on national surveillance data in Japan

Toshiki Kajihara; Koji Yahara; Aki Hirabayashi; Yumiko Hosaka; Norikazu Kitamura; Motoyuki Sugai; Keigo Shibayama

doi:10.1371/journal.pone.0281838

Peer Review History

Original SubmissionAugust 30, 2022
19 Sep 2022 Decision Letter - Takehiko Hanaki, Editor PONE-D-22-24040Association between the proportion of laparoscopic approaches for digestive surgeries and the incidence of consequent surgical site infections, 2009-2019: A retrospective observational study based on national surveillance data PLOS ONE Dear Dr. Toshiki Kajihara, 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. ============================== Please submit your revised manuscript by Nov 03 2022 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. 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Additional Editor Comments: Dear Dr. Toshiki Kajihara: Thank you very much for allowing PLOS ONE team to see your submission entitled "Association between the proportion of laparoscopic approaches for digestive surgeries and the incidence of consequent surgical site infections, 2009-2019: A retrospective observational study based on national surveillance data". We have now reviewed your submission and our view is that some major revisions are required before we can consider it for publication. This email is to invite you to respond to the reviewers comments attached below, and to revise your submission accordingly. We appreciate that these revisions will take some time and effort on your part, but we are confident that they will improve the quality and impact of your submission. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Partly Reviewer #2: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: I Don't Know ****** 3. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 4. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: This is a large register-based study on surgical site infection (SSI) rate diagnosed in hospitals in Japan from 2009-2019. The study also report on the rate of laparoscopic procedures separately for this period. However, the study does not report the SSI rate after laparoscopic procedures. The study would benefit from a more detailed and transparent method section e.g. using RECORD statement, and maybe also other analyses depending on the data available. Major comments: 1. It is not clear if your manuscript is reported in accordance with a reporting guideline, and the study design is not definitely clear to me. But I presume that RECCORD (https://www.equator-network.org/reporting-guidelines/record/) that is for register-based studies using routinely-collected health data would suit your manuscript and increase the transparency of your reporting. 2. Your outcome is somewhat unclear. You state that CDC definition was used, however, being unfamiliar with the JANIS SSI, it is unclear to me if the physicians at the hospital confirm SSI according to CDC when they report an SSI in JANIS SSI. Furthermore, it seems that JANIS SSI only include hospital data – what about the SSI treated at the patients private physician? Thus, I presume that you report the rate of SSI diagnosed in hospitals, correct? 3. Your study covers 10 years of data. It is evident from your data that the laparoscopic procedures increase tremendously during this period. However, could other factor contribute to decrease of SSIs? Patient-related factors, co-interventions such as prophylactic or empiric antibiotic treatment or others? There is no baseline information on the population receiving these procedures and the development in these over time. All your analyses are unadjusted. But this could be a limitation of your results. Please address in the result section or limitations section in the discussion depending on the data you have available. 4. If data are available you could address 3) by differentiating the types of procedures e.g. by using the surgical codes, if these are available. Minor comments: 1. Introduction: Please ad a reference and be more specific than overall complications for the following sentence: “Laparoscopic techniques have been increasingly used in digestive surgeries, leading to fewer postoperative complications.” 2. Methods: Please add more information on the setting. You write “More hospitals progressively joined the JANIS SSI 91 section, and the program included 785 hospitals in 2019.” But what are the total number of hospitals in Japan, in other words how well is your coverage? 3. Methods: Are the procedures submitted to JANIS SSI reported by the hospital og linked by another nationwide register? How where they reported – as procedure codes? Which where used? 4. Methods: Who submit the outcome, SSI, according to CDC definitions? Hospitals, private practitioners? Is the outcome validated to follow CDC definitions? 5. Methods: How was a laparoscopic procedure confirmed? 6. Discussion: Please add a limitations section to your discussion. Reviewer #2: The authors retrospectively investigated SSI ratio using their surveillance system form 2009 to 2019. I think several points should be addressed as follows. How to collect all data from the hospitals participating in the surveillance？ EDC system? CRF by each year? Please represent SSI data showing the differences of superficial, deep or organ. How much was the SSI rate of upper GI surgery? Rec shows high SSI rate, because of the stoma creation, or the incidence coming from the perineal wound? The data of the difference between emergency and scheduled surgeries should be described. What does the table 2 mean? Odd ratio was compared to that of the start year? The trend, fashion and equipment are changing year by year. It is difficult to compare the risk ratio. The caption of the figure axis should be rewritten (e.g., "proportion" should be "Proportion" in Figure 2 and with high DPI figures). ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Siv Fonnes Reviewer #2: No ******** [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". 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Revision 1
21 Dec 2022 Author Response Point-by-point responses to the reviewers’ comments Dear Editor and Reviewers: Thank you for your efforts in reviewing our manuscript and for your helpful comments and suggestions. We have revised the manuscript in accordance with your comments. We hope that the changes, indicated in red font in the revised manuscript, reflect your suggestions and are satisfactory. Our point-by-point responses to your queries are given below. Reviewer #1: This is a large register-based study on surgical site infection (SSI) rate diagnosed in hospitals in Japan from 2009-2019. The study also report on the rate of laparoscopic procedures separately for this period. However, the study does not report the SSI rate after laparoscopic procedures. The study would benefit from a more detailed and transparent method section e.g. using RECORD statement, and maybe also other analyses depending on the data available. Major comments: 1. It is not clear if your manuscript is reported in accordance with a reporting guideline, and the study design is not definitely clear to me. But I presume that RECCORD (https://www.equator-network.org/reporting-guidelines/record/) that is for register-based studies using routinely-collected health data would suit your manuscript and increase the transparency of your reporting. Response: We checked the RECORD guidelines that include 22 checklists. To satisfy the checklists, we have added the following three parts to the revised manuscript: (1) “in Japan” to the title for Item No. 1 in the checklist. (2) “The SSI surveillance in JANIS is conducted using the definition of the US National Nosocomial Infections Surveillance System (NNIS), with some modifications. It is comparable to other international SSI surveillances, such as the OP-KISS of Germany [14] and the National Healthcare Safety Network of the United States of America [15]. Surgeons in hospitals performed procedures and diagnosed SSI cases and reported the data to JANIS according to NHSN Operative Procedure Categories using ICD-9-CM code (https://janis.mhlw.go.jp/section/master/surgicaltechniquecode_ver2.1_20121220.xls).” and “These included 188 of 408 (46.1%) hospitals with over 500 beds, 464 of 2,174 (21.3%) hospitals with 200–499 beds and 133 of 5790 (2.3%) hospitals with less than 200 beds.” to the Materials and Methods section for Item No. 6. (Page 6, Lines 97-104) (3) “This study has several limitations. First, the JANIS is a voluntary surveillance, which inevitably has selection biases, although approximately 10% of all hospitals in Japan were covered in the surveillance. Second, we did not collect data of patients’ conditions, such as the type of antiseptic agent used or presence of bacterial colonization, because JANIS SSI section is designed to focus on SSIs. Third, the data collected in the surveillance have limitations regarding complexity of surgical procedures such as difficulty of the procedure, surgical technique used, and types of diseases that led to the surgery.” to the Discussion section for the Item No. 19. (Page 19, lines 311-317) 2. Your outcome is somewhat unclear. You state that CDC definition was used, however, being unfamiliar with the JANIS SSI, it is unclear to me if the physicians at the hospital confirm SSI according to CDC when they report an SSI in JANIS SSI. Response: Thank you for your comment. Regarding the definition, we have removed the statement of CDC definition, and instead added “The SSI surveillance in JANIS is conducted using the definition of the US National Nosocomial Infections Surveillance System (NNIS), with some modifications. It is comparable to other international SSI surveillances, such as the OP-KISS of Germany and the National Healthcare Safety Network of the United States of America.” to the Materials and Methods section. (Page 6, Lines 97-101) Most procedures of APPY, CHOL, SB, COLO, REC (defined by ICD-9-CM code) were performed in hospitals in Japan. Surgeons are usually responsible for the course of procedures in Japan. This is because JANIS collects the data from hospitals. The surgeons and/or infection control nurses in their hospitals validated the data. The surgeons at the hospital can confirm SSI because most patients are usually followed up at outpatient clinics in the hospitals in Japan. We have thus added “Most patients were followed up at outpatient clinics in their hospitals in Japan. The surgeon is usually responsible for the course of procedures in Japan. This is because JANIS collects the data from hospitals. The surgeons and/or infection control nurses in the hospitals validated the data and submitted the data every six months.” to the Materials and Methods section. (Page 7, Lines 108-111) Furthermore, it seems that JANIS SSI only include hospital data – what about the SSI treated at the patients private physician? Thus, I presume that you report the rate of SSI diagnosed in hospitals, correct? Response: Correct, they report the rate of SSI diagnosed in hospitals. The SSI treated by the patients’ private physician is not reported in JANIS SSI, although surgeons at hospitals can confirm SSI because most patients were usually followed up at outpatient clinics in the hospitals in Japan. 3. Your study covers 10 years of data. It is evident from your data that the laparoscopic procedures increase tremendously during this period. However, could other factor contribute to decrease of SSIs? Patient-related factors, co-interventions such as prophylactic or empiric antibiotic treatment or others? There is no baseline information on the population receiving these procedures and the development in these over time. All your analyses are unadjusted. But this could be a limitation of your results. Please address in the result section or limitations section in the discussion depending on the data you have available. Response: Thank you for your comment. We could not collect patients’ disease stage, comorbidities, antibiotic use, etc., as JANIS was designed to monitor prevalence of nosocomial infections. We have added sentences regarding the limitation to the Discussion, as detailed in the response to your last comment below. 4. If data are available you could address 3) by differentiating the types of procedures e.g. by using the surgical codes, if these are available. Response: We use ICD-9-CM code for case definition. But we collected only NHSN Operative Procedure Categories, such as COLO, REC, etc. Therefore, we cannot analyze using the type of procedures for this study. Minor comments: 1. Introduction: Please ad a reference and be more specific than overall complications for the following sentence: “Laparoscopic techniques have been increasingly used in digestive surgeries, leading to fewer postoperative complications.” Response: We have added “In a systematic review, Buia et al showed that the advantage of the procedure was minimizing trauma to the abdominal wall compared with open surgery [5]. It was based on another systematic review, that pain intensity on VAS scale was reduced on day one and wound infections were decreased in laparoscopic procedures for suspected appendicitis [6]. Laparoscopic procedures accelerated the recovery after colon surgery by decreasing pain and duration of hospital stay [7]. Van der Pas et al. reported that patients in the laparoscopic colectomy group lost less blood, bowel function returned sooner, and hospital stay was shorter than those in the open surgery group in a randomised, phase 3 trial [8].” to the Introduction. (Pages 4-5, Lines 63-72) 2. Methods: Please add more information on the setting. You write “More hospitals progressively joined the JANIS SSI 91 section, and the program included 785 hospitals in 2019.” But what are the total number of hospitals in Japan, in other words how well is your coverage? Response: We have added “These included 188 of 408 (46.1%) hospitals with over 500 beds, 464 of 2,174 (21.3%) hospitals with 200–499 beds and 133 of 5790 (2.3%) hospitals with less than 200 beds.” in the Materials and methods section. (Page 6-7, Lines 106-108) 3. Methods: Are the procedures submitted to JANIS SSI reported by the hospital og linked by another nationwide register? How where they reported – as procedure codes? Which where used? Response: Yes, the procedures submitted to JANIS were reported by the hospital as procedure codes. We have added “Surgeons in hospitals performed procedures and diagnosed SSI cases and reported the data to JANIS according to NHSN Operative Procedure Categories using ICD-9-CM code (https://janis.mhlw.go.jp/section/master/surgicaltechniquecode_ver2.1_20121220.xls).” to the Materials and Methods section. (Page 6, Lines 101-104) 4. Methods: Who submit the outcome, SSI, according to CDC definitions? Hospitals, private practitioners? Is the outcome validated to follow CDC definitions? Response: Surgeons in hospitals performed procedures and diagnosed SSI cases and submitted the data. We have added “Most patients were followed up at outpatient clinics in their hospitals in Japan. The surgeon is usually responsible for the course of procedures in Japan. This is because JANIS collect the data from hospitals. The surgeons and/or infection control nurses in their hospitals validated the data and submitted the data every six months.” to the Materials and Methods section. (Page 7, Lines 108-111) 5. Methods: How was a laparoscopic procedure confirmed? Response: If laparoscopy was used in a patient’s procedure, a surgeon and/or an infection control nurse entered it in the dataset. We have added “The surgeons and/or infection control nurses in their hospitals validated the data and submitted the data every six months.” to the Materials and Methods section. (Page 7, Lines 110-111) 6. Discussion: Please add a limitations section to your discussion. Response: Thank you for your comment. We have added “This study has several limitations. First, the JANIS is a voluntary surveillance, which inevitably has selection biases, although approximately 10% of all hospitals in Japan were covered in the surveillance. Second, we could not collect data of patients’ conditions, such as the type of antiseptic agent used or presence of bacterial colonization, because JANIS SSI section is designed to focus on SSIs. Third, the data collected in the surveillance have limitations regarding complexity of surgical procedures such as difficulty of the procedure, surgical technique used, and types of diseases that led to the surgery.” in the Discussion section. (Page 19, Lines 311-317) Reviewer #2: The authors retrospectively investigated SSI ratio using their surveillance system form 2009 to 2019. I think several points should be addressed as follows. How to collect all data from the hospitals participating in the surveillance？ EDC system? CRF by each year? Response: We collected JANIS SSI division data from the hospitals using original EDC system every six months. Please represent SSI data showing the differences of superficial, deep or organ. Response: Thank you very much. We have added the type of SSI at the core hospitals in table 1. How much was the SSI rate of upper GI surgery? Response: We have added the data of upper GI surgeries in Table S1, and have added the following text “On the contrary, the proportion of SSIs of upper gastrointestinal surgeries was variable (Figure S1). Gastric surgeries were divided into total gastrectomy (GAST-T), Distal gastrectomy (GAST-D) and other gastric surgeries (GAST-O) in 2012. GAST-D and GAST-O showed a similar trend of increase in laparoscopic procedures associated with decrease in SSI rate, compared to the five digestive surgeries (odds ratio of the 10% increase in the proportion of laparoscopic procedures for the surgical site infection rates was 0.941 [95% CI: 0.914-0.968, p<0.001] and 0.947 [95%CI: 0.918-0.977, p<0.001], respectively). On the other hand, GAST-T and esophageal surgeries (ESOP) did not show the trend (p-value=0.606 and 0.614). The number of procedures of GAST-T was continuously decreasing from 2,798 in 2012 to 1,570 in 2019. The number of laparoscopic procedures of GAST-T was also decreasing from 1,182 in 2012 to 704 in 2019. It was because of the development of the technique of gastrointestinal endoscopy, which led to detection and treatment of gastric diseases earlier. With respect to ESOP, the number of procedures of ESOP in 13 of 23 core participating hospitals was under 10 in 2019. Marker SR et al. reported that the outcome of esophageal surgeries in high surgical volume hospitals was better than that in low surgical volume hospitals, which suggests that surgeons' experience was required to reduce post-operative problems.” in the discussion section. (Page 17, lines 270-286) Rec shows high SSI rate, because of the stoma creation, or the incidence coming from the perineal wound? Response: The high SSI rate in REC is not because of the stoma creation in both laparoscopic and open procedures according to the following data: among laparoscopic procedures, the percentage of superficial and deep incisional infections of rectal surgeries was less than that of organ and space infections (34.9% and 7.7%, compared with 57.3%, added to Table 1). Among open procedures, although the percentage of superficial incisional infections (62.8%) was higher than that of the others (11.7% for deep incisional infections and 25.5% for organ and space infections), breakdown of the superficial incisional infections into superficial Incisional Primary (SIP) and Secondary (SIS) confirmed that 124 of 131 superficial incision infections were SIP, indicating that most SSIs in REC procedures are not related to stoma creation. We have added “Regarding REC, the percentage of superficial and deep incisional infections in laparoscopic procedures in 2019 was lower than that of open procedures (34.9, 7.7% vs 62.8, 11.7%). This showed that the SSIs were not related to the part of stoma. There was no difference between laparoscopic and open procedures in the percentage of type of SSIs of the other four surgeries.” to the Discussion section. (Page 16, lines 262-266) ” The data of the difference between emergency and scheduled surgeries should be described. Response: Thank you for your comment. We have added Table S2 and the following sentences to the Discussion: “We have shown the data of emergency and scheduled surgeries in 2019 in Table S2. The proportion of laparoscopic procedures of emergency vs scheduled five digestive surgeries were 71.3% vs 84.0%, 76.7% vs 84.0%, 17.8% vs 25.1%, 23.9% vs 64.8%, and 28.2% vs 76.3%, for each of the five procedures, respectively, which indicates that the proportion of laparoscopic procedures of emergency surgeries was significantly higher than that of scheduled surgeries. This result suggests that surgeons tend to choose open procedures in emergency situations. The rate of SSI of both laparoscopic and open procedures of emergency surgeries was higher than that of scheduled surgeries except for open procedures of APPY.” (Pages 18, 294-302) What does the table 2 mean? Odd ratio was compared to that of the start year? The trend, fashion and equipment are changing year by year. It is difficult to compare the risk ratio. Response: The odds ratio was not compared to that of the start year. Rather, it estimates how the odds (p/(1-p) where p is probability of occurrence of SSI) changes when there is a 10% increase in the proportion of laparoscopic procedures, compared to that when there is no increase in it, across 11 years. The caption of the figure axis should be rewritten (e.g., "proportion" should be "Proportion" in Figure 2 and with high DPI figures). Response: Thank you for your comment. We have corrected it to “Proportion” from “proportion”. Attachments Attachment Submitted filename: ResponsetoReviewersComments_v2.0.docx https://doi.org/10.1371/journal.pone.0281838.r002
1 Feb 2023 Decision Letter - Takehiko Hanaki, Editor Association between the proportion of laparoscopic approaches for digestive surgeries and the incidence of consequent surgical site infections, 2009-2019: A retrospective observational study based on national surveillance data in Japan PONE-D-22-24040R1 Dear Dr. Kajihara, 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. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. 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If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #1: All comments have been addressed Reviewer #2: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #1: Yes Reviewer #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes ****** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #1: Yes Reviewer #2: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #1: Yes Reviewer #2: Yes ****** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: Thank you for addressing all comments and for writing a more transparent method section and for adding a limitation section in the discussion section. Reviewer #2: (No Response) ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Siv Fonnes Reviewer #2: No ******** https://doi.org/10.1371/journal.pone.0281838.r003
Formally Accepted
9 Feb 2023 Acceptance Letter - Takehiko Hanaki, Editor PONE-D-22-24040R1 Association between the proportion of laparoscopic approaches for digestive surgeries and the incidence of consequent surgical site infections, 2009-2019: A retrospective observational study based on national surveillance data in Japan Dear Dr. Kajihara: I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. If we can help with anything else, please email us at plosone@plos.org. Thank you for submitting your work to PLOS ONE and supporting open access. Kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. Takehiko Hanaki Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0281838.r004

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