Knowledge,Perception,and Educational Status of Antimicrobial Resistance Among Chinese Medical Students

Abstract

Aims:

Antimicrobial resistance (AMR) has become a serious global health issue, which is exacerbated globally by the overuse and misuse of antimicrobial drugs. Improving awareness and understanding AMR through effective communication, education, and training is recommended by the World Health Organization as one of five key strategies of tackling AMR. This study explores the knowledge and perception of AMR, its educational status, and any potential associations among Chinese medical students.

Results:

A total of 2,616 students from four medical schools across China were enrolled in this study. Data reveal a general lack of knowledge about both antibiotic use and AMR that is related to school type, major, and clinical experience. Students' AMR knowledge was associated with their perception of issues in this area as well as their educational status. Results of a linear regression model show that learning about AMR in class (OR: 1.85, 95% CI: 1.47–2.23) and the hours spent learning about these issues (OR: 0.11, 95% CI: 0.07–0.15) were both positively associated with enhanced knowledge.

Conclusions:

A significant lack of knowledge about AMR is found among Chinese medical students, associated with their perception of these issues. The status of AMR education in medical schools nationally is therefore less than satisfactory and positively correlated with general knowledge of this issue.

Introduction

Antimicrobial resistance (AMR) refers to the phenomenon by which microorganisms are able to change and become resistant to medicines during exposure to antimicrobial drugs.¹ Although AMR develops naturally over time, this process is accelerated by the overuse and misuse of antimicrobial drugs.¹ AMR has become a serious global public health issue, especially in China. According to one survey, the Chinese population consumed 150 times more antibiotics than that in the United Kingdom in 2013; indeed, national antibiotic use in humans is ∼23 times that of Europe.²

Education is one effective approach for promoting AMR mitigation. In 2015, the WHO issued the Global Action Plan on Antimicrobial Resistance, which advocated tackling AMR.³ The first objective of this plan was to “improve awareness and understanding of antimicrobial resistance through effective communication, education and training.” The Chinese National Action Plan to Contain Antimicrobial Resistance (2016–2020) also encouraged medical schools to strengthen training in the rational use of antibiotics,⁴ in accord with WHO advice, which advocates making AMR-related training a significant component of professional health sector education.³

Significant lack in AMR knowledge including a poor level of awareness among medical students is seen globally. One survey of students attending an urban medical school in the northern United States revealed an unmet need for both education and feedback regarding the prescription of antimicrobial drugs.⁵ Another study that assessed knowledge, attitudes, and perceptions (KAP) of the AMR issue among final-year students at seven European medical schools showed that some students' perceptions of this problem were inaccurate, and that education in schools is insufficient.⁶ It is noteworthy, however, that the response rates of these two studies were low (30% and 35%), an issue that raises concerns about nonresponse bias. A survey on attitudes and perceptions toward antimicrobial use and resistance among fourth-year medical students from five teaching hospitals in central China had a relatively high response rate (84%) but also revealed unsatisfactory levels of knowledge (3.78 correct answers of 11 questions on average). In this case, medical students felt that they needed an enhanced level of education about AMR and the use of antimicrobial drugs.⁷ These three studies highlight the fact that AMR education is generally poor in medical schools. A limited number of studies have been conducted to date on the causes for this lack of education as well as the association between its status and AMR knowledge. Consequently, limited data are available for educators to enhance knowledge of AMR issues.

The aim of this study was to discover the level of knowledge and perceptions among medical students in four medical schools in China to both antimicrobial use and AMR issues, as well as to identify key factors and their levels associated with these variables.

Materials and Methods

Ethics

The research was conducted in accordance with the Declaration of Helsinki as well as with national and institutional standards. No personal identity information was collected because this analysis was website based, with the statement of the study purpose and the data usage shown in the first line of the questionnaire. Informed consent was obtained before questionnaire survey initiation.

Study design and participants

This analysis comprised of a cross-sectional, questionnaire-based study, which aimed to evaluate perceptions and knowledge about antimicrobial use and AMR as well as the content and the quantity of information related to these issues delivered in four medical schools across China. A multistage sampling method was used; we initially selected four medical schools based on their geographic locations and levels. Thus, according to Chinese university level rankings, two medical schools were “Double First-Class” (hereafter “key universities”), while another two were not (hereafter “non-key universities”). Key universities, identified as having the potential to become world class in light of the Chinese government's Double First-Class initiatives, were considered to be leading ones nationwide in terms of education, research, resources, and reputation.⁸ The four medical schools considered here are located in Beijing, Guangzhou, Yinchuan, and Dalian, respectively. Students in graduating classes in each case (i.e., in their final year of study) majoring in clinical medicine, public health, pharmacy, nursing, and other majors were recruited using a cluster sampling method. Our questionnaires reached a total of 2,722 students; of them 2,616 were returned, with a response rate of 96.1%. A total of 2,603 questionnaires were recognized as valid, and so were enrolled for further statistical analysis. Questionnaires with invalid or omitted answers were excluded.

Data collection

Data were collected from participants through Chinese e-questionnaires using Wenjuanxing (Wenjuanxing Tech Co. Ltd, Changsha, China), widely used online questionnaire platform.

The questionnaire used here was designed based on the one used previously by the WHO Western Pacific Regional Office and encompassed AMR knowledge, attitudes, and perceptions.⁹ This initial questionnaire version was piloted for validity in the Philippines, and some alterations were then made after initial data analysis. We adopted this validated questionnaire and modified it, so that it could be more easily understandable for Chinese students and fit into a local context. Three sections were also added to this questionnaire to collect sociodemographic information, a universities' AMR education, and the demand among undergraduate students for education in this area.

A total of 27 questions were employed, encompassing three facets of AMR knowledge, including the use of antibiotics (6 items), AMR mechanisms (9 items), and factors associated with exacerbating the issue of AMR (12 items). Respondents gained one point for each correct answer, and zero points for wrong answers or for responding “I don't know.” A Likert scale was then used to assess perceptions of AMR, including seven questions: (1) “The issue of AMR is closely linked to my major”; (2) “The problem of antimicrobial abuse in China is now severe”; (3) “AMR is a severe issue in my community”; (4) “AMR is a severe issue in my hospital”; (5) “AMR is a severe problem in China”; (6) “AMR is a severe problem globally”; and (7) “I'm very eager to gain AMR-related knowledge.” To assess AMR educational status, we also asked respondents whether they had ever learned about this issue in classes or lectures and reported the accumulated number of hours they had been exposed to AMR education to obtain a quantitative measure. Our questions also encompassed the demands expressed by students for AMR knowledge, including whether they felt they had had sufficient courses about this issue in college and any reasons they felt their knowledge was limited.

Statistics

Data were analyzed using the software SAS version 9.4 (SAS Institute, Cary, NC) having been tested for normality beforehand. Values were presented as means ± standard deviation (SD) or percentages, and were further tested using independent t- and chi-square tests, respectively. A linear regression model was used to explore associations between AMR knowledge score and perception as well as to explore associations between college educational status and AMR knowledge adjusted for school type, major, and clinical experience. A p-value of <0.05 was considered statistically significant in all analyses.

Results

Basic respondent information

The basic information collected from all respondents is summarized in Table 1.

Table 1.

Basic Information for Participants

Characteristics	N (%)
Gender
Male	912 (35.0)
Female	1,691 (65.0)
Location
Guangzhou	616 (23.7)
Beijing	586 (22.5)
Yinchuan	659 (25.3)
Dalian	742 (28.5)
Level of university^a
Key university	1,202 (46.2)
Non-key university	1,401 (53.8)
Major
Clinical medicine	1,098 (42.2)
Pharmacy	299 (11.5)
Public health	320 (12.3)
Nursing	461 (17.7)
Other	425 (16.3)
Has clinical experience
Yes	2,332 (89.6)
No	271 (10.4)

Categorized by the Ministry of Education of China, the key universities are more prestigious and receive a higher level of sponsorship from government.

Antimicrobial use, AMR knowledge, and associated factors

The average AMR knowledge score recovered in this study was 18.7 ± 3.6, encompassing a high score of 27 and a low score of zero. Average scores (total scores) for antibiotic use, AMR mechanism, and factors exacerbating AMR were 3.8 ± 1.6, 5.0 ± 1.6, and 9.9 ± 2.0, respectively. These correspond with total scores of six, nine, and 12, respectively.

Results show that school type, major, and clinical experience are all related to variations in AMR knowledge. Respondents from key universities had higher average scores than those from non-key institutions; the former group also outscored respondents from non-key universities on the use of antibiotics and AMR mechanisms, while respondents from the latter group performed better with regard to knowledge of factors exacerbating AMR. Individuals majoring in clinical medicine had highest total scores, whereas those majoring in nursing scored lowest. Respondents majoring in clinical medicine scored highest for all three variables with the exception of factors exacerbating AMR; it is noteworthy that respondents majoring in nursing scored highest in this category. Respondents who had experienced clinical practice scored higher than those who had no clinical practice, both overall and in each aspect individually. There was no significant variance in total scores between sexes of respondents; male students outscored females in aspects of the use of antibiotics and AMR mechanisms, whereas females outscored males on the factors exacerbating AMR (Table 2).

Table 2.

Difference of Antimicrobial Resistance Knowledge Scores Among Medical Students with Different Characteristics (Mean ± SD)

	Scores of AMR knowledge
	Total	p	The use of antibiotics	p	Mechanism of AMR	p	Factors exacerbating AMR	p
Gender
Male	18.9 ± 3.7	0.118	3.9 ± 1.6	<0.001	5.2 ± 1.6	<0.001	9.7 ± 2.1	<0.001
Female	18.6 ± 3.5	0.118	3.7 ± 1.6	<0.001	4.9 ± 1.6	<0.001	10.0 ± 1.9	<0.001
School type^a
Key university	19.8 ± 3.2	<0.001	4.3 ± 1.5	<0.001	5.7 ± 1.5	<0.001	9.8 ± 1.8	0.001
Non-key university	17.7 ± 3.6	<0.001	3.3 ± 1.6	<0.001	4.3 ± 1.5	<0.001	10.1 ± 2.2	0.001
Major
Clinical medicine	19.6 ± 3.1	<0.001	4.1 ± 1.5	<0.001	5.4 ± 1.5	<0.001	10.0 ± 1.7	<0.001
Public health	18.3 ± 3.5		3.8 ± 1.6		4.8 ± 1.5		9.6 ± 2.2
Pharmacy	18.2 ± 3.8		3.5 ± 1.7		4.8 ± 1.6		9.9 ± 2.2
Nursing	17.5 ± 3.6		3.1 ± 1.5		4.2 ± 1.6		10.2 ± 2.1
Other	18.4 ± 3.9		3.8 ± 1.8		4.9 ± 1.7		9.8 ± 2.1
Clinical practice
Yes	18.8 ± 3.5	<0.001	3.8 ± 1.6	0.162	5.0 ± 1.6	0.011	10.0 ± 1.9	<0.001
No	17.8 ± 4.0	<0.001	3.6 ± 1.7	0.162	4.7 ± 1.6	0.011	9.4 ± 2.5	<0.001

Categorized by the Ministry of Education of China, the key universities are more prestigious and receive a higher level of sponsorship from government.

AMR, antimicrobial resistance.

AMR perception and its association with knowledge score

The data assembled here reveal that most respondents do perceive AMR to be a severe problem within China, although fewer consider this to be a significant global issue (Table 3). The data presented in Table 4 summarize the results of an adjusted logistic model for the statement “The AMR issue is closely linked to my major”; these results show that AMR knowledge scores were positively associated in this case with the choices “Very close” and “Close,” and were negatively associated with the choice of “Not close.” AMR knowledge scores were positively associated with the negative choice in the case of the statement “The problem of antimicrobial abuse in China has reached a severe degree,” while in terms of the four statements concerning whether the AMR issue is a severe problem, knowledge scores were negatively associated with the choice of “No” and “Don't know.” In terms of the statement “I'm very eager to learn about AMR,” a negative correlation was only seen between AMR knowledge scores and the choice of “No” or “Fair.”

Table 3.

The Perception of Antimicrobial Resistance-Related Issues Among College Students [N (%)]

Statement	AMR perception
Statement	Agree	Disagree	Don't know
The AMR issue is closely linked to my major^a	1,525 (58.6)	1,078 (41.4)	/
The problem of antimicrobial abuse has reached a severe degree	2,084 (80.1)	519 (19.9)	/
The AMR issue is a severe problem in my community	1,827 (70.2)	392 (15.0)	384 (14.8)
The AMR issue is a severe problem in my hospital	2,283 (87.7)	141 (5.4)	179 (6.9)
The AMR issue is a severe problem in China	2,500 (96.0)	30 (1.2)	73 (2.8)
The AMR issue is a severe problem globally	2,159 (82.9)	62 (2.4)	382 (14.7)
I'm very eager to learn about AMR	1,744 (67.0)	859 (33.0)	/

For the statement “The AMR issue is closely linked to my major,” Agree = Very close/Close, Disagree = Fair/Not close/No relation. For the statement “I'm very eager to learn about AMR,” Agree = Eager, Disagree = Fair/No.

“/” indicates N/A (not applicable).

Table 4.

Linear Regression Models on Antimicrobial Resistance Knowledge Score and Perception of Antimicrobial Resistance

Statement	β	SE	95% CI	p
The AMR issue is closely linked to my major
Very close	1.17	0.21	(0.75–1.59)	<0.001
Close	0.71	0.21	(0.30–1.13)	<0.001
Fair	Ref.
Not close	−1.64	0.36	(−2.35 to −0.94)	<0.001
No relation	−1.23	0.66	(−2.53 to 0.07)	0.0638
Don't know	−1.54	0.18	(−1.90 to −1.18)	<0.001
The problem of antimicrobial abuse in China has reached a severe stage
Yes	0.26	0.02	(0.22–0.29)	<0.001
No	Ref.
The AMR issue is a severe problem in my community
Yes	Ref.
No	−0.74	0.18	(−1.10 to −0.38)	<0.001
The AMR issue is a severe problem in my hospitals
Yes	0.00
No	−1.31	0.28	(−1.87 to −0.75)	<0.001
Don't know	−1.93	0.25	(−2.43 to −1.43)	<0.001
The AMR issue is a severe problem in China
Yes	Ref.
No	−3.37	0.59	(−4.53 to −2.21)	<0.001
Don't know	−3.21	0.38	(−3.96 to −2.46)	<0.001
The AMR issue is a severe problem globally
Yes	Ref.
No	−1.43	0.33	(−2.08 to −0.77)	<0.001
Don't know	−1.12	0.15	(−1.42 to 0.82)	<0.001
I am very eager to learn more on AMR-related topics/issues
Eager	Ref.
Fair	−0.54	0.14	(−0.81 to −0.27)	<0.001
No	−5.72	0.49	(−6.69 to −4.76)	<0.001

Adjusted for school type, major, and clinical experience.

In-class AMR educational status

The bulk of respondents surveyed here reported that they have learned about AMR in class. Respondents majoring in pharmacy reported being taught about this issue for the longest time, while those majoring in nursing were taught for the shortest time. Respondents from key universities were taught about AMR for longer than their counterparts from non-key institutions (Table 5).

Table 5.

Education Status of Antimicrobial Resistance Issues in Medical Students with Different Majors and School Types [N (%) or Mean ± SD]

	Majors					School types		Total
	Clinical	Pharmacy	Public health	Nursing	Other	Key university	Non-key university	Total
Ever learning about AMR in college	1,002 (91.3)	299 (93.4)	246 (82.8)	360 (78.1)	363 (85.4)	1,085 (90.4)	1,185 (84.6)	2,270 (87.3)
Total hours learning about AMR in class	3.5 ± 3.3	4.0 ± 3.1	2.7 ± 2.9	2.6 ± 2.8	3.0 ± 3.2	3.7 ± 3.2	2.9 ± 3.1	3.2 ± 3.2

Among students who had learned about AMR issues, less than half thought that they had taken enough courses in this area. The top three responses to reasons knowledge about AMR is limited were “AMR isn't a key subject in class,” “AMR isn't a key subject in exams,” and “We don't have enough class periods” (Table 6). The linear regression model summarized in Table 7 (corrected for school type, major, and clinical experience) reveals that AMR knowledge scores are associated with having ever learned about AMR in college and total hours of in-class learning on AMR.

Table 6.

Education Status of Antimicrobial Resistance Issues Among Students Who Have Learned About Antimicrobial Resistance Issues [N (%) or Mean ± SD]

	Majors					School type		Total
	Clinical	Pharmacy	Public health	Nursing	Other	Key university	Non-key university	Total
Having enough courses in college to receive sufficient knowledge	435 (43.4)	150 (50.2)	122 (49.6)	185 (51.4)	177 (48.8)	478 (44.1)	591 (49.9)	1,069 (47.1)
Reasons for lack of AMR knowledge
No interest	292 (29.1)	98 (32.8)	83 (33.7)	145 (40.3)	110 (30.3)	329 (30.3)	399 (33.7)	728 (32.1)
AMR isn't the key subject in class	596 (59.5)	141 (47.1)	151 (61.4)	211 (58.6)	206 (56.8)	662 (61.0)	643 (54.3)	1,305 (57.5)
AMR isn't the key subject in examinations	561 (56.0)	129 (43.1)	145 (58.9)	183 (50.8)	193 (53.2)	590 (54.4)	621 (52.4)	1,211 (53.4)
Don't have enough class periods	460 (45.9)	122 (40.8)	111 (45.1)	175 (48.6)	159 (43.8)	45.7 (42.2)	570 (48.1)	1,027 (45.2)
Teachers' lack of capacity	89 (8.9)	10 (3.3)	17 (6.9)	25 (6.9)	24 (6.6)	66 (6.08)	99 (8.35)	165 (7.3)

Table 7.

Linear Regression Models for Antimicrobial Resistance Education Status in College and Antimicrobial Resistance Knowledge

Statement	β	SE	95% CI	p
Ever learned in college
Yes	1.85	0.19	(1.47–2.23)	<0.001
No	Ref.
Self-perception of whether had enough courses in college
Yes	−0.03	0.14	(−0.30 to 0.24)	0.827
No	Ref.
Total hours of learning AMR in class	0.11	0.02	(0.07–0.15)	<0.0001

Adjusted for school type, major, and clinical experience.

Discussion

This study is one of the few to assess the knowledge and perceptions of AMR issues among Chinese medical students. The students enrolled in this study came from four different medical schools and had different educational levels. Results reveal a general lack of knowledge about both AMR and antimicrobial use among Chinese medical students; specifically, school type, major, and clinical experience are all factors associated with AMR knowledge and antimicrobial use. It is also clear that both perception and AMR educational status are significantly associated with knowledge of this issue and antimicrobial use. Results show that an understanding of this situation as well as more specific guidance and suggestions should be provided to further enhance AMR-related education within China and will also generalize experiences globally. This study is also the first of its kind to make comparisons between students from different majors across China. Considering the special status of medical education nationally such that students majoring in public health and nursing are educated together with clinical medical students in the first stage of undergraduate education, a period that mainly emphasizes basic medical science,^10,11 comparisons might lead to new findings.

The study identified a clear lack of AMR-related knowledge among Chinese medical students. It is the case that these students will have had more direct access to correct AMR knowledge compared with their nonmedical counterparts; thus, AMR-related knowledge of medical students should be better than that found among the general public.^12,13 The majority of the students surveyed here were aware of AMR and although they tended to have a general awareness of issues in this area, a significant knowledge gap was present in terms of specific knowledge. Previous studies targeting Chinese medical students have also indicated a knowledge gap in antibiotic use and prescription, AMR mechanisms, and the underlying factors exacerbating the issue of AMR.^14–16 Here we show that students' knowledge about the use of antibiotics and AMR mechanisms indeed remains relatively poor, while their knowledge regarding factors exacerbating resistance seems enhanced. This knowledge gap is negatively associated with key universities, clinical medicine majors, and clinical experience. This association with key universities might be attributed to the fact that faculties at these institutions tend to be more highly regarded⁸; lecturers at these universities are more likely to realize the importance of AMR and therefore give additional lectures on this topics in their classes. We therefore suggest that students at these key universities might be better at learning and absorbing information about AMR, and will thus have more knowledge in this area.

Students majoring in clinical medicine might also have more chance to be exposed to AMR-related issues such as medication and prescription, and will therefore develop higher knowledge scores.¹⁷ Indeed, as respondents with clinical experience tend to have higher AMR scores than those who do not, this form of training seems conducive for enhancing knowledge in this area. The results of this study also show that students majoring in nursing tend to have the lowest levels of understanding about AMR-related issues, even though nursing practitioners and nurses play important roles in promoting rational antibiotic use.^18,19 Nurses also advocate and encourage patients to participate in public health promotions,²⁰ and so AMR education should be improved for students pursuing these professional qualifications in this area.

The data presented here show that in terms of student's perceptions of AMR-related issues, >40% of respondents felt that these were not linked to their majors and nearly one third actually considered it unnecessary to learn about the issue of AMR. This contrasts with a previous study that reported that >90% of respondents (149 of 161) considered knowledge about antimicrobials to be important to their career²¹; this discrepancy highlights the fact that AMR awareness issues still need to be promoted and advocated among Chinese medical students. The results of this study also show that AMR-related knowledge is positively associated with perception, including the major subjects studied by students and their perception that this issue is a severe problem. This apparent association between knowledge and perception has been explored in numerous previous studies,^5,22 and is in accordance with the knowledge–attitude–practice model, which posited that knowledge can be related to attitude and be further associated with behavioral changes.^23,24 To facilitate final behavioral changes with regard to AMR-related issues among medical students, it will be important to improve both knowledge and perception (which influence each other) of this issue.

The role of education and training in promoting knowledge about AMR has also been shown to be effective, at least on the basis of WHO guidelines.¹ However, when reviewing the content of curricula for undergraduates in different majors, the term “antibiotic resistance” was actually not specifically included at any of the four universities. Education about AMR, how much content and level, is left largely up to individual lecturers who deliver courses. Indeed, in terms of rates of education in this area, ∼90% of students reported receiving information on this topic in college, greater than reports of 80% and 60% in the DR Congo and France.^25,26 Examined in detail, AMR education in college remains limited both in quantity and in quality; taking the first perspective, just 3.2 hours in the first 5 years of medical education were spent on average on AMR. Considering the poor knowledge of respondents in general about AMR, it seems that current education and curricula remain insufficient to provide students with adequate knowledge and skills. This is especially the case for students in non-key schools where nearly hour less is devoted to learning about these issues compared with students at key universities; this result might partly explain why students in non-key school tended to have relatively poor AMR-related knowledge. This is also the case in the United States and Europe where two surveys of students also reported a dearth of AMR education.^6,27 It therefore seems clear that a lack of AMR education is not just a problem in China but globally.

Finally, in terms of quality, issues to do with AMR are generally not considered core in university classes or examinations; ∼30% of the students surveyed here reported that AMR education failed to rouse their interest. Education in this areas in college has been found to be related to that of medical students overall; this result suggests that medical students, as future health care and public health workers, must be well informed about AMR issues at the college level to augment and change their knowledge and perception. Education in this area with regard to AMR in medical schools, especially non-key institutions, must be designed to extend both its duration and promote content. As “AMR isn't a key subject in exams” was the reason selected most often to explain student's lack of knowledge in this area, the inclusion of more content within the curricula (including in examinations) might be one effective way to raise awareness of these issues.

There are a number of limitations inherent to this study. First, despite the fact that we selected four medical schools at different levels across disparate regions of China, sampling in four cities results in a lack of national data representativeness. Second, the cross-sectional nature of this study impedes the exploration of causality, the recall basis, and residual confounders might exist. Further interventional studies should be conducted to discover the neglected part of AMR and propose feasible reformations/solutions. Third, we collected information about AMR educational status through questionnaire rather than by using observational methods, including observation-based courses or with reference to course outlines. This kind of self-reporting could result in bias. However, collecting information from the subjects themselves might also reflect how students receive AMR education from their own perspectives.

The results of this study highlight a significant lack of AMR knowledge among Chinese medical students, which is associated with AMR perception. Moreover, AMR education status in medical school is less than satisfactory and is positively related with AMR knowledge. The results presented here imply that it is prudent to incorporate AMR-related education in medical college to enhance students' AMR knowledge, as well as to further promote students' AMR perception. Further interventions should be implemented to generally promote the awareness of students to AMR-related issues.

Footnotes

Acknowledgments

We thank the WHO Western Pacific Regional Office for providing us with the initial questionnaire used here to assess the knowledge, attitudes, and practices of medical students regarding AMR and for assisting us with our revisions to create a Chinese version. Huaqin Cheng, Yangmu Huang, and Paiyi Zhu all provided helpful suggestions that aided the design of this study.

Disclosure Statement

Y.W. received funding from the UK Foreign & Commonwealth Office's China Prosperity Fund. All other authors have no funding to declare.

Funding Information

This study was funded by the UK Foreign & Commonwealth Office's China Prosperity Fund Programme (16SS35).

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