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. 2021 Feb 27;21:234. doi: 10.1186/s12879-021-05921-2

Nationwide multicenter questionnaire surveys on countermeasures against antimicrobial resistance and infections in hospitals

Jung-ho Shin 1, Seiko Mizuno 1, Takuya Okuno 1, Hisashi Itoshima 1, Noriko Sasaki 1, Susumu Kunisawa 1, Mitsuo Kaku 2, Makiko Yoshida 3, Yoshiaki Gu 4, Daiichi Morii 5, Keigo Shibayama 6, Norio Ohmagari 7, Yuichi Imanaka 1,
PMCID: PMC7912490  PMID: 33639873

Abstract

Background

The goals of the National Action Plan on Antimicrobial Resistance (AMR) of Japan include “implementing appropriate infection prevention and control” and “appropriate use of antimicrobials,” which are relevant to healthcare facilities. Specifically, linking efforts between existing infection control teams and antimicrobial stewardship programs was suggested to be important. Previous studies reported that human resources, such as full-time equivalents of infection control practitioners, were related to improvements in antimicrobial stewardship.

Methods

We posted questionnaires to all teaching hospitals (n = 1017) regarding hospital countermeasures against AMR and infections. To evaluate changes over time, surveys were conducted twice (1st survey: Nov 2016, 2nd survey: Feb 2018). A latent transition analysis (LTA) was performed to identify latent statuses, which refer to underlying subgroups of hospitals, and effects of the number of members in infection control teams per bed on being in the better statuses.

Results

The number of valid responses was 678 (response rate, 66.7%) for the 1st survey and 559 (55.0%) for the 2nd survey. More than 99% of participating hospitals had infection control teams, with differences in activity among hospitals. Roughly 70% had their own intervention criteria for antibiotics therapies, whereas only about 60 and 50% had criteria established for the use of anti-methicillin-resistant Staphylococcus aureus antibiotics and broad-spectrum antibiotics, respectively. Only 50 and 40% of hospitals conducted surveillance of catheter-associated urinary tract infections and ventilator-associated pneumonia, respectively. Less than 50% of hospitals used maximal barrier precautions for central line catheter insertion.

The LTA identified five latent statuses. The membership probability of the most favorable status in the 2nd study period was slightly increased from the 1st study period (23.6 to 25.3%). However, the increase in the least favorable status was higher (26.3 to 31.8%). Results of the LTA did not support a relationship between increasing the number of infection control practitioners per bed, which is reportedly related to improvements in antimicrobial stewardship, and being in more favorable latent statuses.

Conclusions

Our results suggest the need for more comprehensive antimicrobial stewardship programs and increased surveillance activities for healthcare-associated infections to improve antimicrobial stewardship and infection control in hospitals.

Supplementary Information

The online version contains supplementary material available at 10.1186/s12879-021-05921-2.

Keywords: Antimicrobial resistance, Antimicrobial stewardship, Healthcare-associated infection, Infection control, Surveillance

Introduction

The World Health Assembly adopted the Global Action Plan on Antimicrobial Resistance (AMR) in May 2015 [1]. In Japan, the National Action Plan on Antimicrobial Resistance was adopted in April 2016 and included two goals [2], “implementing appropriate infection prevention and control” and “appropriate use of antimicrobials.” These goals are of particular relevance to healthcare facilities in terms of preventing the spread of antimicrobial-resistant organisms. Specifically, at the field level, linking efforts between existing infection control team (ICT) and antimicrobial stewardship (AMS) programs was suggested to be important [2].

Previous studies reported that human resources (expressed as full-time equivalents (FTEs) of infection control practitioners) and FTE-to-bed ratios were related to improvements in AMS [35]. However, the definition of improvement varied from study to study. For example, one study used an increase in the number of implemented AMS programs [3] to evaluate the performance of AMS, while another study examined the effectiveness of each program [4].

The purpose of the present study was two-fold: to report the results of nationwide multicenter questionnaire surveys on countermeasures against AMR and infections in Japanese teaching hospitals, and to identify latent statuses, which might imply underlying subgroups of hospitals with similar achievement levels of AMS, and examine the effects of FTE-to-bed ratios of ICT members on the latent statuses.

Methods

We posted questionnaires to all teaching hospitals in Japan (n = 1017 as of 2015). To examine changes over a period of roughly 1 year, surveys were conducted twice in November 2016 and February 2018 (see the English translation of the questionnaires in Additional file 1). No intervention was provided by our study team between the two surveys. The contents of the questionnaire included basic information, such as the number of beds (1st survey only), questions divided into sections 1 to 12 for countermeasures against AMR based from a previous study [6] and a guide published by the Japanese Ministry of Health, Labour and Welfare [7], and section 13 for results of bacterial cultures, as follows: 1. Organizational structure for nosocomial infection control; 2. Activities of ICT; 3. Preventive measures by the route of infections; 4. Maintenance of medical equipment; 5. Standard precautions; 6. Ward; 7. Intensive care unit (ICU); 8. Operating room; 9. Prevention of postoperative infections; 10. Management of food hygiene in hospitals; 11. Management of medical waste; 12. Cleaning, disinfection, and sterilization of instruments; and 13. Antimicrobial-resistant organisms. The questions were answered (1) numerically (e.g., number of physicians) or by choosing (2) either “yes” or “no” or (3) one among three to five options in order (e.g., “in approximately 100%/80%/50%/20%/0% of relevant cases”).

We analyzed valid responses, which included hospital information to link the 1st and 2nd surveys. We excluded duplicate responses to the same survey by the same hospital. Answers to questions in sections 1 to 12 are presented as medians and interquartile ranges, calculated after excluding missing values. For single-choice questions, we presented the proportions of “yes” or the most favorable option (e.g., “approximately 100% of relevant cases”). For these types of questions, we created a “missing” category. Student’s t-tests or Satterthwaite tests were used for continuous variables, and Cochran-Mantel-Haenszel tests for categorical variables, to compare results from the 1st and 2nd surveys.

The answers to questions in section 13 were the results of surveillance in 2015 for the 1st survey and 2016 for the 2nd survey, which were 1 year before each survey. We calculated the proportions of isolated microorganisms and antimicrobial-resistant organisms for each hospital that responded to both surveys. Wilcoxon signed-rank tests were used, assuming that the results from the 1st and 2nd surveys regarding section 13 were paired data.

To study the achievement level for AMS programs of hospitals, we performed a latent transition analysis (LTA), which is a longitudinal extension of latent class analysis [8]. Latent class analysis identifies underlying subgroups in a population, but the characteristics of these underlying subgroups are hard to observe directly; these are indicated by several observed variables [8]. While latent class analysis identifies underlying (unobservable) subgroups within a population as “classes,” LTA refers to the subgroups as “statuses” to reflect the fact that membership in the subgroups can change over time [8]. In this study, we performed LTA using data from hospitals that responded to both surveys, and time periods 1 and 2 for LTA were defined as those of 1st and 2nd surveys, respectively. Questions for which the proportion of the most favorable answer was less than 80% in the 2nd survey were used to classify hospitals into subgroups, latent statuses, with similar sets of answers to these questions. We excluded questions regarding handwashing sinks in ICUs, for which the proportion of the most favorable answer was less than 80%, given the lack of established guidelines. We also reduced the multiple categories in each question to two (most favorable/others) to improve the precision of estimates [9]. FTEs of ICT members were selected as a covariate that might affect the membership probabilities for time period 1. We determined the number of statuses by considering interpretability and fit statistics, and presented the fit statistics, status membership probabilities, transition probabilities, item-response probabilities, and estimated odds ratios for covariates. The domains, which consisted of several questions, were determined empirically according to the LTA results.

SAS® software version 9.4 (SAS Institute Inc., Cary, NC, USA) was used for all analyses, and PROC LTA (version 1.3.2) was used for the LTA [10]. A two-tailed significance level of 0.05 was used for all tests.

Results

Among 1017 teaching hospitals, 683 and 563 hospitals responded to the 1st and 2nd surveys, respectively. The numbers of valid responses were 678 for the 1st survey (response rate: 66.7%) and 559 for the 2nd survey (response rate: 55.0%) after excluding duplicated responses and those with missing hospital information. The number of hospitals that responded to both surveys was 437 (response rate: 43.0%).

The mean number of hospital beds was 434 (median, 389: 675 responses). Table 1 presents the results of the two surveys for all hospitals with valid responses and hospitals that responded to both surveys (see Tables S1 and S2 in Additional file 2 for more details). More than 99% of hospitals reported having active ICTs, with a median of 10 to 11 ICT members. Both crude numbers and FTEs of ICT members did not differ significantly between the 1st and 2nd surveys.

Table 1.

Results of the 1st and 2nd questionnaire surveys

All hospitals with valid responses Hospitals that responded to both surveys
Question 1st survey
(n = 678)
2nd survey
(n = 559)
P* 1st survey
(n = 437)
2nd survey
(n = 437)
P*
Number of staff
 Physician (full-time) 75 (47–128) 80 (48.5–137.5) 0.237 80 (50–140) 81 (50–137) 0.805
 Nurse (full-time) 336 (235–528.5) 360 (251–561) 0.066 368 (246–543) 371 (251–561) 0.629
 Laboratory technologist (full-time) 23 (16–34) 24 (17–36) 0.107 24 (17–36.5) 24.5 (17–37) 0.819
 Pharmacist (full-time) 19 (13–28) 20 (14–30) 0.066 19 (14–28) 20 (14–30) 0.360
 Dietitian 5 (4–8) 5 (4–8) 0.097 5 (4–8) 6 (4–8) 0.370
 Administrative staff 52 (32–86) 53.5 (32–87) 0.611 56 (33–87) 56 (33–89) 0.718
 Registered ICD (MD or PhD) 2 (1–4) 3 (2–4) 0.139 3 (2–4) 3 (2–4) 0.322
We have an active ICT. 674 (99.4%) 557 (99.6%) 0.843 436 (99.8%) 435 (99.5%) 0.607
Number of ICT member, crude 10 (8–16) 11 (7–16) 0.103 11 (8–17) 11 (7–17) 0.530
 Physician 2.5 (2–4) 3 (2–4) 0.153 3 (2–4) 3 (2–4) 0.576
 Nurse 2 (2–4) 2 (2–4) 0.488 2 (2–4) 2 (2–4) 0.757
 Pharmacist 2 (1–2) 2 (1–2) 0.255 2 (1–2) 2 (1–2) 0.242
 Laboratory technologist 2 (1–2) 2 (1–2) 0.230 2 (1–2) 2 (1–2) 0.709
 Dietitian 0 (0–0) 0 (0–0) 0.910 0 (0–0) 0 (0–0) 0.948
 Administrative staff 1 (0–2) 1 (0–1) 0.969 1 (0–2) 1 (1–2) 0.926
Number of ICT member, full-time equivalent 2.8 (1.3–4.3) 2.8 (1.8–4) 0.717 2.8 (1.6–4.3) 2.8 (1.8–4.1) 0.920
 Physician 2.5 (2–4) 3 (2–4) 0.951 3 (2–4) 3 (2–4) 0.830
 Nurse 0.8 (0.8–1.3) 0.8 (0.8–1.3) 0.675 0.8 (0.8–1.3) 0.8 (0.8–1.3) 0.693
 Pharmacist 0.5 (0–0.8) 0.5 (0–0.8) 0.725 0.5 (0–0.8) 0.5 (0–0.65) 0.531
 Laboratory technologist 0.5 (0–0.8) 0.5 (0–0.5) 0.953 0.5 (0–1) 0.5 (0–0.8) 0.931
 Dietitian 0 (0–0) 0 (0–0) 0.068 0 (0–0) 0 (0–0) 0.067
 Administrative staff 0 (0–0.5) 0 (0–0.5) 0.839 0 (0–0.5) 0 (0–0.5) 0.524
FTE per 100 beds 0.7 (0.4–1.0) 0.7 (0.4–1.0) 0.918 0.7 (0.4–1.0) 0.7 (0.4–1.0) 0.918
We performed bacterial culture, identification, and susceptibility tests basically in our hospital. 542 (79.9%) 466 (83.4%) 0.301 355 (81.2%) 367 (84.0%) 0.362
We participate in JANIS programs. 647 (95.4%) 548 (98.0%) 0.025 426 (97.5%) 432 (98.9%) 0.219
 Clinical laboratory division 636 (93.8%) 536 (95.9%) 0.103 421 (96.3%) 422 (96.6%) 0.855
 Antimicrobial-resistant bacterial infection division 311 (45.9%) 288 (51.5%) 0.048 228 (52.2%) 235 (53.8%) 0.635
 Surgical site infection division 366 (54.0%) 324 (58.0%) 0.161 249 (57.0%) 259 (59.3%) 0.493
 Intensive care unit division 116 (17.1%) 88 (15.7%) 0.519 80 (18.3%) 74 (16.9%) 0.595
 Neonatal intensive care unit division 74 (10.9%) 64 (11.4%) 0.766 56 (12.8%) 51 (11.7%) 0.606
1. Organizational structure for nosocomial infection control
 The head of our hospital attends ICC almost every time. 576 (85.0%) 473 (84.6%) 0.027 379 (86.7%) 369 (84.4%) 0.018
 We have a comprehensive hospital infection control manual that can be used all around our hospital. 677 (99.9%) 559 (100.0%) 0.364 437 (100.0%) 437 (100.0%)
 We hold a workshop regarding countermeasures against hospital infection more than once a year. 677 (99.9%) 559 (100.0%) 0.364 437 (100.0%) 437 (100.0%)
 We have tools, such as the intranet and bulletin boards, to inform our staff of hospital infection-related matters. 671 (99.0%) 556 (99.5%) 0.397 434 (99.3%) 436 (99.8%) 0.317
2. Activities of ICT
 We hold a regular ICT meeting. 628 (92.6%) 534 (95.5%) 0.042 410 (93.8%) 416 (95.2%) 0.353
 We provide consultation as an activity of the ICT. 633 (93.4%) 516 (92.3%) 0.274 412 (94.3%) 407 (93.1%) 0.333
We have an AST (a member can work for both ICT and AST). 542 (79.9%) 373 (66.7%) <.001 355 (81.2%) 305 (69.8%) <.001
 We monitor the uses of antibiotics to assure their propriety. 652 (96.2%) 544 (97.3%) 0.476 420 (96.1%) 431 (98.6%) 0.064
 We intervene to assure appropriate uses of antibiotics. 631 (93.1%) 527 (94.3%) 0.177 410 (93.8%) 415 (95.0%) 0.317
We have established criteria of interventions, such as their administration duration and selection, for patients administered antibiotics. 466 (68.7%) 399 (71.4%) 0.589 304 (69.6%) 310 (70.9%) 0.691
We have criteria for the uses of anti-MRSA antibiotics. 433 (63.9%) 361 (64.6%) 0.964 267 (61.1%) 278 (63.6%) 0.594
 We record the used amount of anti-MRSA antibiotics. 667 (98.4%) 554 (99.1%) 0.508 432 (98.9%) 432 (98.9%) 0.788
 We have a reporting system (1st survey: “registration system”) for the use of anti-MRSA antibiotics. 390 (57.5%) 542 (97.0%) <.001 259 (59.3%) 425 (97.3%) <.001
We have a preauthorization and/or restriction system for the use of anti-MRSA antibiotics. 321 (47.3%) 208 (37.2%) <.001 206 (47.1%) 169 (38.7%) 0.035
We have criteria for the uses of broad-spectrum antibiotics such as carbapenems. 355 (52.4%) 287 (51.3%) 0.369 217 (49.7%) 224 (51.3%) 0.305
 We have a reporting system (1st survey: “registration system”) for the use of broad-spectrum antibiotics. 391 (57.7%) 530 (94.8%) <.001 251 (57.4%) 415 (95.0%) <.001
We have a preauthorization and/or restriction system for the use of broad-spectrum antibiotics. 258 (38.1%) 131 (23.4%) <.001 157 (35.9%) 111 (25.4%) 0.003
 We record the used amount of broad-spectrum antibiotics. 667 (98.4%) 550 (98.4%) 0.935 429 (98.2%) 431 (98.6%) 0.777
 We have a reference system, such as the intranet of a booklet, for the antibiogram. 562 (82.9%) 482 (86.2%) 0.238 371 (84.9%) 383 (87.6%) 0.499
We performed TDM for basically all cases. 423 (62.4%) 362 (64.8%) 0.273 273 (62.5%) 287 (65.7%) 0.193
 We record the vaccination proportion of employees who are HBsAg-negative. 581 (85.7%) 485 (86.8%) 0.415 369 (84.4%) 378 (86.5%) 0.096
 We perform IGRAs for employees who are in contact with tuberculosis patients. 616 (90.9%) 503 (90.0%) 0.772 404 (92.4%) 397 (90.8%) 0.556
We record employees’ immunization statuses for measles, rubella, chickenpox, and mumps (2nd survey: “for all of measles, rubella, chickenpox, and mumps”). 572 (84.4%) 340 (60.8%) <.001 371 (84.9%) 273 (62.5%) <.001
 We have a manual and a reporting system of needle punctures and sharp object injuries. 678 (100.0%) 559 (100.0%) 437 (100.0%) 437 (100.0%)
Needle puncture and sharp object injuries are reported to a relevant department, such as ICT. 463 (68.3%) 391 (69.9%) 0.177 301 (68.9%) 307 (70.3%) 0.408
ICT and/or ICPs check the number of isolated antimicrobial-resistant organisms and other microorganisms that are relevant to infection control on a daily basis 436 (64.3%) 357 (63.9%) 0.409 281 (64.3%) 286 (65.4%) 0.110
 ICT and/or ICPs record the species and trends of isolated microorganisms on a type-of-sample and a ward-by-ward basis. 636 (93.8%) 530 (94.8%) 0.142 413 (94.5%) 414 (94.7%) 0.257
 We have a direct and fast reporting system to the doctor-in-charge, such as e-mail and telephone, when microorganisms are isolated from a sample that is supposed to be aseptic (e.g., a blood sample). 653 (96.3%) 550 (98.4%) 0.068 422 (96.6%) 431 (98.6%) 0.088
We perform surveillance for surgical site infections. 510 (75.2%) 446 (79.8%) 0.038 334 (76.4%) 355 (81.2%) 0.119
We perform surveillance for ventilator-associated pneumonia. 238 (35.1%) 219 (39.2%) 0.254 162 (37.1%) 175 (40.0%) 0.422
We perform surveillance for central line-associated bloodstream infections. 508 (74.9%) 440 (78.7%) 0.190 330 (75.5%) 351 (80.3%) 0.088
We perform surveillance for catheter-associated urinary tract infections. 345 (50.9%) 310 (55.5%) 0.275 224 (51.3%) 258 (59.0%) 0.063
We perform active surveillance cultures. 334 (49.3%) 273 (48.8%) 0.905 228 (52.2%) 219 (50.1%) 0.831
 We have an established manual for outbreaks. 637 (94.0%) 534 (95.5%) 0.370 417 (95.4%) 419 (95.9%) 0.947
3. Preventive measures by the route of infections
 We have a manual for the outbreak of tuberculosis. 675 (99.6%) 559 (100.0%) 0.290 435 (99.5%) 437 (100.0%) 0.368
 We have a manual for the outbreak of measles. 623 (91.9%) 513 (91.8%) 0.175 398 (91.1%) 401 (91.8%) 0.222
 We have a manual for the outbreak of chickenpox. 612 (90.3%) 502 (89.8%) 0.161 393 (89.9%) 395 (90.4%) 0.222
 We provide N95 masks at the outpatient emergency department and other outpatient departments. 664 (97.9%) 551 (98.6%) 0.648 429 (98.2%) 432 (98.9%) 0.661
 We put a surgical mask on patients with suspected airborne infections while transporting. 677 (99.9%) 558 (99.8%) 0.361 436 (99.8%) 436 (99.8%) 0.368
 Wearing an N95 mask is mandatory while entering the ward of a patient with suspected tuberculosis. 676 (99.7%) 558 (99.8%) 0.680 436 (99.8%) 436 (99.8%) 1.000
 We have a manual for the outbreak of influenza. 674 (99.4%) 555 (99.3%) 0.736 435 (99.5%) 435 (99.5%) 1.000
 Wearing a surgical mask while entering the ward of a patient with a droplet infection is instructed by a manual. 671 (99.0%) 558 (99.8%) 0.152 432 (98.9%) 437 (100.0%) 0.081
 We provide surgical masks in the wards of patients with droplet infections. 589 (86.9%) 486 (86.9%) 0.716 374 (85.6%) 380 (87.0%) 0.336
 We have a manual for cases in which MRSA is isolated from a patient. 667 (98.4%) 551 (98.6%) 0.661 429 (98.2%) 433 (99.1%) 0.400
 Wearing disposable gloves and a gown is mandatory while entering the ward of a patient with suspected contagious diseases. 618 (91.2%) 508 (90.9%) 0.966 399 (91.3%) 401 (91.8%) 0.793
 We provide alcohol-based hand sanitizers in all wards except for some special wards, such as the psychiatric ward. 657 (96.9%) 546 (97.7%) 0.525 427 (97.7%) 428 (97.9%) 0.607
 We provide alcohol-based hand sanitizers in all outpatient departments. 624 (92.0%) 529 (94.6%) 0.151 404 (92.4%) 415 (95.0%) 0.224
4. Maintenance of medical equipment
 We adopt closed urine drainage systems. 644 (95.0%) 544 (97.3%) 0.112 419 (95.9%) 426 (97.5%) 0.412
We do not change catheters without blockages or infections regularly. 512 (75.5%) 418 (74.8%) 0.619 322 (73.7%) 323 (73.9%) 0.904
 We have a manual for the maintenance of ventilators. 583 (86.0%) 499 (89.3%) 0.221 376 (86.0%) 388 (88.8%) 0.424
 We adopt closed tracheal suction systems. 568 (83.8%) 476 (85.2%) 0.799 382 (87.4%) 381 (87.2%) 0.931
 We use sterile water for humidifiers. 658 (97.1%) 544 (97.3%) 0.120 428 (97.9%) 426 (97.5%) 0.311
We perform regular oral cleansing for intubated patients in approximately 100% of relevant cases. 524 (77.3%) 425 (76.0%) 0.225 340 (77.8%) 333 (76.2%) 0.226
 We have a manual for the maintenance of central line catheters. 654 (96.5%) 542 (97.0%) 0.108 418 (95.7%) 425 (97.3%) 0.294
We insert central line catheters under maximal barrier precautions in approximately 100% of relevant cases. 254 (37.5%) 210 (37.6%) 0.086 163 (37.3%) 167 (38.2%) 0.150
We prepare intravenous hyperalimentation admixtures on clean benches in approximately 100% of relevant cases. 277 (40.9%) 225 (40.3%) 0.415 182 (41.6%) 175 (40.0%) 0.335
 We use transparent dressings on the sites of catheter insertion to make them easy to inspect visually in approximately 100% of relevant cases. 563 (83.0%) 486 (86.9%) 0.224 357 (81.7%) 380 (87.0%) 0.112
5. Standard precautions
We instruct new employees in hand hygiene by practical training sessions for all professions. 361 (53.2%) 290 (51.9%) 0.955 229 (52.4%) 222 (50.8%) 0.700
 We evaluate the implementation of hand hygiene instructions of all wards at least once a year. 603 (88.9%) 523 (93.6%) 0.018 389 (89.0%) 411 (94.1%) 0.028
We instruct new employees of all professions how to put on and remove PPE. 532 (78.5%) 426 (76.2%) 0.638 347 (79.4%) 330 (75.5%) 0.255
We instruct all employees in PPE by practical training sessions every year. 135 (19.9%) 107 (19.1%) 0.281 85 (19.5%) 80 (18.3%) 0.126
6. Wards
 We provide hand sanitizers at the entrance of all wards. 656 (96.8%) 544 (97.3%) 0.407 426 (97.5%) 426 (97.5%) 0.593
 All medical devices (e.g., thermometers, stethoscopes) of single isolation rooms are patient-dedicated. 653 (96.3%) 529 (94.6%) 0.152 423 (96.8%) 414 (94.7%) 0.174
 We check expiry dates of sterilized medical devices daily. 638 (94.1%) 528 (94.5%) 0.949 415 (95.0%) 416 (95.2%) 0.987
 We check expiry dates of unused medications. 664 (97.9%) 551 (98.6%) 0.516 429 (98.2%) 430 (98.4%) 0.741
 We have established guides for the expiry dates of opened medications. 649 (95.7%) 542 (97.0%) 0.285 421 (96.3%) 422 (96.6%) 0.514
 All wards have at least one infection control link nurse. 669 (98.7%) 547 (97.9%) 0.535 432 (98.9%) 429 (98.2%) 0.571
7. ICU
Medical professions do not change their shoes while entering ICU. 548 (80.8%) 425 (76.0%) 0.123 363 (83.1%) 335 (76.7%) 0.037
Medical professions are not recommended to wear gowns while entering ICU. 548 (80.8%) 425 (76.0%) 0.116 361 (82.6%) 337 (77.1%) 0.128
We have handwashing sinks at the entrance of ICU. 397 (58.6%) 320 (57.2%) 0.085 259 (59.3%) 248 (56.8%) 0.107
We provide hand sanitizers at the entrance of ICU. 549 (81.0%) 426 (76.2%) 0.114 362 (82.8%) 338 (77.3%) 0.095
We advise the patients’ families to use hand sanitizers or wash hands before and after entering ICU. 545 (80.4%) 428 (76.6%) 0.016 362 (82.8%) 339 (77.6%) 0.066
8. Operating room
 We do not change stretchers while entering operating rooms. 518 (76.4%) 449 (80.3%) 0.046 334 (76.4%) 352 (80.5%) 0.211
Medical professions do not change their shoes while entering operating rooms. 395 (58.3%) 356 (63.7%) 0.102 263 (60.2%) 285 (65.2%) 0.299
 We do not provide sticky mats at the entrance of operation rooms. 670 (98.8%) 552 (98.7%) 0.734 434 (99.3%) 432 (98.9%) 0.715
 We have established standards of surgical hand preparation. 579 (85.4%) 492 (88.0%) 0.331 375 (85.8%) 381 (87.2%) 0.553
 We do not recommend the use of a brush for surgical hand preparation. 641 (94.5%) 534 (95.5%) 0.424 419 (95.9%) 420 (96.1%) 0.867
9. Prevention of postoperative infections
 We use electric clippers or depilatory creams for patients who need to remove their hair before surgery in all departments. 651 (96.0%) 532 (95.2%) 0.572 420 (96.1%) 418 (95.7%) 0.271
 We advise patients who can take a shower to take a shower on the night before or the morning of the day of surgery. 638 (94.1%) 526 (94.1%) 0.865 410 (93.8%) 410 (93.8%) 0.478
 We recommend the administration of prophylactic antibiotics 30 min to 1 h before the incision. 640 (94.4%) 522 (93.4%) 0.582 421 (96.3%) 406 (92.9%) 0.710
We have manuals to establish the duration of prophylactic antibiotics administration in all departments. 304 (44.8%) 266 (47.6%) 0.532 188 (43.0%) 214 (49.0%) 0.230
10. Management of food hygiene in hospitals
 We adopt dry kitchen systems for hospital meals. 508 (74.9%) 453 (81.0%) 0.005 330 (75.5%) 356 (81.5%) 0.040
11. Management of medical waste
 We distinguish infectious waste from other waste and store it in a place inaccessible to non-authorized people. 667 (98.4%) 546 (97.7%) 0.667 428 (97.9%) 427 (97.7%) 0.607
12. Cleaning, disinfection, and sterilization of instruments
 We do not pre-clean or pre-disinfect medical devices in wards. 549 (81.0%) 463 (82.8%) 0.526 355 (81.2%) 368 (84.2%) 0.501
 We clean and disinfect endoscopes in accordance with the manuals or check them regularly. 582 (85.8%) 472 (84.4%) 0.498 375 (85.8%) 372 (85.1%) 0.885

ICD Infection control doctor, MD Medical doctor, PhD Doctor of philosophy, ICT Infection control team, JANIS Japan Nosocomial Infections Surveillance, ICC Infection control committee, AST Antimicrobial stewardship team, MRSA Methicillin-resistant Staphylococcus aureus, TDM Therapeutic drug monitoring, HBsAg Hepatitis B surface antigen, IGRA Interferon-gamma release assay, ICP Infection control practitioner, PPE Personal protective equipment, ICU Intensive care unit

Values are presented as medians (interquartile range) for numeric variables and numbers (%) for categorical variables

Questions in bold indicate that the proportion of the most favorable answer was < 80%

*Student’s t-test or Satterthwaite test as appropriate for continuous variables; Cochran-Mantel-Haenszel test for categorical variables

P values in bold indicate P < .05

More than 90% of hospitals had weekly ICT meetings, although proportions of specific activities differed from hospital to hospital (section 2): 79.9% (1st survey) and 66.7% (2nd survey) of hospitals had an antimicrobial stewardship team. More than 90% of hospitals indicated that they monitored and intervened to assure appropriate use of antibiotics, but only 70% had established intervention criteria. The proportions of hospitals with intervention criteria for patients administered anti-methicillin-resistant Staphylococcus aureus (MRSA) antibiotics and carbapenems were approximately 60 and 50%, respectively. The proportions of hospitals that performed surveillance varied by the types of infections: catheter-associated urinary tract infections and ventilator-associated pneumonia were monitored less frequently compared to surgical site infections and central line-associated bloodstream infections.

With regard to the maintenance of medical equipment (section 4), less than 50% of hospitals indicated that they used maximal barrier precautions for central line catheter insertion and prepared intravenous hyperalimentation admixtures on clean benches.

For standard precautions (section 5), approximately 50% of hospitals held practical hand hygiene training sessions for new employees regardless of professions; the remaining hospitals trained new employees of selected professions only. Training regarding personal protective equipment for all new employees was held in about 80% of hospitals, although less than 20% of hospitals held these training sessions every year.

Regarding the ICU (section 7), the proportion of hospitals that answered “yes” to “We have handwashing sinks at the entrance of ICU” was lower than the other questions in this section. Roughly 60% of hospitals had handwashing sinks at the ICU entrance, whereas approximately 80% of hospitals answered “yes” for other questions.

Less than 70% of hospitals responded that their staff members do not change their shoes when entering the operating room, and less than 50% had manuals regarding the duration of prophylactic antibiotics available in all departments (section 8). The proportion was lower than 80% even when hospitals that had manuals in selected departments were included (Tables S1 and S2 in Additional file 2).

Table 2 presents the proportions of isolated microorganisms and antimicrobial-resistant microorganisms. Among antimicrobial-resistant microorganisms, only the proportion of those belonging to the family Enterobacteriaceae decreased in 2016 compared with 2015. The proportions of antimicrobial-resistant Streptococcus pneumoniae and Escherichia coli increased during this period.

Table 2.

Isolation proportions of microorganisms and antimicrobial-resistant microorganisms

Number of hospitals 1st survey (2015) 2nd survey (2016)
Microorganism Mean ±SD Median (IQR) Mean ±SD Median (IQR) P*
Staphylococcus aureus 378 14.4% ±7.7% 13.2% (9.6–17.3%) 15.0% ±7.4% 14.2% (9.7–19.0%) 0.046
 Methicillin-resistant 378 37.8% ±14.3% 34.9% (28.6–43.9%) 37.9% ±13.3% 35.8% (28.6–44.7%) 0.342
  Methicillin-resistant, in a blood sample 378 6.0% ±4.3% 5.1% (3.2–8.1%) 6.8% ±4.9% 6.2% (3.9–8.8%) 0.002
Streptococcus pneumoniae 296 2.1% ±2.3% 1.5% (0.8–2.7%) 1.9% ±2.7% 1.2% (0.7–2.1%) <.001
 Penicillin-resistant 296 22.6% ±21.9% 18.9% (0.3–40.4%) 29.1% ±20.8% 33.3% (5.5–45.5%) <.001
Escherichia coli 298 12.8% ±7.3% 11.8% (8.3–15.7%) 12.6% ±5.9% 11.6% (9.0–15.4%) 0.181
 Fluoroquinolone-resistant 298 27.2% ±11.0% 27.8% (19.7–34.4%) 29.4% ±10.6% 30.0% (22.0–36.4%) <.001
Pseudomonas aeruginosa 299 4.7% ±3.3% 4.1% (2.7–5.8%) 5.2% ±2.9% 4.8% (3.4–6.4%) <.001
 Carbapenem-resistant 299 10.8% ±7.2% 9.8% (6.0–14.8%) 10.8% ±7.1% 10.0% (5.1–15.6%) 0.843
Enterobacteriaceae 279 22.5% ±10.9% 21.2% (15.2–28.0%) 18.6% ±9.3% 17.2% (13.2–22.9%) <.001
 Carbapenem-resistant 279 1.0% ±1.5% 0.5% (0.1–1.4%) 0.9% ±1.7% 0.2% (0.0–0.9%) 0.001

SD Standard deviation, IQR Interquartile range

*Wilcoxon signed-rank test

P values in bold indicate P < .05

Tables 3, 4, 5, 6, 7, and Table S3 and Figure S1 in Additional file 2 show the results of the LTA. Five statutes, from the most favorable (status 1) to the least favorable (status 5), were identified (Table 3). Latent status 4 showed the highest status membership probabilities for both time periods (Table 4). As for transition probabilities, members of statuses 1, 2, 4, and 5 were stable in their status membership (Table 5). On the other hand, members of status 3 showed the lowest probability of remaining in the same status (42.7%, Table 5), with 32.7% moving to status 5 and 14.8% moving to status 4 (Table 5). We assigned five domains according to the item-response probabilities for each question (Tables 36 and Figure S1 in Additional file 2): “antimicrobial stewardship” (domain 1); “surveillance” (domain 2); “medical and hospital equipment” (domain 3); “ICT activities regarding vaccinations and education of employees” (domain 4); and “acknowledgment of updating relevant guidelines” (domain 5). Compared to status 1, status 2 showed lower probabilities of having criteria for anti-MRSA antibiotic use and broad-spectrum antibiotic use, whereas status 3 had lower probabilities of performing surveillance. Status 4 had only one domain (i.e., domain 3) with higher probabilities for questions in it. Status 5 had no domain that showed higher probabilities compared to other statuses. In the analysis using the number of ICT members (FTE per 100 beds) as a covariate, the odds ratio of status 3 versus status 5 was 1.32, whereas odds ratios were 0.55 and 0.61 for statuses 1 and 2 versus status 5, respectively (p = 0.027, Table 7).

Table 3.

Item-response probabilities for each question by identified latent statuses

Domain Question Latent status
1 2 3 4 5
Antimicrobial stewardship We have an antimicrobial stewardship team (a member can work for both an infection control team and an antimicrobial stewardship team). 0.853 0.828 0.934 0.742 0.743
We have established criteria of interventions, such as their administration duration and selection, for patients administered antibiotics. 0.819 0.729 0.821 0.653 0.563
We have criteria for the uses of anti-MRSA antibiotics. 1 0 1 0.595 0.487
We have a preauthorization and/or restriction system for the use of anti-MRSA antibiotics. 0.525 0.505 1 0.176 0.169
We have criteria for the uses of broad-spectrum antibiotics such as carbapenems. 0.847 0.187 0.856 0.385 0.304
We have a preauthorization and/or restriction system for the use of broad-spectrum antibiotics. 0.365 0.348 0.947 0.072 0.065
We performed therapeutic drug monitoring for basically all cases. 0.800 0.723 0.607 0.593 0.506
We have manuals to establish the duration of prophylactic antibiotics administration in all departments. 0.603 0.621 0.513 0.426 0.324
Surveillance We perform surveillance for ventilator-associated pneumonia. 0.819 0.780 0.164 0.114 0.037
We perform surveillance for catheter-associated urinary tract infections. 0.874 0.710 0.261 0.450 0.375
We perform active surveillance cultures. 0.798 0.738 0.315 0.402 0.298
Medical and hospital equipment We perform regular oral cleansing for intubated patients in approximately 100% of relevant cases. 0.816 0.808 0.749 0.801 0.712
We insert central line catheters under maximal barrier precautions in approximately 100% of relevant cases. 0.374 0.358 0.416 1 0.000
We prepare intravenous hyperalimentation admixtures on clean benches in approximately 100% of relevant cases. 0.400 0.393 0.496 0.521 0.340
We have handwashing sinks at the entrance of an intensive care unit. 0.673 0.687 0.476 0.502 0.533
Infection control team activities regarding vaccinations and education of employees Needle puncture and sharp object injuries are reported to a relevant department, such as an infection control team. 0.735 0.580 0.756 0.805 0.644
We instruct new employees in hand hygiene by practical training for all professions. 0.493 0.423 0.593 0.460 0.571
We instruct new employees of all professions how to put on and remove personal protective equipment. 0.762 0.745 0.818 0.774 0.769
We instruct all employees in personal protective equipment by practical training every year. 0.198 0.125 0.242 0.146 0.202
Acknowledgment of updating relevant guidelines We do not change catheters without blockages or infections regularly. 0.892 0.786 0.657 0.666 0.657
Medical professions do not change their shoes while entering operating rooms. 0.764 0.713 0.509 0.532 0.509

Values in bold indicate that the probability was above the mean of each question (i.e., each row)

Table 4.

Status membership probabilities for the 1st and 2nd time periods

Time Latent status
1 2 3 4 5
1 0.236 0.171 0.180 0.149 0.263
2 0.253 0.171 0.088 0.170 0.318

Table 5.

Transition probabilities of each status from the 1st to 2nd time periods

Status, time 2
1 2 3 4 5
Status, time 1 1 0.996 0 0 0.004 0
2 0 1 0 0 0
3 0.099 0 0.427 0.148 0.327
4 0 0 0.040 0.961 0
5 0 0 0.015 0 0.985

Table 6.

Characteristics of each latent status

Latent status
Domain, number of questions in each domain 1 2 3 4 5
Antimicrobial stewardship, 8
Surveillance, 3
Medical and hospital equipment, 4
Infection control team activities regarding vaccinations and education of employees, 4
Acknowledgment of updating relevant guidelines, 2

✓, the number of questions for which the probability (shown in Table 3) was above the mean of probabilities for five domains for each question (the mean value of each row in Table 3) was higher than half of the number of questions in each domain; , the number of questions for which the probability (shown in Table 3) was above the mean of probabilities for five domains for each question (the mean value of each row in Table 3) was lower than a half of the number of questions in each domain. For example, latent status 2 had 7 questions of which probabilities were higher than the mean probability of corresponding questions in the first domain “antimicrobial stewardship.” These 7 probabilities were written in bold. The number of these bold ones was 5, which was more than half of the number of questions in the domain “antimicrobial stewardship,” 8, then status 3 was assigned to “✓ “for the first domain

Table 7.

Odds ratio estimates of covariates

Covariate Latent status P
1 2 3 4 5
Number of members in an infection control team* 0.55 0.61 1.32 0.74 Reference 0.027

* In full-time equivalent per 100 hospital beds

Discussion

We conducted two surveys on AMR and infections in teaching hospitals in Japan, with an interval of approximately 1 year between the surveys. Most hospitals had activities of ICTs, however, actual activities differed among hospitals. The results of LTA suggested that there were five subgroups of hospitals, which were considered indicating similar achievement levels of AMS. The presence of local (i.e. hospital-level) guidelines for using anti-MRSA and broad-spectrum antibiotics, and the range of surveillance activities of each hospital were identified as two major determinants of the membership in each subgroup.

The proportion of hospitals with antimicrobial stewardship teams decreased during the study period. In fiscal year 2018 (after the 2nd survey), a fee for antimicrobial stewardship teams was introduced by the National Fee Schedule. To claim this fee, hospitals must fulfill requirements such as having at least one full-time staff member who is a physician with more than 3 years of experience in infectious disease treatment, a nurse with more than 5 years of experience working in a hospital, or a pharmacist or a laboratory technologist with more than 3 years of experience working in a hospital. Our results suggest that hospitals not fulfilling this requirement might have changed their answers to this question from “having an antimicrobial stewardship team” to “not having an antimicrobial stewardship team.”

The proportion of hospitals with preauthorization and/or restriction systems for the use of anti-MRSA antibiotics and broad-spectrum antibiotics decreased during the study period. Preauthorization and/or prospective audit and feedback interventions by AMS programs are strongly recommended [11]. Although more than 90% of hospitals in our study responded that they carried out monitoring and intervention activities, roughly 70% had established intervention criteria, and less than 40% had preauthorization and/or restriction systems for anti-MRSA antibiotics and broad-spectrum antibiotics. These proportions also decreased throughout the study period. The use of restricted antibiotics lists has been reported to reduce antimicrobial resistance rates and costs [12]. Thus, hospitals should consider introducing preauthorization and/or restriction systems for relevant antibiotics to enhance their AMS programs.

The proportions of hospitals with surveillance for ventilator-associated pneumonia and catheter-associated urinary tract infections increased slightly, but remained under 60%. Given that these infections are considered major healthcare-associated infections along with surgical site infections and central line-associated bloodstream infections, surveillance is recommended [1315]. The proportion of hospitals performing active surveillance cultures was roughly 65%. However, active surveillance cultures for MRSA and vancomycin-resistant enterococci for all inpatients except for high-risk patients are not recommended [16]. The WHO Guidelines Development Group strongly recommends surveillance cultures for asymptomatic carbapenem-resistant Enterobacteriaceae and surveillance for carbapenem-resistant Acinetobacter baumannii and Pseudomonas aeruginosa despite a very low quality of evidence [17]. Further studies will be needed to determine the targets for active surveillance cultures and their efficacy.

For all questions regarding the ICU, the proportions of hospitals with the most favorable answers were less than 80%. This might be due to the fact that hospitals without an ICU were also included in this study. However, the proportion of hospitals that answered “yes” to the question about handwashing sinks at the ICU entrance was considerably lower (less than 60%) compared to those of hospitals that answered “yes” to the other questions. A Japanese guideline (2002) that recommended hospitals to place handwashing sinks at the ICU entrance [18] was revised to allow for the location to be based on staff accessibility [19]. However, since recent studies have suggested that sinks in the ICU might be a source of infections [2022], further investigations will be needed on appropriate locations and specifications of sinks in the ICU.

The LTA identified five statuses. There was a slight increase in the most favorable status (status 1) over the course of the study period (23.6 to 25.3%). However, the least favorable status (status 5) also showed an increase (26.3 to 31.8%), which was mainly due to a decrease in status 3 (18.0 to 8.8%). Previous studies have reported that human resources (FTEs of infection control practitioners) and FTE-to-bed ratios were related to improvements in AMS [35], defined as an increase in the number of implemented AMS programs [3] or effectiveness of AMS programs [4]. However, improvements in AMS may not correlate with the number of implemented programs, considering that the weight of each program is unlikely to be equal. In fact, the results of the LTA do not support a relationship between increasing the number of FTEs per bed and being in more favorable latent statuses. The odds ratio of status 3 versus status 5 was 1.32, indicating that more infection control practitioners might be required to improve domain 1, “antimicrobial stewardship,” whereas improvement in domains 2, 3, and 5 could not be fully explained by an increase in human resources alone. However, since previous studies, as well as our study, did not account for patient-level variations, further studies will be needed to identify factors associated with AMS other than human resources.

This study had some limitations. First, response rates were 55.0% for all hospitals with valid responses and 43.0% for those that responded to both surveys. There may have been selection bias in these hospitals. Second, hospitals participating in our study may have different profiles of cases and individual risks. To address these issues, we plan to link administrative data and the data of this study for further analyses.

Conclusion

The present nationwide surveys revealed the need for more comprehensive AMS programs; specifically, hospitals should consider introducing preauthorization and/or restriction systems for anti-MRSA antibiotics and broad-spectrum antibiotics. Our results also suggest that surveillance activities for ventilator-associated pneumonia and catheter-associated urinary tract infections need to be increased.

Supplementary Information

12879_2021_5921_MOESM1_ESM.docx (26.3KB, docx)

Additional file 1. English translation of the questionnaire for the study.

12879_2021_5921_MOESM2_ESM.docx (267KB, docx)

Additional file 2: Supplementary tables and a figure.

Acknowledgements

None.

Abbreviations

AMR

Antimicrobial resistance

AMS

Antimicrobial stewardship

FTE

Full-time equivalent

ICT

Infection control team

ICU

Intensive care unit

LTA

Latent transition analysis

MRSA

Methicillin-resistant Staphylococcus aureus

Authors’ contributions

Conception/design of the work: JS, SM, NS, SK, MK, MY, YG, DM, KS, NO, YI. Acquisition of data: SM, NS, SK, YI. Interpretation of data: JS, TO, HI, NS, YI. Drafted the work: JS. Revised the work: JS, SM, TO, HI, NS, SK, MK, MY, YG, DM, KS, NO, YI. All authors have approved the manuscript and agree with its submission to the journal.

Funding

This work was supported by Health Labour Sciences Research Grants from the Ministry of Health, Labour and Welfare, Japan [H27-shinkogyosei-shitei-005, H29-shinkogyosei-shitei-005, and 20HA2003 to Y. I.] and JSPS KAKENHI from the Japan Society for the Promotion of Science [JP16H02634 and JP19H01075 to Y. I.]. The funders played no role in the study design, data collection, and analysis, decision to publish, or preparation of the manuscript.

Availability of data and materials

The datasets used and/or analyzed during the current study are de-identified and available from the corresponding author on reasonable request.

Ethics approval and consent to participate

This study was conducted in accordance with the Ethical Guidelines for Medical and Health Research Involving Human Subjects of the MHLW, Japan. The Ethics Committee, Graduate School of Medicine, Kyoto University has approved this study (approval number: R0849). The Ethics Committee has also approved that consent is not applicable for the study. Patients’ information was anonymized prior to analysis. No additional permission was needed from each hospital to post the questionnaire.

Consent for publication

Not applicable.

Competing interests

None.

Footnotes

Publisher’s Note

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

12879_2021_5921_MOESM1_ESM.docx (26.3KB, docx)

Additional file 1. English translation of the questionnaire for the study.

12879_2021_5921_MOESM2_ESM.docx (267KB, docx)

Additional file 2: Supplementary tables and a figure.

Data Availability Statement

The datasets used and/or analyzed during the current study are de-identified and available from the corresponding author on reasonable request.


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