Association Between Parental Leave and Ophthalmology Resident Physician Performance

Dana D Huh; Jiangxia Wang; Michael J Fliotsos; Casey J Beal; Charline S Boente; C Ellis Wisely; Lindsay M De Andrade; Alice C Lorch; Saras Ramanathan; Maria A Reinoso; Ramya N Swamy; Evan L Waxman; Fasika A Woreta; Divya Srikumaran

doi:10.1001/jamaophthalmol.2022.3778

. 2022 Sep 29;140(11):1066–1075. doi: 10.1001/jamaophthalmol.2022.3778

Association Between Parental Leave and Ophthalmology Resident Physician Performance

Dana D Huh ¹, Jiangxia Wang ², Michael J Fliotsos ¹, Casey J Beal ³, Charline S Boente ⁴, C Ellis Wisely ⁵, Lindsay M De Andrade ⁶, Alice C Lorch ⁷, Saras Ramanathan ⁸, Maria A Reinoso ⁹, Ramya N Swamy ¹⁰, Evan L Waxman ¹¹, Fasika A Woreta ¹, Divya Srikumaran ^1,^✉

¹Wilmer Eye Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland

²Johns Hopkins Biostatistics Center, Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland

³Department of Ophthalmology, University of Florida, Gainesville

⁴Department of Ophthalmology, Indiana University School of Medicine, Indianapolis

⁵Department of Ophthalmology, Duke University, Durham, North Carolina

⁶Department of Ophthalmology and Visual Sciences, University of Iowa Hospitals & Clinics, Iowa City

⁷Department of Ophthalmology, Massachusetts Eye and Ear, Harvard Medical School, Boston

⁸Department of Ophthalmology, University of California, San Francisco, San Francisco

⁹Department of Ophthalmology, Louisiana State University Health Science Center, New Orleans

¹⁰Department of Ophthalmology and Visual Sciences, University of Maryland School of Medicine, Baltimore

¹¹Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania

Accepted for Publication: August 2, 2022.

Published Online: September 29, 2022. doi:10.1001/jamaophthalmol.2022.3778

^✉

Corresponding Author: Divya Srikumaran, MD, Wilmer Eye Institute, Johns Hopkins University School of Medicine, 600 N Wolfe St, Wilmer 376, Baltimore, MD 21287 (dsrikum1@jhmi.edu).

Author Contributions: Dr Srikumaran had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Fliotsos, Ramanathan, Woreta, Srikumaran.

Acquisition, analysis, or interpretation of data: Huh, Wang, Fliotsos, Beal, Boente, Wisely, De Andrade, Lorch, Ramanathan, Reinoso, Swamy, Waxman, Srikumaran.

Drafting of the manuscript: Huh, Wang, Fliotsos, Srikumaran.

Critical revision of the manuscript for important intellectual content: All authors.

Statistical analysis: Wang.

Administrative, technical, or material support: Huh, Fliotsos, Beal, Boente, Reinoso, Srikumaran.

Supervision: Wisely, Swamy, Woreta, Srikumaran.

Conflict of Interest Disclosures: Ms Wang reported receiving grants from the National Eye Institute and a Wilmer Biostatistics Core Grant during the conduct of the study. Dr Beal reported receiving grants from Research to Prevent Blindness during the conduct of the study. Dr Lorch reported receiving consultant fees from Regeneron Pharmaceuticals Inc outside the submitted work. Dr Reinoso reported receiving grant support from the National Institute of Health/National Eye Institute outside the submitted work. Dr Woreta reported receiving grant support from the Donaghue Foundation’s Greater Value Portfolio Grant Program, Research to Prevent Blindness and American Academy of Ophthalmology Award for IRIS Registry Research, and the H. Dunbar Hoskins Jr., MD, Center for Quality Eye Care IRIS Registry Research Fund. Dr Srikumaran reported receiving grants from the Johns Hopkins Institute for Clinical and Translational Research, the National Eye Institute, Zoster Eye Disease Study, Diabetes Endothelial Keratoplasty Study, Eye Bank Association of America, the Leighton Cornea Research Fund, Research to Prevent Blindness, and the American Academy of Ophthalmology Hoskins Center IRIS Registry; consulting fees from Alcon; and fees for expert legal testimony outside the submitted work. No other disclosures were reported.

Funding/Support: This work was supported by grant P30EY01765 from Wilmer Biostatistics Core.

Role of the Funder/Sponsor: The funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We thank Moran Roni Levin, MD (Department of Ophthalmology and Visual Sciences, University of Maryland), Pratap Challa, MD (Duke University Eye Center), Elizabeth Renee Wynne (Duke University Eye Center), Christie L. Little, CPC (Department of Ophthalmology, University of Florida), Mallory Mack, BA (Department of Ophthalmology, Indiana University School of Medicine), Deborah Bruce (Department of Ophthalmology and Visual Sciences, University of Maryland), and Topister Bonyo, MPH (Massachusetts Eye and Ear) for their support with data collection for our study. No compensation was received from any of the aforementioned individuals.

^✉

Corresponding author.

PMCID: PMC9523550 PMID: 36173610

This cross-sectional study investigates if there is an association between parental leave and ophthalmology resident physician performance.

Key Points

Question

Is there an association between parental leave and ophthalmology resident physician performance?

Findings

In this multicenter, cross-sectional review of educational records of 283 ophthalmology residents who graduated between 2015 and 2019, 44 residents (16%) used parental leave. No differences were identified between residents who took leave vs those who did not in regard to their performance across multiple metrics, including examination performance, evaluation scores, research activity, and surgical volume.

Meaning

Results of this study suggest that there was no association between resident performance and parental leave, which supports adequate parental leave for residents.

Abstract

Importance

Although parental leave is essential in enhancing resident wellness and fostering inclusive workplace environments, residents may often feel discouraged from using parental leave owing to perceived stigma and concerns about possible negative effects on their training.

Objective

To examine parental leave usage across multiple institutions and compare residency performance metrics between residents who took parental leave vs their peers who did not take leave.

Design, Setting, and Participants

This was a retrospective cross-sectional analysis conducted from April 1, 2020, to July 28, 2022, of educational records. Multicenter data were obtained from 10 Accreditation Council for Graduate Medical Education (ACGME)–accredited ophthalmology programs across the US. Included ophthalmology residents graduated between 2015 and 2019. Data were analyzed from August 15, 2021, to July 25, 2022.

Exposures

Performance metrics of residents who used parental leave during residency were compared with those of residents who did not take parental leave.

Main Outcomes and Measures

Measures of performance included the Ophthalmic Knowledge Assessment Program (OKAP) scores, ACGME milestones scores, board examination pass rates, research activity, and surgical volumes.

Results

Of the 283 ophthalmology residents (149 male [52.7%]) included in the study, 44 (15.5%) took a median (IQR) parental leave of 4.5 (2-6) weeks. There were no differences in average OKAP percentiles, research activity, average ACGME milestones scores, or surgical volume between residents who took parental leave and those who did not. Residents who pursued fellowship were less likely to have taken parental leave (odds ratio [OR], 0.43; 95% CI, 0.27-0.68; P < .001), and residents who practiced in private settings after residency were more likely to have taken parental leave (OR, 3.56; 95% CI, 1.79-7.08; P < .001). When stratified by sex, no differences were identified in performance between female residents who took parental leave compared with residents who did not take leave, except a mild surgical number difference in 1 subspecialty category of keratorefractive procedures (difference in median values, −2; 95% CI, −3.7 to −0.3; P = .03).

Conclusions and Relevance

In this multicenter cross-sectional study, no differences in performance metrics were identified between residents taking parental leave compared with their peers. These findings may provide reassurance to trainees and program directors regarding the unlikelihood, on average, that taking adequate parental leave will affect performance metrics adversely.

Introduction

As pregnancy and child-rearing during surgical residency become increasingly prevalent,^1,2 parental leave policies in ophthalmology graduate medical education (GME) have become an important topic of discussion. Residency years often coincide with biologically and personally compelling times to start a family, leading a substantial portion of surgical residents to have children during training.^3,4 In fact, female physicians who delay parenthood owing to the demands of training have increased rates of fertility difficulties compared with the general population, in addition to higher rates of career dissatisfaction and burnout.^5,6,7,8,9 Supporting trainees through adequate parental leave has been found to improve resident wellness and productivity, as well as long-term maternal and child health outcomes.^4,10,11,12 Furthermore, parental leave is not only essential for women but for nonpregnant and nontraditional partners such as expectant fathers and adoptive parents, with adequate paternal leave also associated with important benefits for both child and family.¹³

Among US GME programs, there is widespread variability in how parental leave is offered and used. Historically, the Accreditation Council for Graduate Medical Education (ACGME) required institutions to have parental leave policies in place, deferring to individual specialty boards and institutions in setting specific guidelines.¹⁴ As of July 2022, however, the ACGME has updated its guidelines to mandate that all programs offer 6 weeks of paid medical, parental, and caregiver leave to trainees.¹⁵ Additionally, the American Board of Medical Specialties unveiled a policy effective July 2021, mandating that member boards have written policies stating the minimum amount of training time required for certification and allowing a minimum of 6 weeks of leave without requiring training extension.¹⁶ The American Board of Ophthalmology now requires a minimum of 6 months of training at any postgraduate year level and allows satisfactory ratings in each of the ACGME competencies to fulfill certification criteria, paving the way for more competency-based determination in certification rather than time-based determination.^17,18 Although these recent developments are significant changes that may affect leave usage in the future, many programs still lack explicit written policies that guide appropriate duration of leave and specific protocols, resulting in wide variability and uncertainty in practice.^18,19,20

Although more leave policies are being outlined by programs over time,¹⁹ parental leave is still often surrounded by stigma and concerns from both residents and program directors. Numerous surveys have revealed that program directors in ophthalmology, as well as general surgery, obstetrics and gynecology, otolaryngology, and anesthesiology, perceive parental leave and childbearing to negatively affect resident scholarly activities, surgical and clinical skills, and even dedication to patient care.^{18,21,22,23,24} Likewise, residents expressed concern for their loss of training time, perceiving that parental leave may lead to delayed program completion, loss of professional opportunities, and increased burden for coresidents.^3,25,26,27 A majority of ophthalmology residents reported receiving negative feedback or actions regarding parenthood during training, and many residents do not feel fully supported by their colleagues in taking parental leave.^{27,28,29,30,31}

Currently, there are limited data on whether these negative perceptions and concerns are based on objective measures of performance of residents who take parental leave during training. In a single-center study of 25 ophthalmology residents, we previously reported no difference in any measures of resident performance between those who took parental leave and their peers.³² As institutional policies vary and parental leave practices vastly differ across institutions, we expanded on our previous findings to report multicenter data from 10 ACGME-accredited ophthalmology programs. In this study, we aimed to examine parental leave usage across multiple institutions and compare various residency performance metrics such as research productivity, Ophthalmic Knowledge Assessment Program (OKAP) scores, ACGME milestones scores, board examination performance, and surgical volumes between residents who took parental leave vs their peers.

Methods

The study protocol for this cross-sectional analysis, conducted from April 1, 2020, to July 28, 2022, was approved by the institutional review board of Johns Hopkins University School of Medicine and deemed exempt as it involved review of deidentified internal records available to the ophthalmology department. The study protocol was reviewed and approved by the institutional reviewer board of all collaborating institutions. All study activities adhered to the tenets of the Declaration of Helsinki. In order to identify eligible programs for our study, we contacted program directors who participated in our prior parental leave survey¹⁸ as well as members from the Women in Ophthalmology listserv. Programs that had at least 1 trainee take parental leave between 2015 and 2019 were invited to participant, and a total of 10 programs were included: Johns Hopkins University, University of Maryland, University of Iowa, University of Florida, University of California San Francisco (UCSF), Duke University, Indiana University, Louisiana State University, Harvard University, and University of Pittsburgh. A standardized protocol was developed to ensure that data from each institution were collected in an identical manner.

Deidentified information of all residents who graduated between 2015 and 2019 was collected, including data on duration of parental leave, other types of leave taken (such as sick leave), and whether a resident had an extension of training. Demographic data such as sex, race, ethnicity, and number of children before residency were collected based on self-reported data available through internal program records, as well as preresidency characteristics, such as the United States Medical Licensing Examination (USMLE) Step 1 and Step 2 Clinical Knowledge scores, Alpha Omega Alpha (AOA) status, and whether the resident had other postgraduate degrees (such as doctor of philosophy, master of public health, or master of business administration), as these metrics were available on the SF Match residency applications and consistent across programs. The race and ethnicity categories included in this analysis were Asian, Black, Hispanic, White, other (including American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, and multiple race or ethnicities), and unknown.

The primary outcomes of this study were measures of resident performance. Mean OKAP percentiles were calculated using scores from the first, second, and third year of residency. Graduating ACGME milestones scores (scale 1-9) were grouped into 6 core competencies (patient care, medical knowledge, systems-based practice, practice-based learning and improvement, professionalism, interpersonal and communication skills), and the mean scores of each core competency were used for analysis. Surgical volumes were obtained from ACGME case logs and grouped into subspecialty procedural categories (cataract, laser, cornea, keratorefractive, strabismus, glaucoma, retinal vitreous, oculoplastic and orbit, and globe trauma) based on minimum case requirements set by the ACGME Review Committee for Ophthalmology. Research activity was defined by whether the resident participated in research during residency (yes/no) and published any peer-reviewed publications during residency (yes/no). Lastly, postresidency data included whether the resident passed the Written Qualifying Examination and oral boards examination on their first attempt (yes/no), pursued fellowship training (yes/no), or pursued a career in academic ophthalmology vs private practice upon graduating. This study followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) reporting guidelines.

Statistical Analysis

The continuous outcomes were compared by parental leave status, and the differences in the medians between the 2 groups were estimated using population-averaged linear regression models with quantile regression models with robust and clustered SEs. The categorical variables were compared using exact logistic regression models. The analyses accounted for correlations in parental leave usage for residents from the same institution. The median differences between groups, or the odds ratio (OR) for taking parental leave, along with the 95% CIs, were reported. All statistical analyses were performed using Stata, version 17.0 (StataCorp). All P values were 2-sided without adjustment for multiple analyses, and statistical significance was defined as P < .05. Data were analyzed from August 15, 2021, to July 25, 2022.

Results

Of the 283 ophthalmology residents (149 male [52.7%]; 134 female [47.3%]) included in the study, 44 (15.5%) took a median (IQR) parental leave of 4.5 (2-6) weeks. Among those who took parental leave, 23 residents (52.3%) were female with leave duration (IQR) of 6 (6-8) weeks, whereas male residents had leave duration of 2 (1-2) weeks. Of the 2 residents who ultimately extended their training by 52 weeks, 1 resident took parental leave while the other resident did not take parental leave, although the exact reasons behind the extensions were not obtained. Residents self-identified with the following race and ethnicity categories: 87 Asian (30.7%), 8 Black (2.8%), 9 Hispanic (3.2%), 137 White (48.4%), 3 other (1.1%), and 39 unknown (13.8%).

Table 1 shows demographic and preresidency characteristics of residents, stratified by those who took parental leave compared with those who did not. Residents who had 1 or more children before starting residency had higher odds of having taken parental leave (OR, 2.75; 95% CI, 1.19-6.36; P = .02) compared with those who had no children before residency. No differences were identified between those who took parental leave vs their peers in regard to preresidency characteristics including USMLE Step 1 and 2 scores and AOA membership.

Table 1. Demographic and Preresidency Characteristics for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Characteristic	No. (%)		Difference in medians between residents who did or did not take leave; or odds ratio for taking leave (95% CI)^a	P value
Characteristic	Residents who did not take parental leave (n = 239)	Residents who took parental leave (n = 44)		P value
Graduating year
2015	49 (20.5)	9 (20.5)	1 [Reference]	.43
2016	51 (21.3)	6 (13.6)	0.63 (0.29 to 1.41)
2017	41 (17.2)	13 (29.5)	1.69 (0.74 to 3.81)
2018	51 (21.3)	6 (13.6)	0.65 (0.33 to 1.26)
2019	47 (19.7)	10 (22.7)	1.16 (0.44 to 3.04)
Sex
Male	128 (53.8)	21 (47.7)	1 [Reference]	.43
Female	110 (46.2)	23 (52.3)	1.64 (0.48 to 5.62)	.43
Race and ethnicity
Asian	79 (33.1)	8 (18.2)	0.54 (0.32 to 0.94)	.09
Black	7 (2.9)	1 (2.3)	0.90 (0.21 to 2.76)
Hispanic	8 (3.3)	1 (2.3)	0.81 (0.20 to 3.23)
White	108 (45.2)	29 (65.9)	1 [Reference]
Other^b	2 (0.8)	1 (2.3)	1.30 (0.31 to 5.40)
Unknown	35 (14.6)	4 (9.1)	0.47 (0.20 to 1.14)
No. of children before residency
0	212 (91.8)	27 (65.9)	1 [Reference]	.02
≥1	19 (8.2)	14 (34.1)	2.75 (1.19 to 6.36)	.02
Preresidency characteristics
USMLE score, median (IQR)
Step 1	242 (234 to 251)	246 (233.5 to 252)	3 (−1.7 to 7.7)	.21
Step 2	247 (235 to 256)	244 (232 to 254)	−3 (−10.3 to 4.3)	.42
AOA membership
Yes	54 (22.6)	19 (43.2)	1.85 (1.05 to 3.27)	.10
No	117 (49.0)	14 (31.8)	1 [Reference]
Unknown	68 (28.5)	11 (25.0)	1.30 (0.51 to 3.33)
MD/PhD, and other advanced degrees (MBA, MPH, MS)
Yes	45 (18.8)	10 (22.7)	1.34 (0.44 to 4.03)	.60
No	194 (81.2)	34 (77.3)	1 [Reference]	.60

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Abbreviations: AOA, Alpha Omega Alpha; MBA, master of business administration; MD, doctor of medicine; MPH, master of public health; MS, master of science; PhD, doctor of philosophy; USMLE, United States Medical Licensing Examination.

^{^a}

Difference in medians calculated for continuous variables; odds ratio for taking leave calculated for categorical variables.

^{^b}

Other race and ethnicity includes American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, multiple race or ethnicities, and unknown.

In comparing performance metrics during residency (Table 2), there were no differences in average OKAP percentiles, research activity during residency, or mean ACGME milestones scores between residents who took parental leave and those who did not. There were no differences in any subspecialty categories of surgical volume (eTable in the Supplement).

Table 2. Residency Performance for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Characteristic	Median (IQR)		Difference in medians between residents who did or did not take leave; or odds ratio for taking parental leave (95% CI)^a	P value
Characteristic	Residents who did not take parental leave (n = 239)	Residents who took parental leave (n = 44)		P value
Academic
OKAP percentile (first-, second-, third-year scores averaged)	53.50 (36.33 to 71.33)	56.33 (35.67 to 66.33)	2.17 (−7.03 to 11.4)	.64
Research activity during residency, No. (%)
Yes	237 (99.6)	44 (100.0)	NA	<.99^b
No	1 (0.4)	0 (0.0)	NA	<.99^b
Peer-reviewed publications during residency, No. (%)
Yes	165 (69.6)	10 (22.7)	0.99 (0.51 to 1.93)	.98
No	72 (30.4)	34 (77.3)	1 [Reference]	.98
Milestones
Patient care	7.13 (7 to 7.88)	7.25 (7 to 8)	0.125 (−0.08 to 0.33)	.24
Medical knowledge	7 (7 to 8)	7.50 (7 to 8)	0.5 (−0.28 to 1.28)	.21
Systems-based practice	7 (6.67 to 7.67)	7 (6.67 to 8)	0 (−0.53 to 0.53)	<.99
Practice-based learning and improvement	7 (7 to 7.67)	7 (6.67 to 7.83)	0 (−0.43 to 0.43)	<.99
Professionalism	7 (7 to 8)	7.50 (6.88 to 8)	0.5 (−0.70 to 1.70)	.41
Interpersonal and communication skills	7 (7 to 7.75)	7 (7 to 8)	0 (−0.50 to 0.50)	<.99
Surgical volumes
Cataract	201 (161 to 252)	208 (178 to 272)	10 (−51.10 to 71.10)	.75
Laser	70 (51 to 101)	76.5 (59 to 103.5)	9 (−5.18 to 23.20)	.21
Cornea	17 (13 to 26)	17.5 (11.5 to 28)	1 (−2.43 to 4.43)	.57
Keratorefractive	8 (6 to 14)	6.5 (4 to 11)	−1 (−2.61 to 0.62)	.22
Strabismus	22 (17 to 38)	27.5 (16 to 36)	6 (−2.55 to 14.60)	.17
Glaucoma	12 (8 to 17)	12 (8 to 18.5)	0 (−2.74 to 2.74)	<.99
Retinal vitreous	22 (12 to 36)	13 (3 to 18.5)	−9 (−22.50 to 4.52)	.19
Oculoplastic and orbit	68 (48 to 104)	102 (57 to 134.5)	34 (−4.72 to 72.70)	.09
Globe trauma	8 (6 to 13)	9 (5.5 to 13)	1 (−1.01 to 3.01)	.33

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Abbreviations: NA, not applicable; OKAP, Ophthalmic Knowledge Assessment Program.

^{^a}

Difference in medians calculated for continuous variables; odds ratio for taking leave calculated for categorical variables.

^{^b}

P value calculated using Fisher exact test for variables in which one group has a low n less than or equal to 1.

In examining postresidency characteristics (Table 3), the 2 groups showed no differences in whether they passed their written or oral board examinations on the first attempt. Residents who pursued fellowship after residency were less likely to have taken parental leave (OR, 0.43; 95% CI, 0.27-0.68; P < .001) compared with residents who did not pursue fellowship. In addition, residents who practiced in private settings after residency were more likely to have taken parental leave (OR, 3.56; 95% CI, 1.79-7.08; P < .001) compared with those who practiced in academic settings.

Table 3. Postresidency Characteristics for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Characteristic	No. (%)		Odds ratio for taking parental leave (95% CI)	P value
Characteristic	Residents who did not take parental leave (n = 239)	Residents who took parental leave (n = 44)	Odds ratio for taking parental leave (95% CI)	P value
Passed written qualifying board examination on first attempt
Yes	206 (86.2)	37 (84.1)	0.39 (0.10-1.62)	.001
No	10 (4.2)	5 (11.4)	1 [Reference]
Not taken/unknown	23 (9.6)	2 (4.5)	0.14 (0.04-0.55)
Passed oral boards examination on first attempt
Yes	171 (71.5)	34 (77.3)	1.04 (0.34-3.86)	<.99
No	33 (13.8)	5 (11.4)	1 [Reference]
Not taken/unknown	35 (14.6)	5 (11.4)	1.00 (0.26-3.86)
Fellowship training
Yes	198 (82.8)	28 (63.6)	0.43 (0.27-0.68)	<.001
No	41 (17.2)	16 (36.4)	1 [Reference]	<.001
Fellowship specialty
Comprehensive^a	3 (1.5)	1 (3.4)	NA	.004
Cornea, external disease, refractive	46 (23.0)	7 (24.1)	1 [Reference]
Glaucoma	35 (17.5)	6 (20.7)	1.03 (0.66-1.62)
Medical retina and vitreoretinal	72 (36.0)	7 (24.1)	0.60 (0.21-1.74)
Neuro-ophthalmology	2 (1.0)	2 (6.9)	4.65 (0.42-51.60)
Oculoplastics	19 (9.5)	4 (13.8)	1.25 (0.41-3.85)
Pediatric ophthalmology and adult strabismus	22 (11.0)	2 (6.9)	0.61 (0.14-2.63)
Telemedicine^a	1 (0.5)	0	NA
Practice setting
Academic	89 (42.6)	8 (19.0)	1 [Reference]	<.001
Private	116 (55.5)	34 (81.0)	3.56 (1.79-7.08)
Combined or unknown^a	4 (1.9)	0	NA

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Abbreviation: NA, not available.

^{^a}

Excluded from regression as one or both of the comparison groups has n less than or equal to 1 resident.

Lastly, as male residents took shorter duration of leave (with some taking as minimal as 1 week) compared with female residents, results were further stratified by sex to exclude male residents from the analysis and examine female-specific performance. Table 4 demonstrates comparisons between female residents who took parental leave vs all residents who did not take parental leave. There were no differences between the 2 groups regarding OKAP performance, research activity, ACGME milestones scores, or most subspecialty categories of surgical volume including cataract procedures. Female residents had slightly lower keratorefractive surgical number (difference in median values, −2; 95% CI, −3.7 to −0.3; P = .03) compared with residents who did not take leave.

Table 4. Resident Characteristics and Residency Performance, Stratified by Female Residents Who Took Parental Leave Compared With All Residents Who Did Not Take Parental Leave.

Characteristic	No. (%)		Difference in medians between residents who did/did not take leave; or odds ratio for taking parental leave (95% CI)^a	P value
Characteristic	All residents who did not take parental leave (n = 239)	Female residents who took parental leave (n = 23)		P value
Race and ethnicity
Asian	79 (33.1)	7 (30.4)	1.36 (0.48 to 4.21)	.77^c
Black	7 (2.9)	1 (4.3)	0.84 (0.10 to 40.9)
Hispanic	8 (3.3)	0	NA
White^b	108 (45.2)	13 (56.5)	1 [Reference]
Other	2 (0.8)	0	NA
Unknown	35 (14.6)	2 (8.7)	2.10 (0.44 to 20.1)
No. of children before residency
0	212 (91.8)	16 (76.2)	1 [Reference]	.02
≥1	19 (8.2)	5 (23.8)	4.08 (1.21 to 13.7)	.02
USMLE Score, median (IQR)
Step 1	242.00 (234.00 to 251.00)	247.00 (229.00 to 252.00)	5 (−0.6 to 10.6)	.08
Step 2	247.00 (235.00 to 256.00)	244.50 (230.00 to 254.00)	−3 (−21.2 to 15.2)	.75
AOA status
Yes	54 (22.6)	8 (34.8)	2.64 (1.04 to 8.18)	.09
No	117 (49.0)	6 (26.1)	1 [Reference]
Unknown	68 (28.5)	9 (39.1)	2.67 (0.87 to 8.18)
MD/PhD or other advanced degrees (MBA, MPH, MS, etc)
Yes	45 (18.8)	7 (30.4)	1.93 (1.01 to 3.70)	.05
No	194 (81.2)	16 (69.6)	1 [Reference]	.05
Residency performance metrics
Average OKAP percentile, median (IQR)	53.5 (36.3 to 71.3)	57.0 (32.3 to 67.3)	3.50 (−6.60 to 13.60)	.50
Research activity during residency
Yes	237 (99.6)	23 (100.0)	1 [Reference]	<.99^c
No	1 (0.4)	0	NA	<.99^c
Peer-reviewed publications during residency
Yes	165 (69.6)	18 (78.3)	1 [Reference]	.22
No	72 (30.4)	5 (21.7)	1.59 (0.75 to 3.33)	.22
ACGME milestones, median (IQR)
Patient care	7.13 (7 to 7.88)	7.25 (6.88 to 8)	0.13 (−0.32 to 0.57)	.58
Medical knowledge	7 (7 to 8)	7.50 (7 to 8)	0.50 (−0.33 to 1.33)	.24
Systems-based practice	7 (6.67 to 7.67)	7 (6.33 to 7.33)	0 (−0.37 to 0.37)	<.99
Practice-based learning and improvement	7 (7 to 7.67)	7 (6.33 to 7.67)	0 (−0.55 to 0.55)	<.99
Professionalism	7 (7 to 8)	7.25 (5.25 to 7.75)	0.25 (−0.21 to 0.71)	.28
Interpersonal and communication skills	7 (7 to 7.75)	7 (6 to 7)	0 (−0.22 to 0.22)	<.99
Surgical volume, median (IQR)
Cataract	201.00 (161.00 to 252.00)	183.00 (165.00 to 238.00)	−18 (−43.5 to 7.5)	.17
Laser	70.00 (51.00 to 101.00)	69.00 (56.00 to 100.00)	−1 (−22.7 to 20.7)	.93
Corneal	17.00 (13.00 to 26.00)	16.00 (11.00 to 28.00)	−1 (−6.4 to 4.4)	.72
Keratorefractive	8.00 (6.00 to 14.00)	7.00 (3.00 to 13.00)	−2 (−3.7 to −0.3)	.03
Strabismus	22.00 (17.00 to 38.00)	20.00 (16.00 to 34.00)	−2 (−11.0 to 7.0)	.66
Glaucoma	12.00 (8.00 to 17.00)	12.00 (8.00 to 25.00)	0 (−3.1 to 3.1)	<.99
Retinal vitreous	22.00 (12.00 to 36.00)	17.00 (10.00 to 25.00)	−5 (−10.8 to 0.8)	.09
Oculoplastic and orbit	68.00 (48.00 to 104.00)	74.00 (49.00 to 106.00)	6 (−20.5 to 32.5)	.66
Globe trauma	8.00 (6.00 to 13.00)	9.00 (5.00 to 14.00)	1 (−2.6 to 4.6)	.59

Open in a new tab

Abbreviations: ACGME, Accreditation Council for Graduate Medical Education; AOA, Alpha Omega Alpha; MD, doctor of medicine; MPH, master of public health; MS, master of science; NA, not available; OKAP, Ophthalmic Knowledge Assessment Program; PhD, doctor of philosophy; USMLE, United States Medical Licensing Examination.

^{^a}

Difference in medians calculated for continuous variables; odds ratio for taking leave calculated for categorical variables.

^{^b}

Other race and ethnicity includes American Indian or Alaska Native, Native Hawaiian or Other Pacific Islander, multiple race or ethnicities, and unknown.

^{^c}

P value calculated using exact logistic regression.

Discussion

In this multicenter cross-sectional study, we found that ophthalmology residents used a median of 4.5 weeks for parental leave, and there were no differences between those who took parental leave and their peers across multiple performance metrics. These findings are consistent with a recent single-center study that similarly showed no differences in OKAP scores, number of publications during residency, milestone scores, or surgical volume.³² We found no differences in surgical volume between the 2 groups in all subspecialty categories, including cataract surgeries, which is also consistent with a study by Gong et al,³³ showing that residents who took maternity leave performed similar numbers of cataract operations and overall procedural volume as those who did not take leave. These results may suggest that residents who take parental leave—and their program leadership—are making extra efforts before and after leave to ensure that the lost training time does not negatively affect their performance and surgical numbers. Studies have shown that residents performed well above the minimum number of operations required by the ACGME regardless of parental leave status,³³ supporting the notion that taking parental leave still allows for trainees to acquire adequate procedural and educational experiences.

Our study found that a lower proportion of parental leave residents pursued fellowship or a career in academic ophthalmology. A prior study examining postgraduate career decisions of ophthalmology residents found that residents who decided to pursue fellowship had fewer children, had less educational debt, and were more likely to plan to practice in academic settings,³⁴ suggesting several factors that may be relevant to residents taking parental leave examined in our study. One hypothesis for the differences observed may be that residents who took parental leave may potentially have had fewer months during training to build longitudinal mentorship opportunities with faculty in academia, which may have affected their eventual career choices in pursuing fellowships and ultimately their interest in a career in academia. In addition, residents who use parental leave are often concerned about the possibility of extending their training,^9,35 which could lead to uncertainties in applying and planning for fellowships in the period after graduation. In our study, however, only 2 residents (0.7%) extended their training (1 used parental leave and the other did not) and both of these residents pursued fellowships after residency. As child-rearing can take substantial amounts of financial resources, financial factors involving educational debt may additionally play into trainees’ decisions to pursue additional years of fellowship training. Finally, private practice environments may present fewer mandatory evening commitments and offer more flexibility for physicians’ family responsibilities or personal schedules as well as more part-time opportunities, leading trainees with children to pursue private practice.

When stratified by sex, we found that female residents tended to take longer parental leave (median, 6 weeks) compared with male residents (median, 2 weeks). As female residents taking longer parental leave may be affected by leave in different ways than male residents taking shorter parental leave, we performed additional analyses excluding male residents and comparing the same metrics for female residents only. We found that the performance of female residents taking parental leave were not different from the performance of residents who did not take leave in all metrics except surgical volume in 1 subspecialty category. There were no differences identified in other subcategories, including cataract and laser surgeries, that constituted the majority of total surgical volume, and the slight difference in surgical number was identified in keratorefractive surgery, which constitutes a small proportion of overall volume. Previous studies have revealed that program directors perceive childbearing to negatively affect resident dedication to patient care.¹⁸ In addition, program directors were found to perceive that taking leave would more negatively affect dedication and performance for childbearing parents compared with nonchildbearing parents, revealing gender gaps in perceptions of leave.¹⁸ Our results demonstrate that these perceptions may not be based on measurable metrics of performance including standardized examinations, research activity, most categories of surgical volume, and milestones evaluations that specifically measure resident competencies in categories including patient care and professionalism. As such, it is critical to examine ways in which both childbearing and nonchildbearing residents could be better supported in taking adequate leave and to consider whether explicit and implicit gender biases may play a role in the perception of parental leave during medical education.

As part of the recently unveiled leave policy, the American Board of Medical Specialties recommended continued collection of data to study the affect of parental leave on certifying examination pass rates after implementation of the new policy.¹⁶ Although our data are retrospective and included residents who took leave before the policy changes, we believe that these findings can contribute to our knowledge on the association between parental leave and examination pass rates, in addition to other performance metrics. Overall, our findings could provide reassurance to both trainees and program directors to support adequate parental leave and changes at the institution, and program levels can improve the experiences of residents taking leave. Programs with explicit parental leave policies in place have been shown to have higher proportion of residents using leave.³⁶ As such, programs should have explicit written parental leave policies that address childbearing, nonchildbearing, and adoptive parents to promote an inclusive environment and provide clear guidelines on standard practices such as work hours, extension of training, and board eligibility to allow residents to make informed decisions.

According to previous studies, program directors not only worry about the effect of leave on residents’ training but also on the fellow trainees in regard to finding coverage and maintaining consistency and fairness.^18,21 Currently, coverage for residents on leave is usually spread across the remaining coresidents without compensation or advanced scheduling.²³ Each program should implement specific protocols as part of their parental leave policy, aiming for reallocation of call schedules and redistribution of the department workforce based on the need for service volume, number of residents on service, and length of leave. Recruitment of advanced practice clinicians, residents on research years, and program faculty may help alleviate the work burden for residents during leave periods.

Multiple options exist for changes in the program infrastructure to accommodate parental leave, such as allowing flexible research time or placing residents returning from leave on rotations with fewer weekly hours or closer to residents’ home program. Programs such as the “flexible option” for pediatric residents at UCSF, or the American Board of Surgery’s “6-year option,” which allows residents to complete 5 clinical years over 6 years of training, demonstrate that it is possible to implement flexible scheduling programs that still satisfy board requirements.^3,37

Strengths and Limitations

The strengths of this study include the fact that it was a multicenter approach, representative of leave practices among a variety of programs across the US. Limitations include the small sample size owing to the limited number of residents who take parental leave each year. There were additionally some limitations in the data available through the ACGME and internal records of each institution, eg, the exact reasons behind training extensions could not be specified owing to privacy concerns, leading to uncertainties regarding whether parental leave had any influence on the extension of 1 resident’s training. In addition, data on research activity could not be stratified into types (case reports vs research manuscripts) or number of publications. Similarly, the preresidency characteristics analyzed were limited to those available in program files, such as USMLE scores and AOA status, which did not provide more granular or holistic views of academic performance. However, although standardized USMLE scores may not predict residency performance, USMLE and OKAP performance have been found to be correlated with Written Qualifying Examination performance and is thus still worthwhile to examine.³⁸ Lastly, our data were obtained from programs that were mainly research institutions and led by program directors willing to participate in this study. As such, our data may be skewed toward programs that have more favorable policies or attitudes toward parental leave and thus may not be fully representative of all residency programs. It is important to note that there may be inherent differences between institutions in regard to program size and structure, as well as availability of resources to accommodate trainees who take parental leave.

Conclusions

Results of this cross-sectional study suggest that there was no association between parental leave and ophthalmology resident physician performance. We believe it is critical that program and institution leaders continue active discussions on establishing consistent and transparent parental leave policies and strategizing ways to reduce burden on residents. We hope that findings from this study can contribute to our current understanding of leave practices and address perceptions associated with parental leave, helping improve resident retention, well-being, and gender equity in the field of ophthalmology.

Supplement.

eTable. Detailed Surgical Volume for Ophthalmology Residents Graduating From 2015-2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not

Click here for additional data file.^{(145.6KB, pdf)}

References

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7.Sullivan MC, Yeo H, Roman SA, Bell RH Jr, Sosa JA. Striving for work-life balance: effect of marriage and children on the experience of 4402 US general surgery residents. Ann Surg. 2013;257(3):571-576. doi: 10.1097/SLA.0b013e318269d05c [DOI] [PubMed] [Google Scholar]
8.Bering J, Pflibsen L, Eno C, Radhakrishnan P. Deferred personal life decisions of women physicians. J Womens Health (Larchmt). 2018;27(5):584-589. doi: 10.1089/jwh.2016.6315 [DOI] [PubMed] [Google Scholar]
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26.Brown EG, Galante JM, Keller BA, Braxton J, Farmer DL. Pregnancy-related attrition in general surgery. JAMA Surg. 2014;149(9):893-897. doi: 10.1001/jamasurg.2014.1227 [DOI] [PubMed] [Google Scholar]
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28.Reilly G, Tipton C, Liberman P, Berkenstock M. Attitudes toward parental leave and breastfeeding during ophthalmology residency. Can J Ophthalmol. 2022;57(3):175-187. doi: 10.1016/j.jcjo.2021.02.039 [DOI] [PubMed] [Google Scholar]
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Associated Data

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

Supplementary Materials

Supplement.

eTable. Detailed Surgical Volume for Ophthalmology Residents Graduating From 2015-2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not

Click here for additional data file.^{(145.6KB, pdf)}

[eoi220057r1] 1.Smith C, Galante JM, Pierce JL, Scherer LA. The surgical residency baby boom: changing patterns of childbearing during residency over a 30-year span. J Grad Med Educ. 2013;5(4):625-629. doi: 10.4300/JGME-D-12-00334.1 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r2] 2.Turner PL, Lumpkins K, Gabre J, Lin MJ, Liu X, Terrin M. Pregnancy among women surgeons: trends over time. Arch Surg. 2012;147(5):474-479. doi: 10.1001/archsurg.2011.1693 [DOI] [PubMed] [Google Scholar]

[eoi220057r3] 3.Altieri MS, Salles A, Bevilacqua LA, et al. Perceptions of surgery residents about parental leave during training. JAMA Surg. 2019;154(10):952-958. doi: 10.1001/jamasurg.2019.2985 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r4] 4.Javier-DesLoges JF, Cone EB, Smelser WW. A call to action for resident parental leave. Urology. 2020;144:274-275. doi: 10.1016/j.urology.2020.06.028 [DOI] [PubMed] [Google Scholar]

[eoi220057r5] 5.Riska E. Gender and medical careers. Maturitas. 2011;68(3):264-267. doi: 10.1016/j.maturitas.2010.09.010 [DOI] [PubMed] [Google Scholar]

[eoi220057r6] 6.Phillips EA, Nimeh T, Braga J, Lerner LB. Does a surgical career affect a woman’s childbearing and fertility? a report on pregnancy and fertility trends among female surgeons. J Am Coll Surg. 2014;219(5):944-950. doi: 10.1016/j.jamcollsurg.2014.07.936 [DOI] [PubMed] [Google Scholar]

[eoi220057r7] 7.Sullivan MC, Yeo H, Roman SA, Bell RH Jr, Sosa JA. Striving for work-life balance: effect of marriage and children on the experience of 4402 US general surgery residents. Ann Surg. 2013;257(3):571-576. doi: 10.1097/SLA.0b013e318269d05c [DOI] [PubMed] [Google Scholar]

[eoi220057r8] 8.Bering J, Pflibsen L, Eno C, Radhakrishnan P. Deferred personal life decisions of women physicians. J Womens Health (Larchmt). 2018;27(5):584-589. doi: 10.1089/jwh.2016.6315 [DOI] [PubMed] [Google Scholar]

[eoi220057r9] 9.Dundon KM, Powell WT, Wilder JL, et al. ; APPD LEARN Parenthood in Pediatric Residency Study Consortium . Parenthood and parental leave decisions in pediatric residency. Pediatrics. 2021;148(4):e2021050107. doi: 10.1542/peds.2021-050107 [DOI] [PubMed] [Google Scholar]

[eoi220057r10] 10.Stack SW, McKinney CM, Spiekerman C, Best JA. Childbearing and maternity leave in residency: determinants and well-being outcomes. Postgrad Med J. 2018;94(1118):694-699. doi: 10.1136/postgradmedj-2018-135960 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r11] 11.Avendano M, Berkman LF, Brugiavini A, Pasini G. The long-run effect of maternity leave benefits on mental health: evidence from European countries. Soc Sci Med. 2015;132:45-53. doi: 10.1016/j.socscimed.2015.02.037 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r12] 12.Staehelin K, Bertea PC, Stutz EZ. Length of maternity leave and health of mother and child—a review. Int J Public Health. 2007;52(4):202-209. doi: 10.1007/s00038-007-5122-1 [DOI] [PubMed] [Google Scholar]

[eoi220057r13] 13.Huerta MC, Adema W, Baxter J, et al. Fathers’ leave and fathers’ involvement: evidence from four OECD countries. Eur J Soc Secur. 2014;16(4):308-346. doi: 10.1177/138826271401600403 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r14] 14.Accreditation Council for Graduate Medical Education . ACGME institutional requirements, revised July 1, 2018. Accessed October 1, 2021. https://www.acgme.org/globalassets/PFAssets/InstitutionalRequirements/000InstitutionalRequirements2018.pdf?ver=2018-02-19-132236-600&ver=2018-02-19-132236-600

[eoi220057r15] 15.Accreditation Council for Graduate Medical Education . ACGME institutional requirements, revised July 1, 2022. Accessed July 11, 2022. https://www.acgme.org/globalassets/pfassets/programrequirements/800_institutionalrequirements_2022_tcc.pdf

[eoi220057r16] 16.American Board of Medical Specialties . American Board of Medical Specialties policy on parental, caregiver, and medical leave during training. Accessed November 7, 2021. https://www.abms.org/policies/parental-leave/ [DOI] [PubMed]

[eoi220057r17] 17.American Board of Ophthalmology . Requirements for certification. Accessed October 3, 2021. https://abop.org/become-certified/requirements/

[eoi220057r18] 18.Wang KM, Lee B, Woreta FA, et al. Parental leave policy for ophthalmology residents: results of a nationwide cross-sectional study of program directors. J Surg Educ. 2021;78(3):785-794. doi: 10.1016/j.jsurg.2020.08.034 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r19] 19.Humphries LS, Lyon S, Garza R, Butz DR, Lemelman B, Park JE. Parental leave policies in graduate medical education: a systematic review. Am J Surg. 2017;214(4):634-639. doi: 10.1016/j.amjsurg.2017.06.023 [DOI] [PubMed] [Google Scholar]

[eoi220057r20] 20.Rose SH, Burkle CM, Elliott BA, Koenig LF. The impact of parental leave on extending training and entering the board certification examination process: a specialty-based comparison. Mayo Clin Proc. 2006;81(11):1449-1453. doi: 10.4065/81.11.1449 [DOI] [PubMed] [Google Scholar]

[eoi220057r21] 21.Sandler BJ, Tackett JJ, Longo WE, Yoo PS. Pregnancy and parenthood among surgery residents: results of the first nationwide survey of general surgery residency program directors. J Am Coll Surg. 2016;222(6):1090-1096. doi: 10.1016/j.jamcollsurg.2015.12.004 [DOI] [PubMed] [Google Scholar]

[eoi220057r22] 22.Tang AL, Miller A, Hauff S, et al. Maternity and paternity leave in otolaryngology residency training in the US. Laryngoscope. 2019;129(5):1093-1099. doi: 10.1002/lary.27328 [DOI] [PubMed] [Google Scholar]

[eoi220057r23] 23.Hariton E, Matthews B, Burns A, Akileswaran C, Berkowitz LR. Pregnancy and parental leave among obstetrics and gynecology residents: results of a nationwide survey of program directors. Am J Obstet Gynecol. 2018;219(2):199.e1-199.e8. doi: 10.1016/j.ajog.2018.04.017 [DOI] [PubMed] [Google Scholar]

[eoi220057r24] 24.Sharpe EE, Ku C, Malinzak EB, et al. A cross-sectional survey study of US residency program directors’ perceptions of parental leave and pregnancy among anesthesiology trainees. Can J Anaesth. 2021;68(10):1485-1496. doi: 10.1007/s12630-021-02044-9 [DOI] [PMC free article] [PubMed] [Google Scholar]

[eoi220057r25] 25.Blair JE, Mayer AP, Caubet SL, Norby SM, O’Connor MI, Hayes SN. Pregnancy and parental leave during graduate medical education. Acad Med. 2016;91(7):972-978. doi: 10.1097/ACM.0000000000001006 [DOI] [PubMed] [Google Scholar]

[eoi220057r26] 26.Brown EG, Galante JM, Keller BA, Braxton J, Farmer DL. Pregnancy-related attrition in general surgery. JAMA Surg. 2014;149(9):893-897. doi: 10.1001/jamasurg.2014.1227 [DOI] [PubMed] [Google Scholar]

[eoi220057r27] 27.Gupta M, Reichl A, Diaz-Aguilar LD, et al. Pregnancy and parental leave among neurosurgeons and neurosurgical trainees. J Neurosurg. 2020;134(3):1325-1333. doi: 10.3171/2020.2.JNS193345 [DOI] [PubMed] [Google Scholar]

[eoi220057r28] 28.Reilly G, Tipton C, Liberman P, Berkenstock M. Attitudes toward parental leave and breastfeeding during ophthalmology residency. Can J Ophthalmol. 2022;57(3):175-187. doi: 10.1016/j.jcjo.2021.02.039 [DOI] [PubMed] [Google Scholar]

[eoi220057r29] 29.Krause ML, Elrashidi MY, Halvorsen AJ, McDonald FS, Oxentenko AS. Impact of pregnancy and gender on internal medicine resident evaluations: a retrospective cohort study. J Gen Intern Med. 2017;32(6):648-653. doi: 10.1007/s11606-017-4010-5 [DOI] [PMC free article] [PubMed] [Google Scholar]

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PERMALINK

Association Between Parental Leave and Ophthalmology Resident Physician Performance

Dana D Huh, BA

Jiangxia Wang, MS

Michael J Fliotsos, MD

Casey J Beal, MD

Charline S Boente, MD, MS

C Ellis Wisely, MD, MBA

Lindsay M De Andrade, MD

Alice C Lorch, MD, MPH

Saras Ramanathan, MD

Maria A Reinoso, MD

Ramya N Swamy, MD

Evan L Waxman, MD, PhD

Fasika A Woreta, MD, MPH

Divya Srikumaran, MD

Key Points

Question

Findings

Meaning

Abstract

Importance

Objective

Design, Setting, and Participants

Exposures

Main Outcomes and Measures

Results

Conclusions and Relevance

Introduction

Methods

Statistical Analysis

Results

Table 1. Demographic and Preresidency Characteristics for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Table 2. Residency Performance for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Table 3. Postresidency Characteristics for Ophthalmology Residents Graduating From 2015 to 2019, Stratified by Residents Who Took Parental Leave Compared With Those Who Did Not.

Table 4. Resident Characteristics and Residency Performance, Stratified by Female Residents Who Took Parental Leave Compared With All Residents Who Did Not Take Parental Leave.

Discussion

Strengths and Limitations

Conclusions

References

Associated Data

Supplementary Materials

ACTIONS

PERMALINK

RESOURCES

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