Abstract
Purpose
To compare patient and provider satisfaction with saline ultrasound (SIS) versus office hysteroscopy for cavity evaluation prior to in vitro fertilization (IVF) and to assess the capability of hysteroscopy to manage pathology at time of diagnosis to reduce delays and supernumerary procedures.
Methods
This was a randomized, controlled trial in a university fertility clinic. One hundred enrolled subjects undergoing routine uterine cavity evaluation prior to planned embryo transfer were randomized to SIS or office hysteroscopy without anesthesia. Subjects and providers completed surveys about their experience. Subjects with findings on SIS had a hysteroscopy performed or scheduled for further evaluation. Those with hysteroscopy findings had management attempted within the same procedure.
Results
Overall patient satisfaction was high and did not differ between groups, while providers indicated that hysteroscopy provided a better cavity evaluation. There was no difference in time to complete procedures between groups. Pain score on a ten-scale was slightly higher in the hysteroscopy group compared to the SIS group (3.38 ± 1.85 vs. 2.44 ± 1.64, p < 0.01), but this did not impact satisfaction scores. Although pathology was found in a similar rate (22% vs. 36% for SIS and HSC groups, respectively), those in the SIS group all required secondary procedures, while only 1/17 did in the HSC group (p < 0.01).
Conclusion
Although the hysteroscopy group exhibited slightly higher pain scores, overall patient and provider satisfaction was high and similar between groups. There were significantly fewer secondary procedures and delays in the hysteroscopy group. Hysteroscopy is a reasonable first line screening tool for patients requiring cavity evaluation.
Trial registration
Supplementary Information
The online version contains supplementary material available at 10.1007/s10815-021-02065-9.
Keywords: Ultrasound, Office hysteroscopy, Assisted reproduction
Introduction
The process of in vitro fertilization (IVF) often incurs significant financial, time, and labor investments such as clinical evaluations and extensive tests before ultimately culminating in embryo transfer (ET). Standardizing practices to optimize and improve outcomes of each transfer is a primary focus of providers. Among these efforts include widespread use of routine uterine cavity evaluation prior to embryo transfer, given the increased incidence of uterine pathology in infertile woman [1, 2], which has been reported as high as 40% [3]. The purpose of this practice is to identify pathologies that may impact ET success and prospectively manage them in order to achieve greatest likelihood of success [4].
Uterine cavity evaluation methods include transvaginal ultrasonography, hysterosalpingogram (HSG), saline infusion sonography (SIS), and hysteroscopy. SIS is considered superior to transvaginal ultrasound and HSG, demonstrating improved PPV and NPV [5], and is often favored as an office-based imaging modality for this reason. Studies have shown a sensitivity of 75–100% and specificity of 60–100% for the detection of various pathologies using this tool [5, 6]. While hysteroscopy is regarded as the gold standard of uterine cavity evaluation, it has been regarded as more costly and invasive and is often deferred for first line screening [7]. However, one study reported abnormalities on hysteroscopy on nearly 43% of patients with prior negative uterine cavity evaluation [8]. Head to head comparisons have examined SIS versus hysteroscopy in symptomatic patients [9–11] and found comparable diagnostic accuracy. Alternatively, a more recent meta-analysis notes higher false-positive rates with SIS compared to hysteroscopy [12].
With increased access of office hysteroscopy, and data supporting patient satisfaction and tolerability compared to operating room-based hysteroscopy [13], several early studies have compared satisfaction with SIS and office hysteroscopy. A study examining this, performed by Kelecki et al. in 2005, found diagnostic equivalence between SIS and office hysteroscopy, with lower pain scores in the former [14]. This study performed sequential procedures in a relatively small sample size of 50, all of whom were scheduled for hysterectomy for previously identified various gynecologic pathologies. Similarly, Brown et al. also explored this question in 2000, one of few studies focused on infertile women. These findings concluded that while SIS and hysteroscopy demonstrated similar accuracy in 46 subjects, SIS was advantageous due to decreased pain and length of procedure [15].
With respect to pain, van Dongen et al. assessed pain scores predominantly in patients with abnormal uterine bleeding who were randomized to either SIS or office hysteroscopy. They found overall lower pain scores in the SIS group, but no significant difference between groups for severe pain [16]. Additionally, a follow-up study performed by the same investigators in 2011 found that despite the pain score differences, the majority of these same women had a preference for office hysteroscopy if they required uterine cavity evaluation again, citing the possibility for immediate treatment [17].
Significant advancements have evolved in office hysteroscopy in the past two decades, including smaller caliber hysteroscopes, better visualization, and disposable equipment, allowing improved patient and provider experience as well as cost efficiency [18–21]. Optimal patient selection for success of office hysteroscopy has also been examined and elucidated [19, 22]. Perhaps most significantly, office hysteroscope designs have continued to improve to facilitate ease of use, lower cost points, and increase operative function—all factors which may impact both the provider and patient experience with office hysteroscopy.
For women awaiting an embryo transfer, not only are tolerability and duration of the procedure critical but also delays in care and the need for supernumerary procedures are important contributors to overall satisfaction and streamlined care. The primary aim of this study was to compare patient and provider satisfaction with SIS versus office diagnostic hysteroscopy sans anesthesia for routine cavity evaluation prior to in vitro fertilization with modern equipment. The secondary aim of this study was to assess if the frequency of supernumerary procedures could be reduced by utilizing a disposable office hysteroscope with an operative port for immediate intervention in a “see and treat” fashion.
Materials and methods
Patient recruitment and allocation
Approval was obtained through the University of North Carolina (UNC) Institutional Review Board. Calculation of sample size was performed by an assumption of moderate effect size of 0.6, with a power of 80% and alpha of 0.05 to compare means of satisfaction scores. This indicated a required sample size of 45 subjects per group for this effect size, with 5 additional enrolled to account for the possibility of patient dropout. Block randomization scheme in blocks of 10 were performed via electronically generated scheme by validated tool Randomization.com (seed 10,597, 26,551), in order to account for possible improved provider skill or efficiency over time. The randomization scheme was generated with an allocation ratio of 1:1, and subject assignment was performed by the research team according to order of enrollment. Patients requiring routine uterine cavity evaluation prior to embryo transfer were approached for participation from December 2019 through June 2020 at a single university-based fertility clinic. Inclusion criteria were women aged 18–50 years with planned embryo transfer. Exclusion criteria included patients undergoing evaluation for clinically suspected pathology, uncorrected sonographic evidence of abnormality, known history of cervical stenosis, or presence of medical conditions that were a contraindication to in-office procedures (such as bleeding disorder, vaginismus). After informed consent was obtained, subjects were randomized according to the generated scheme. Subject recruitment, allocation, and follow-up are depicted in the Consort diagram (Online Resource 1).
SIS procedure
Subjects randomized to SIS (n = 50) had a speculum placed in order to visualize the cervix. A Rocket IUI catheter was introduced via the cervix into the lower uterine segment. Normal saline was instilled with a 20-ml syringe, and concurrent imaging performed with 2-dimensional (2D) transvaginal ultrasonography. If an abnormality was found, this was recorded, and office or operating room-based hysteroscopy was scheduled for further evaluation and management based on schedule availability. SIS was performed by 5 different providers.
Hysteroscopy procedure
Subjects randomized to hysteroscopy (n = 50) underwent vaginoscopy for location of the cervical os with the 4.2-mm disposable zero-degree LiNA OperåScope with operative port. Only when vaginoscopy was unable to promptly identify the cervix was a speculum utilized (n = 2). The hysteroscope was connected to a 500-ml sterile normal saline bag via standard IV tubing suspended to gravity. The hysteroscope was advanced until the entire cavity and both tubal ostia could be visualized. If an abnormality amenable to immediate intervention was found, hysteroscopic graspers were introduced and used to provide immediate therapeutic intervention. If an abnormality was not amenable to in-office intervention, the procedure was completed. For both groups, patients did not receive any instruction for pre-medication prior to the procedure and no analgesics or anesthetics were administered by the providers before or during either procedure. Two previously trained providers performed the hysteroscopies.
Survey
After completion of assigned procedure, patients and providers completed a survey (Online Resource 2). Patients addressed questions assessing satisfaction with different elements of the procedure (Likert scale) and pain (1–10, with higher scores representing greater pain). Providers recorded findings, need for secondary procedure, ease of use, satisfaction with uterine cavity evaluation, perceived pain control, and overall satisfaction (Likert scale when appropriate). Financial impact of disposable costs for the clinic as well as reimbursement paid by patients and insurance were recorded as well.
Statistics
Population demographics, variables related to patient/provider experience, and outcomes were compared by treatment type (SIS vs. hysteroscopy) with intention to treat. T tests and Fisher’s exact tests were used to assess statistical differences across groups where appropriate. Among those women with a second procedure needed in each treatment group, the proportion who were able to have the additional procedure completed on the same day was tabulated. Additionally, the proportion of women who were able to have their pathology completely resolved among those with hysteroscopies was assessed. In this analysis, the single subject with a unicornuate uterus was excluded as a resolution was not applicable.
Lastly, the financial variables associated with the procedures were examined. Women were categorized as either receiving SIS treatment, a diagnostic hysteroscopy, or an operative hysteroscopy based on presence/absence of a detected pathology. Due to the non-normal distribution of the financial variables, statistical differences were assessed using the Wilcoxon rank-sum test. p values were generated for SIS vs. diagnostic hysteroscopy and for SIS vs. operative hysteroscopy. All analyses were conducted in SAS 9.4 (Cary, NC).
Results
The demographic characteristics of the SIS and hysteroscopy groups are summarized in Table 1. There were no significant differences in age, BMI, or infertility diagnosis. Additionally, there was no difference in presence of risk factors for pathology or hysteroscopy failure between groups, including prior uterine or cervical procedures, prior uterine pathology, or parity. Fifty participants were randomized to each group, and none were secondarily excluded or lost to follow-up.
Table 1.
Participant demographics
| Demographics | SIS (n = 50) | Hysteroscopy (n = 50) | p value |
|---|---|---|---|
| N (%) or mean (± SD) | |||
| Age (years) | 34.7 (± 4.9) | 33.9 (± 4.6) | 0.40 |
| Race | 0.19 | ||
| Caucasian | 39 (78.0) | 42 (84.0) | |
| African American | 6 (12.0) | 5 (10.0) | |
| Asian | 1 (2.0) | 3 (6.0) | |
| Hispanic | 4 (8.0) | 0 (0) | |
| BMI (kg/m2) | 27.7 (± 6.4) (n = 45) | 26.2 (± 6.4) | 0.26 |
| Infertility diagnosis | 0.31 | ||
| DOR | 7 (14.0) | 3 (6.0) | |
| Endometriosis | 1 (2.0) | 3 (6.0) | |
| Ovulatory dysfunction | 7 (14.0) | 10 (20.0) | |
| Male factor | 10 (20.0) | 17 (34.0) | |
| Tubal factor | 4 (8.0) | 1 (2.0) | |
| Unexplained | 13 (26.0) | 10 (20.0) | |
| Other | 8 (16.0) | 6 (12.0) | |
| Pregnancy history | |||
| Nulliparous | 34 (68.0) | 34 (68.0) | 1 |
| Prior vaginal delivery | 11 (22.0) | 9 (18.0) | 0.80 |
| Prior failed IUP | 17 (34.0) | 12 (24.0) | 0.38 |
| Prior uterine surgery (any) | 17 (34.0) | 14 (28.0) | 0.71 |
| D and C | 9 (18.0) | 4 (8.0) | 0.23 |
| Myomectomy | 2 (4.0) | 4 (8.0) | 0.68 |
| Polypectomy | 2 (4.0) | 0 (0) | 0.49 |
| LOA | 0 (0) | 0 (0) | - |
| Cesarean | 7 (14.0) | 7 (14.0) | 1 |
| Other | 0 (0) | 1 (2.0) | 1 |
| Prior cervical surgery | |||
| LEEP | 1 (2.0) (n = 49) | 1 (2.0) | 1 |
| History of uterine pathology (any) | 4 (8.0) | 2 (4.0) | 0.68 |
| None | 46 (92.0) | 48 (96.0) | 0.68 |
| Polyp | 2 (4.0) | 0 (0) | 0.49 |
| Myoma | 3 (6.0) | 2 (4.0) | 1 |
| Adhesions | 0 | 0 | - |
| RPOC | 0 | 0 | - |
Mean comparisons by T test. Categorical variables were compared using Fisher’s exact test
“Other” infertility diagnosis includes gestational carrier, uterine factor, recurrent pregnancy loss, and same sex
The mean age of study participants was 34.3 ± 4.7 years, and mean BMI was 26.9 ± 6.4 kg/m2. The most common infertility diagnoses were unexplained and male factor. The mean length of procedure was similar between groups and was 4.0 ± 2.0 min for SIS and 4.6 ± 2.4 min for hysteroscopy (p = 0.16). For hysteroscopy patients who received an intervention, the mean time was 5.2 ± 2.3 min, compared to 4.3 ± 2.0 min for those that did not (p = 0.20).
A summary of patient and provider survey results is presented in Table 2. Pain score on a ten-point scale, with a score of ten correlating with the greatest pain, was slightly higher in the hysteroscopy compared to the SIS group (3.4 ± 1.9 vs. 2.4 ± 1.6, p < 0.01). Only three patients pre-medicated with oral analgesics at their own discretion, one in the SIS group and two in the hysteroscopy group. Overall patient satisfaction was similar between groups on a Likert scale with a score of five indicating greatest satisfaction (SIS 4.8 ± 0.5 vs. hysteroscopy 4.9 ± 0.3, p = 0.57). Provider survey results were similar, with slightly improved cavity evaluation scores with office hysteroscopy. Pathology was observed at a similar rate between groups (22% vs. 36% for SIS and hysteroscopy groups, respectively; p = 0.1). The most common pathology noted in both groups was endometrial polyps (17 subjects), followed by retained products of conception (6 subjects), and intrauterine adhesions (4 subjects). Example images from subjects are depicted in Figs. 1 and 2.
Table 2.
Primary and secondary outcomes by intention to treat. Top range of scale used depicted in parentheses after each variable. For pain scores, 1 correlated with the least amount of pain and 10 the greatest. For ease of procedure and likelihood to recommend to friend scores, 1 represented the least favorable scoring and 10 the highest. The remaining scores are on a 5-point Likert scale, with 5 depicting the greatest satisfaction
| SIS (n = 50) | Hysteroscopy (n = 50) | p value | |
|---|---|---|---|
| Time to complete (minutes)* | 3.98 (± 2.03) | 4.61 (± 2.42) | 0.16 |
| Patient satisfaction (scale) | |||
| Pain score (10)* | 2.44 (± 1.64) | 3.38 (± 1.85) | < 0.01 |
| Recommend to friend (10)* | 9.02 (± 1.96) | 9.44 (± 1.40) | 0.22 |
| Overall satisfaction (5)‡ | 4.84 (± 0.47) | 4.92 (± 0.34) | 0.57 |
| Satisfaction time to complete (5)‡ | 4.88 (± 0.52) | 4.92 (± 0.34) | 1 |
| Provider satisfaction (scale) | |||
| Ease of procedure (10)* | 9.20 (± 1.40) | 8.74 (± 1.89) | 0.17 |
| Uterine cavity evaluation (5)‡ | 4.70 (± 0.54) | 4.84 (± 0.62) | 0.04 |
| Perception of pain (5)‡ | 4.74 (± 0.66) | 4.70 (± 0.61) | 0.13 |
| Overall satisfaction (5)‡ | 4.56 (± 0.81) | 4.76 (± 0.69) | 0.11 |
| Pathology found‡ | |||
| Total | 11 (22.0) | 18 (36.0) | 0.12 |
| Polyp | 7 (14.0) | 10 (20.0) | |
| Myoma | 1 (2.0) | 0 (0) | |
| Adhesions | 2 (4.0) | 2 (4.0) | |
| RPOC | 1 (2.0) | 5 (10.0) | |
| Uterine anomaly | 0 (0) | 2 (4.0) | |
| Inconclusive | 1 (2.0) | 0 (0) | |
| Second procedure needed‡ | 11 (22.0) | 1 (2.0) | < 0.01 |
| Ability to complete second procedure same day | 5/11 (45.5) | 1/1 (100) | |
| Ability to completely resolve pathology | n/a | 16/17† | n/a |
*T test
‡Fisher’s exact test
†Unicornuate uterus excluded from denominator, as “resolution” not applicable. Single unresolved case was ostia obstructed by adhesions. LOA performed, but ostia not clearly visualized
Fig. 1.
Abnormalities detected with office hysteroscopy and SIS. Top row: retained products of conception, endometrial polyp, intrauterine synechiae, and unicornuate uterus. Bottom row: retained products of conception, multiple polyps, intrauterine synechiae, and intramural fibroid impinging on uterine cavity
Fig. 2.
Comparative cavity evaluation. Both subjects were randomized to SIS and received office hysteroscopy after detection of abnormality on the initial screen. Left column depicts endometrial polyp in one patient in SIS (top) and hysteroscopy (bottom). Right column depicts a second patient, with copious circumferential polypoid tissue in SIS (top) and hysteroscopy (bottom)
Of note, 11 (22%) of patients in the SIS group required a secondary procedure, compared to one (2%) patient in the hysteroscopy group (p < 0.01). Of the SIS subjects requiring a secondary procedure, 54.5% required scheduling of additional appointment due to scheduling constraints, constituting a delay. The others were able to be performed the same day with the same equipment used in the hysteroscopy arm. Only one subject required intervention in the operating room. Two of the 11 subjects in the SIS group with positive findings had subsequent negative hysteroscopy, indicating false-positive screening with SIS. The one subject in the hysteroscopy group that required a secondary procedure was due to a narrow cervical os and inability to enter the cavity with the hysteroscope. She underwent immediate subsequent successful SIS.
Since screening with office hysteroscopy was not routinely performed in the practice prior to this study, results between early study procedures versus late were compared to account for increased provider experience with office hysteroscopy over time. Providers did not report different satisfaction or ease of procedure scores for the first 25 hysteroscopies compared to the second 25, and time to complete was similar.
Table 3 summarizes differences in insurance paid and patient paid costs in each group. As these procedures were performed as a screening test without suspicion for pathology under an infertility diagnosis code, 45.2% of office hysteroscopy patients and 32.5% of SIS patients had no insurance contribution. For self-pay patients, the charge was the same and these were excluded. For patients with insurance coverage, charges were determined by the Center for Medicare and Medicaid fee schedule. While total charges were higher in the hysteroscopy group, there was no significant difference in patient paid costs for those receiving diagnostic hysteroscopy. For patients requiring intervention and conversion to operative hysteroscopy, overall charges were significantly higher, but reimbursement paid by patient were significantly lower due to insurance coverage and overall reimbursement was significantly higher to the clinic (Table 3). On average, patients who had a combined screening and intervention procedure incurred less costs than those with screening alone or sequential screening and interventional procedures, suggesting a financial advantage to this approach.
Table 3.
Charge differences of saline ultrasound compared to hysteroscopic approaches in patients with insurance coverage
| Mean charges | Charge difference (diagnostic hysteroscopy) | p value* | Charge difference (operative hysteroscopy) | p value* |
|---|---|---|---|---|
| Total amount charged | $47.30 | p < 0.01 | $994.20 | p < 0.01 |
| Amount paid by patient | − $68.60 | 0.13 | − $50.70 | 0.04 |
| Amount paid by insurance | $128.60 | p < 0.01 | $1306.40 | p < 0.01 |
The mean amount charged, and amount covered by insurance was higher in both diagnostic and operative hysteroscopy compared to saline ultrasound. The net result was that patients receiving SIS did not incur significantly different costs than those receiving hysteroscopy
After exclusion of patients with no insurance coverage, SIS (n = 27), diagnostic hysteroscopy (n = 16), operative hysteroscopy (n = 14)
*Wilcoxon rank-sum test was used to test for differences in distributions
Discussion
Similar to earlier studies when sequential tests were performed in patients with suspected pathologies, pain scores were again noted to be slightly higher in the office hysteroscopy group compared to SIS [14, 15]. However, this was approximately a one point out of 10 difference between groups on the lower end of the scale, indicating likely limited clinical significance. Additionally, this did not reflect in satisfaction scores for patients or providers, as those were high and did not differ between the two study arms. In concert with the findings of van Dongen et al. [17], the relative lack of severe pain resulted in overall equal satisfaction with the hysteroscopy despite the statistical difference in pain scores. By immediate survey, this study was also able to avoid recall bias, and more closely assess the immediate patient experience in a refined group of asymptomatic women with infertility. Additionally, this data provides perspective on an asymptomatic infertile population, while the majority of prior studies examined women with abnormal uterine bleeding and overt uterine pathology. This study also provides an updated comparison of these imaging modalities, using a small caliber hysteroscope with operative capabilities, which was previously unavailable.
In contrast to previous studies, a difference in length of screening procedures was not appreciated between SIS and hysteroscopy, likely reflecting advancements in hysteroscopic technology. All procedures in this study were scheduled in 15-min appointments, which included procedure setup and operative procedure should one be needed in the hysteroscopy group. A particular advantage of this study is providing additional information about necessity of future procedures, allowing for more complete assessment of the advantages of offering immediate intervention.
Overall, frequency of observed pathology between the two groups was similar. The SIS group experienced greater false positives and supernumerary procedures than the hysteroscopy group. For subjects with pathology visualized, 16/17 patients in the hysteroscopy group were able to achieve resolution of that pathology within the same procedure, reducing need for treatment or office delays. Notably, of the 28 total subjects requiring additional intervention in either group, only one required intervention in the operating room, suggesting a significant majority of patients undergoing screening can experience resolution of pathology with office hysteroscopy alone, and further supporting the use of this tool.
Interestingly, six out of 29 patients with prior pregnancy loss demonstrated retained products of conception, nearly 21%. While this study was not designed to specifically identify risk factors for finding asymptomatic pathology, this finding suggests that patients with prior intrauterine pregnancy losses may specifically benefit from the option of intervention at time of uterine cavity screening.
This study showed that office hysteroscopy is profitable even with disposable instrumentation, especially if there is a significant prevalence of removable pathology. It is difficult to extrapolate the financial data to a broader population, due to varying insurance plans and state policies on coverage for infertility-related testing. However, in a state without mandated coverage, there appears to be little financial difference to patients between screening procedures. As mentioned above, for those requiring additional intervention, there is significant advantage to a one-step approach.
Strengths of this study include the use of a randomized controlled trial and block randomization. This study did not utilize any clinic administered anesthesia or analgesia, allowing for unmedicated assessment of pain scores. The instruments used in this study were disposable, with low capital costs, minimal required training in setup or use, and low staff utilization, describing an easily attainable model for office hysteroscopy. Additionally, about 20% of procedures were performed by trainees in this academic practice, supporting that applicability of this approach without extensive specialized pre-existing experience.
Limitations of this study include that patients with pre-existing clinical suspicion for uterine pathology, such as abnormal uterine bleeding, recent imaging suggesting cavitary involvement of leiomyomata or retained products, were not enrolled. While our findings support hysteroscopy screening in low-risk individuals, further studies are necessary to determine if these findings are consistent in a higher risk population. 2D SIS was utilized, and therefore, the possible advantages in sensitivity and specificity of 3D SIS cannot be compared to hysteroscopy in this study. Furthermore, different fluid instillation methods were utilized for SIS and hysteroscopy (syringe vs. bag), and the contribution of these to pain scores cannot be ascertained from this study. There is also a possibility for selection bias, with patients with prior negative experiences with pelvic procedures deferring enrollment in our study. Lastly, only one type of office hysteroscopy was used, and findings may differ with different equipment.
In conclusion, for IVF patients without explicit clinical suspicion for uterine pathology, office hysteroscopy provides a comparable patient and provider experience compared to SIS for screening evaluation of the uterine cavity. Length of procedure and overall satisfaction scores did not differ between groups. Additionally, office hysteroscopy may be a favorable choice due to the opportunity to “see and treat”, reducing delays and anxieties for patients awaiting embryo transfer and reducing costs of supernumerary procedures. Conversion to operative hysteroscopy did not alter satisfaction or pain scores when used in this study. With reduced need of costly equipment, improved reimbursement, comparable patient experience, and increased functional capacity, office hysteroscopy can be considered as a primary screening tool in the asymptomatic infertile population planning IVF.
Supplementary information
Online Resource 1 Consort flow diagram depicting subject enrollment and follow up. (PNG 290 kb).
(DOC 219 kb).
(DOCX 16 kb).
Code availability
Not applicable.
Data availability
Data are available upon request with appropriate institutional ethics approval.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
This study was prospectively approved by the University of North Carolina Institutional Review Board.
Consent to participate
All patients signed informed consents to participate in this trial.
Consent for publication
All patients and providers consented to publication of the results of this trial.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Online Resource 1 Consort flow diagram depicting subject enrollment and follow up. (PNG 290 kb).
(DOC 219 kb).
(DOCX 16 kb).
Data Availability Statement
Data are available upon request with appropriate institutional ethics approval.