Pelvic organ prolapse (POP) leads to considerable symptomatic distress and reduced quality of life among women.1 2 Large-scale studies of women in the United States and Europe have shown that the risks of undergoing POP or stress urinary incontinence (SUI) surgery by 80 years of age range from 12.6% to 18.7%.3 4 5 Advanced POP stage and worse quality of life are factors that increase the likelihood of surgical treatment.2 Symptom resolution is the most important goal among women who seek consultations for POP.6 Importantly, quality of life improves in women who undergo surgical treatment.7 However, there is a high mean recurrence rate after POP surgery: 36% after a follow-up interval of 0.1 to 10 years. Reoperation is also common (29.2%) and the between-procedure interval decreases with successive repairs.3 8

A systematic review and meta-analysis of 25 randomised controlled trials revealed that, compared with native tissue repair, transvaginal mesh surgery for anterior compartment prolapse has reduced risks of awareness of prolapse (risk ratio=0.66, 95% confidence interval=0.54-0.81), recurrent prolapse (risk ratio=0.4, 95% confidence interval=0.3-0.53), and repeat surgery for prolapse (risk ratio=0.53, 95% confidence interval=0.31-0.88) over 1 to 3 years of follow-up.9 However, transvaginal mesh surgery carried an increased risk of repeat surgery for a composite outcome of prolapse, SUI, and mesh erosion (risk ratio=2.4, 95% confidence interval=1.51-3.81). Considering this risk-benefit profile, the authors concluded that transvaginal mesh has limited utility in primary surgery; however, the quality of analysed evidence only ranged from very low to moderate. Among the randomised controlled trials considered in that systematic review, only one was conducted in Asia. Moreover, high objective and subjective cure rates of transvaginal mesh and a low mesh erosion rate have been reported over 5 to 7 years of follow-up, although some studies have had a high rate of loss to follow-up.10 11 12

The present study was performed to evaluate the long-term outcome of transvaginal mesh surgery for advanced anterior compartment prolapse in a tertiary centre. It also investigated the recurrence rate and the types of postoperative complications among women who underwent transvaginal mesh surgery.

This was a retrospective analysis of prospectively collected data concerning transvaginal mesh reconstructive surgeries performed for POP treatment from January 2008 to June 2019 in a urogynaecology training centre. Ethics approval was obtained (CREC 2015.125); the ethics committee waived the requirement for informed consent. All women who underwent transvaginal mesh surgery in the study centre were recruited. Demographic data, including age, parity, mode of delivery, urinary symptoms (eg, SUI and/or urgency urinary incontinence [UUI]), and symptoms of prolapse were collected during the first consultation; the Pelvic Organ Prolapse Quantification assessment was also performed.13 Management options of vaginal ring pessary and surgery were offered. For women who chose surgery, a urodynamic study was arranged.

Transvaginal mesh surgery (ie, anterior vaginal mesh or total vaginal mesh) was available to women with stage III or IV anterior and apical and posterior compartment prolapse, age ≥65 years, and (preferably) sexual inactivity, or with recurrent POP. Beginning in January 2013, vaginal mesh insertion in the posterior compartment was not performed because of published evidence indicating no improvement from posterior vaginal mesh, compared with native tissue repair alone.14 Transvaginal mesh was performed with concomitant vaginal hysterectomy or a uterine-preserving operation depending on each woman’s choice and medical condition. In women with stage III or IV apical compartment prolapse, concomitant bilateral sacrospinous fixation was performed. Because of variations in commercial product availability, Prolift^®, Perigee^®, and Restorelle^® were used from 2008 to 2012, 2013 to August 2017, and September 2017 to June 2019, respectively.

Women were admitted on the day of the operation. One dose of prophylactic intravenous antibiotics was administered on induction. The operation was performed under either spinal or general anaesthesia depending on each woman’s choice and the attending anaesthetist’s assessment. For women who chose hysterectomy, the operation began with vaginal hysterectomy, followed by hydrodissection with adrenaline solution and midline incision over the anterior vaginal wall. Subsequent dissection of the bladder from the anterior vaginal wall was performed; the sacrospinous ligament was reached without opening the posterior vaginal wall. Sacrospinous ligament fixation was conducted using a Mayo-hook from 2008 to 2017; it was conducted using a Capio device^® from 2018 to 2019. Depending on the mesh design, anterior mesh was introduced and all arms either passed through the obturator membranes (Prolift^® and Perigee^®) or were fixed to the ipsilateral pelvic wall and sacrospinous ligament using stitches (Restorelle^®). Anterior mesh was then attached to the bladder fascia and anterior vaginal wall using absorbable stitches. If total vaginal mesh was performed, the posterior vaginal wall was opened at the midline and the sacrospinous ligament was identified; the arms of posterior mesh were introduced to the sacrospinous ligaments. Cystoscopy was performed to exclude bladder injury and confirm ureteric jets. Per rectal examination was performed to exclude rectal perforation. Only the edge of the vaginal epithelium was trimmed; the anterior vaginal wall was closed by three interrupted stitches at the distal region, followed by continuous sutures. In the event of symptomatic posterior compartment prolapse, posterior colporrhaphy was performed. Concomitant continence surgery (ie, mid-urethral sling) was performed for women with urodynamic stress incontinence (USI). At the end of the operation, one piece of vaginal gauze soaked with chlorhexidine solution was packed into the vagina and a transurethral Foley catheter was placed. Most vaginal hysterectomies were performed by gynaecology trainees; all procedures involving mesh were performed by urogynaecologists or urogynaecology subspecialty trainees under direct supervision by urogynaecologists. Operative details including anaesthesia type, operative time, blood loss, and any organ injuries were collected from electronic operative notes that were completed by surgeons immediately after the operation.

Oral intake was resumed on the day of the operation. Standard oral paracetamol were administered. One course of antibiotics was administered to women with a high risk of infection (eg, patients with diabetes mellitus and/or a prolonged operation) and women with postoperative fever that persisted for more than 24 hours. The vaginal gauze and Foley catheter were removed on the day after the operation. Women were discharged from day 1 onwards if they resumed a normal diet, voided well, and remained afebrile.

Women were followed up once at 2 to 4 months, then annually until 5 years after surgery. Subsequently, if they had no active pelvic floor symptoms, they were discharged from the clinic. Earlier follow-up was offered on request. During follow-up examinations, the attending gynaecologist specifically asked women about symptoms of prolapse, SUI, UUI, vaginal bleeding, pain, and dyspareunia, as well as the severity of such symptoms. Vaginal examinations were performed to assess any recurrence of prolapse or mesh erosion, in accordance with recommendations of the International Urogynecological Association and International Continence Society.15 16 Satisfaction (ie, very unsatisfied, unsatisfied, satisfied, or very satisfied) was recorded during each postoperative visit. Subjective recurrence was defined as reported symptoms of prolapse, vaginal bulge, or dragging sensation. Objective recurrence was defined by the Pelvic Organ Prolapse Quantification assessment with any compartment reaching ≥1 cm above the hymen (stage ≥II). In the event of mesh erosion, the location, size, and area of mesh erosion were recorded. Vaginal oestrogen cream was offered. The options of conservative management or surgical excision of exposed mesh were discussed with women who experienced mesh erosion, depending on the erosion severity, accompanying symptoms, and their personal preferences.

If women reported symptoms of SUI or UUI, a urodynamic study was offered. If USI was diagnosed, tension-free vaginal tape surgery was offered to women for whom pelvic floor exercises were ineffective. Medical treatment was offered to women with overactive bladder or detrusor overactivity.

SPSS software (Windows version 21.0; IBM Corp, Armonk [NY], United States) was used to analyse the collected data. Categorical data are shown using descriptive statistics. Normally distributed data are shown as means (standard deviations), whereas non-normally distributed data are shown as medians (ranges). The times to subjective and objective recurrences were depicted using Kaplan–Meier curves. A P value of <0.05 was considered statistically significant.

In total, 183 women (mean age, 71.8 ± 8.4 years) underwent transvaginal mesh surgery. Nearly all were Hong Kong Chinese women, with the exception of two who were non-Chinese Asian women. The characteristics of the overall cohort are shown in the Table.

The operative procedures and hospital stay are summarised in the Table. Forty-six (25.1%) women had spinal anaesthesia. The mean operative time was 122.9 ± 40.7 minutes and the mean blood loss was 193 ± 155 mL. Three (1.6%) women required blood transfusion. One woman had bladder injury during the trocar insertion of the anterior vaginal mesh; the involved trocar was immediately removed and reinserted in the correct surgical plane. Cystoscopy showed a small perforation site at the lateral bladder wall, but no repair was required. The woman recovered uneventfully. One woman had a mesh infection with abscess formation in the vulva, requiring removal of the anterior mesh on day 18. The infection subsided with antibiotics and drainage, but the woman died 7 weeks after surgery because of other medical morbidities.17

Overall, one woman was lost to follow-up and three women, including the woman mentioned above, died of medical diseases within 1 year; thus, 179 (97.8%) women were eligible for the postoperative outcome analysis. Of these 179 women, 23 (12.8%) underwent operation within 1 year prior to this report, while 156 (87%), 113 (63%), and 77 (43%) had completed 1, 3, and 5 years of follow-up, respectively. The mean duration of follow-up was 50 ± 22 months. There were no differences in demographics, preoperative symptoms, stage and compartment of prolapse, or operative data between the 23 women with <1 year of follow-up and the 156 women with ≥1 year of follow-up, except for the vaginal mesh brand (because of variations in commercial product availability) and the duration of follow-up (Table).

Among the 156 women with ≥1 year of follow-up, eight reported symptoms of prolapse recurrence (subjective recurrence rate of 5.1%). Five women had stage II POP, while three women had stage III POP. Four women experienced recurrence in the first year of follow-up; two, one, and one additional women experienced recurrence in the second, third, and fourth year of follow-up, respectively. While five women with recurrence had conservative treatment for POP, one woman had vaginal pessary and two (1.3%) women had surgery to manage prolapse recurrence. In addition, nine other women had asymptomatic stage II POP: two had anterior compartment prolapse and seven had posterior compartment prolapse. The objective recurrence rate was 10.9% (n=17). The mesh erosion rate was 9.6% (n=15). In all, 40% of the erosions (n=6) occurred at the posterior wall; the remaining erosions occurred at other sites in the vagina (four anterior wall, four vaginal vault, and one lateral wall). Most instances of mesh erosion (n=8, 53.3%) occurred in the first year. Ten of the 15 affected women underwent surgical excision under local anaesthesia at the bedside; seven, one, and two women required one, two, and three surgical excisions, respectively. The times to subjective and objective recurrences are depicted using Kaplan–Meier curves (Fig 1).

The preoperative and postoperative symptoms of SUI are listed in Figure 2. Occult USI was observed in 11 (16.2%) of 68 women who reported no SUI before the operation. Among four women who had occult USI and did not undergo continence surgery, two had postoperative SUI; they did not require surgical treatment. De novo SUI occurred in 12 (7.7%) women. Only one (1/53, 1.9%) woman received tension-free transvaginal tape (transobturator route) [TVT-O] for treatment of SUI; the remaining 11 women had mild symptoms or achieved improvement with pelvic floor exercise. Among the 31 women who had preoperative SUI but normal urodynamic study findings and did not undergo continence surgery, 19 (61.2%) women had postoperative SUI. Among them, two received TVT-O afterwards. Overall, 22 (14%) women had de novo UUI: seven received anticholinergics and the remaining 15 had conservative treatment. No women reported vaginal pain, pelvic pain, or dyspareunia.

In summary, the total re-operation rate was 9.6%: two women for recurrent POP, 10 women for mesh erosion, three women for TVT-O, and one woman for de novo SUI. In all, 103 (66%) women and 50 (32.1%) women were ‘satisfied’ and ‘very satisfied’, respectively, with the operation at their latest follow-up examination. Three women who ever had recurrence did not report being ‘satisfied’ or ‘very satisfied’.

This study provided a comprehensive evaluation of the intermediate- to long-term (ie, 3 to 5 years) outcomes of transvaginal mesh surgery in women with advanced POP. Risk factors for POP recurrence reportedly include levator ani muscle avulsion (odds ratio=2.8), preoperative stage III-IV POP (odds ratio=2.1), family history (odds ratio=1.8), and large hiatal area (odds ratio=1.06 per 1 cm²).8 The prevalence of levator ani muscle avulsion is higher in women with more advanced POP: we previously reported that 54.5% and 66.7% of women with stage III and IV POP had levator ani muscle avulsion, respectively.18 Although this factor was not evaluated in the present study, we presume that a similar proportion of our cohort would have this condition, placing them at high risk of POP recurrence. Indeed, transvaginal mesh repair leads to a lower rate of anterior compartment prolapse recurrence, compared with native tissue repair in women with levator ani muscle avulsion.19 20

Transvaginal mesh was not recommended in a systematic review and meta-analysis of 25 randomised controlled trials, based on its risk-benefit profile. The risk of awareness of prolapse was 13%; the risks of repeat surgery for prolapse and SUI were 1.8% and 2.9%, respectively.9 However, if the transvaginal mesh treatment efficacy remains high over a longer follow-up period and the risk of morbidity is low, the above recommendation may not apply to all women. In our cohort, these risks were 5.1%, 1.3%, and 1.9% for a mean follow-up period of 50 months. This indicates a tendency towards lower POP recurrence risks in our cohort. The objective recurrence rate of 10.6% also tended to be lower, compared with previous studies that recruited women who had stage II POP8, although 95% of our women had stage III or IV POP. Our subjective and objective recurrence rates are similar to the rates in other Asian centres in the past decade.10 11

Apical compartment prolapse is more prevalent among women in Hong Kong, compared with Caucasian women.18 21 Furthermore, apical support is important in the management of anterior compartment prolapse, which comprises impairment of the pubovisceral muscle and the uterosacral and cardinal ligaments.10 22 23 Thus, we performed concomitant sacrospinous fixation to suspend the vaginal vault among women in this study; this additional procedure did not increase perioperative morbidity. This may explain why the vaginal vault was not commonly involved in women who had subjective or objective recurrence of POP in the present study. Most women with objective recurrence had stage II posterior compartment prolapse, but they were asymptomatic.

The mesh erosion rate was 9.6%; 40% of erosions were caused by posterior vaginal mesh. The erosion rate for anterior vaginal mesh alone was 5.8%; this was comparable with previously reported rates of 2.7% to 20%, with a mean of 11.1%.10 11 24 25 26 Furthermore, our rate was similar to other Asian centres where a low mesh erosion rate was reported.10 11 Most instances of erosion in our study occurred within the first or second year of follow-up; approximately two-thirds of the affected women underwent excision of the exposed part of the mesh and repair of the vaginal epithelium under local anaesthesia at the bedside.17 Among the various types of possible mesh complications, Warembourg et al24 reported that mesh erosion was the most common complication that required re-operation; however, it was also treated most effectively. However, more serious complications could occur, such as erosion into the urinary tract or bowel.24 No instances of vaginal pain or dyspareunia were reported in our cohort, in contrast to previous findings26; this was presumably because we mainly offered transvaginal mesh surgery to women who were sexually inactive. The proportion of women with POP who report sexual inactivity is generally high (64%) in Hong Kong.27 Further research is needed to determine whether ethnicity contributes to vaginal pain or dyspareunia after transvaginal mesh surgery.

Preoperative urodynamic studies showed that, of 68 women who did not report SUI, 16% and 6% had occult USI and other diagnoses, respectively; thus, only 53 (78%) women had no abnormal findings. De novo SUI occurred in 12 of these 53 women (7.7% of all 156 women with ≥1 year of follow-up); only one woman requested continence surgery. Although some women reported symptoms of SUI, our policy was not to offer continence surgery if no USI was evident during the urodynamic study. Of the remaining 31 of 53 women with no abnormal findings, only two subsequently required continence surgery. Overall, repeat surgery for SUI only occurred in three (1.9%) women; we regarded this as a low risk of repeat surgery. Preoperative urodynamic studies and our more conservative approach (ie, not frequently offering continence surgery) might have reduced the risk of long-term complications. However, treatment was offered to women with preoperative clinically bothersome USI. Women who received concomitant TVT-O were satisfied with this management.

This study had some limitations. First, this was a single-centre study with a moderate sample size. However, the data were collected prospectively using a standardised form. Second, a health-related quality of life questionnaire was not used because validated questionnaires were unavailable when transvaginal mesh surgery first began in our centre; thus, no data were available for some women.1 We plan to investigate these data in a future study. Finally, the effects of sexual function on the surgical outcomes were not explored because most women in this cohort were sexually inactive. We did not recommend transvaginal mesh surgery to women who were sexually active because there were increased risks of mesh erosion and dyspareunia.

Women with stage III or IV POP experienced a benefit from transvaginal anterior mesh surgery (and concomitant sacrospinous fixation if concomitant stage III/IV apical compartment prolapse) with low risks of subjective recurrence of POP (5.1%), objective recurrence of POP (10.9%), and re-operation for POP recurrence (1.3%) at a mean follow-up interval of 50 months. Although some women required re-operations because of various factors (eg, POP recurrence, SUI, and mesh erosion), the overall re-operation rate was 9.6%. Most women were satisfied or highly satisfied with the transvaginal mesh surgery. This type of surgery may be suitable for women with POP who are sexually inactive, particularly women who have a higher risk of recurrence related to conditions such as advanced POP and levator ani muscle avulsion.

Concept or design: All authors.
Acquisition of data: SSC Chan, OYK Wan, RYK Chung.
Analysis or interpretation of data: All authors.
Drafting of the manuscript: SSC Chan.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

All authors have disclosed no conflicts of interest.

The authors would like to thank Miss Loreta Lee for data collection and data entry for this research.

Portions of the results were presented in the 26th Asia and Oceania Federation of Obstetrics and Gynecology (AOFOG) Congress in the Philippines in 2019, during a talk that received the “Best Oral Presentation” award in the Urogynaecology session.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Ethics approval was obtained from The Joint Chinese University of Hong Kong–New Territories East Cluster Clinical Research Ethics Committee (Ref: CREC 2015.125). The requirement for written informed consent was waived by the ethics board.

1. Chan SS, Cheung RY, Yiu AK, et al. Chinese validation of pelvic floor distress inventory and pelvic floor impact questionnaire. Int Urogynecol J 2011;22:1305-12. Crossref

2. Chan SS, Cheung RY, Yiu KW, Lee LL, Pang AW, Chung TK. Symptoms, quality of life, and factors affecting women’s treatment decisions regarding pelvic organ prolapse. Int Urogynecol J 2012;23:1027-33. Crossref

3. Olsen AL, Smith VJ, Bergstrom JO, Colling JC, Clark AL. Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 1997;89:501-6. Crossref

4. Wu JM, Matthews CA, Conover MM, Pate V, Funk MJ. Lifetime risk of stress urinary incontinence or pelvic organ prolapse surgery. Obstet Gynecol 2014;123:1201-6. Crossref

5. Løwenstein E, Ottesen B, Gimbel H. Incidence and lifetime risk of pelvic organ prolapse surgery in Denmark from 1977 to 2009. Int Urogynecol J 2015;26:49-55. Crossref

6. Lowenstein L, FitzGerald MP, Kenton K, et al. Patient-selected goals: the fourth dimension in assessment of pelvic floor disorders. Int Urogynecol J Pelvic Floor Dysfunct 2008;19:81-4. Crossref

7. Chan SS, Cheung RY, Lai BP, Lee LL, Choy KW, Chung TK. Responsiveness of the Pelvic Floor Distress Inventory and Pelvic Floor Impact Questionnaire in women undergoing treatment for pelvic floor disorders. Int Urogynecol J 2013;24:213-21. Crossref

8. Friedman T, Eslick GD, Dietz HP. Risk factors for prolapse recurrence: systematic review and meta-analysis. Int Urogynecol J 2018;29:13-21. Crossref

9. Maher C, Feiner B, Baessler K, Christmann-Schmid C, Haya N, Marjoribanks J. Transvaginal mesh or grafts compared with native tissue repair for vaginal prolapse. Cochrane Database Syst Rev 2016;(2):CD012079. Crossref

10. Lo TS, Pue LB, Tan YL, Wu PY. Long-term outcomes of synthetic transobturator nonabsorbable anterior mesh versus anterior colporrhaphy in symptomatic, advanced pelvic organ prolapse surgery. Int Urogynecol J 2014;25:257-64. Crossref

11. Dong S, Zhong Y, Chu L, Li H, Tong X, Wang J. Agestratified analysis of long-term outcomes of transvaginal mesh repair for treatment of pelvic organ prolapse. Int J Gynecol Obstet 2016;135:112-6. Crossref

12. Meyer I, McGwin G, Swain TA, Alvarez MD, Ellington DR, Richter HE. Synthetic graft augmentation in vaginal prolapse surgery: long-term objective and subjective outcomes. J Minim Invasive Gynecol 2016;23:614-21. Crossref

13. Bump RC, Mattiasson A, Bø K, et al. The standardization of terminology of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet Gynecol 1996;175:10-7. Crossref

14. Maher C, Feiner B, Baessler K, Schmid C. Surgical management of pelvic organ prolapse in women. Cochrane Database Syst Rev 2013;(4):CD004014. Crossref

15. Haylen BT, Freeman RM, Swift SE, et al. An International Urogynecological Association (IUGA)/International Continence Society (ICS) joint terminology and classification of the complications related directly to the insertion of prostheses (meshes, implants, tapes) & grafts in female pelvic floor surgery. Int Urogynecol J 2011;22:3-15. Crossref

16. Toozs-Hobson P, Freeman R, Barber M, et al. An International Urogynecological Association (IUGA)/International Continence Society (ICS) joint report on the terminology for reporting outcomes of surgical procedures for pelvic organ prolapse. Int Urogynecol J 2012;23:527-35. Crossref

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Assessment of the fetal cerebral lateral ventricle is a standard requirement during the mid-trimester morphology ultrasound performed between 18 and 22 weeks of gestation.1 The International Society of Ultrasound in Obstetrics and Gynecology has recommended a standard method to measure the size of the lateral ventricle, which should be in an axial transventricular plane at the atrium of the posterior horn with calibres placed over the inner edges.2 The reference ranges of lateral ventricle width were established by Cardoza et al3 in 1988; they are consistent across gestations. The diameter (mean ± standard deviation) of the lateral ventricle is 7.6 ± 0.6 mm (range, 6-9). Therefore, fetal cerebral ventriculomegaly is defined as dilation of the lateral ventricle atrium to a width of >10 mm (>4 standard deviations from the mean).3

The degree of lateral ventricle dilation is classically categorised as mild (10-11.9 mm), moderate (12-14.9 mm), or severe (≥15 mm) for clinical and research purposes. Mild fetal ventriculomegaly can be isolated and may represent a normal variant if other pathologies are excluded.4 Therefore, the identification of cerebral ventriculomegaly on prenatal ultrasound does not represent a conclusive diagnosis; it signifies a need to identify various underlying pathologies, including structural abnormalities of the central nervous system (CNS), from hypoxic, haemorrhagic, infective, and genetic causes. Fetal ventriculomegaly is considered a marker of abnormal karyotype; it can be associated with pathogenic copy number variations (CNVs) identified by chromosomal microarray analysis (CMA). The Society for Maternal Fetal Medicine recommends antenatal diagnostic testing (amniocentesis) with CMA when ventriculomegaly is detected.4 In this study, we examined the incidences of abnormal karyotype and CMA results in fetuses with cerebral ventriculomegaly in Hong Kong; we also evaluated their correlations with different degrees of ventriculomegaly. We aimed to determine whether amniocentesis with CMA should be offered to all fetuses with cerebral ventriculomegaly, regardless of the degree of ventriculomegaly. We also reviewed the neurodevelopmental outcomes of all live births with fetal ventriculomegaly to identify factors associated with developmental delay.

This retrospective cohort study included all pregnant women with antenatal ultrasound diagnosis of fetal cerebral ventriculomegaly from two maternal-fetal-medicine units in tertiary referral public obstetric centres in Hong Kong, United Christian Hospital and Prince of Wales Hospital, from January 2014 to December 2018. Cases of fetal ventriculomegaly were identified from the registries of prenatal ultrasound structural abnormalities, as well as the antenatal ultrasound and invasive procedures databases of the respective departments; they were also identified from the laboratory genetic diagnosis database of the Chinese University of Hong Kong (CUHK). All cases of fetal ventriculomegaly in the two units were carefully analysed by the maternal fetal medicine specialists, in accordance with standard departmental protocols. Fetal cerebral ventriculomegaly was classified as mild (10-11.9 mm), moderate (12-14.9 mm), or severe (≥15 mm), according to the greatest atrial width observed during ultrasound examinations in that pregnancy. Based on assessments of any associated ultrasound abnormalities, fetal cerebral ventriculomegaly was classified as isolated (if cerebral ventriculomegaly was the only abnormality identified) or non-isolated (if other structural abnormalities were detected, including CNS abnormalities of the brain or spine and abnormalities in other organ systems).

Pregnant women who chose amniocentesis underwent karyotyping as the standard primary genetic investigation. Chromosomal microarray analysis was offered as an additional self-financed test. The genetic samples of patients from United Christian Hospital were sent to the Prenatal Diagnostic Laboratory of Tsan Yuk Hospital; the genetic samples of patients from Prince of Wales Hospital were sent to the Prenatal Diagnostic Genetic Diagnosis Centre of the CUHK. The microarray platform Perkin Elmer CGX V2.0 (60K oligonucleotide array) and Affymetrix CytoScan 750K single nucleotide polymorphism array were used for CMA studies in Tsan Yuk Hospital from January 2014 to September 2018 and from October to December 2018, respectively; the Agilent Fetal DNA chip version 2.0 (8×60k) array comparative genomic hybridisation and single nucleotide polymorphism analysis methods were used in the CUHK throughout the study period. The neurodevelopmental outcomes of live births were reviewed using the hospital’s computerised clinical management system. Each child’s development was assessed by a paediatrician during follow-up; assessments determined the presence of cognitive impairment, speech delay, fine and gross motor skills, epilepsy, or developmental delay.

The study protocol was approved by the research ethics committees of the respective hospitals. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement was used as a reporting guideline for this study. SPSS software (Windows version 20.0; IBM Corp, Armonk [NY], United States) was used for data entry and analysis. Comparisons of categorical variables were performed using the Chi squared test or Fisher’s exact test, as appropriate. A P value of <0.05 was considered statistically significant.

From January 2014 to December 2018, there were 55 565 total deliveries in the study centres; 91 fetuses (0.16%) had antenatal ultrasound diagnosis of cerebral ventriculomegaly. After the exclusion of cases (ie, pregnant women and their fetuses) with incomplete information (eg, incomplete ultrasound details) and cases that had not delivered in the study units, 84 cases were included for final analysis. The maternal and fetal characteristics are shown in Table 1. Overall, 65.5% (55/84) of fetuses exhibited mildly dilated lateral ventricles and 54.8% (46/84) of fetuses exhibited isolated ventriculomegaly. More male fetuses had cerebral ventriculomegaly than did female fetuses (63.1% vs 36.9%). Screening for congenital fetal infections (eg, cytomegalovirus in amniotic fluid, maternal blood, or urine; toxoplasmosis in maternal blood) was conducted in 66.7% of all cases (73.9% of isolated ventriculomegaly cases); all had negative results. Infection screening was often not performed in cases of non-isolated fetal ventriculomegaly associated with other structural abnormalities; abnormalities in those cases were often presumed to be associated with genetic causes, rather than infection. Fetal magnetic resonance imaging (MRI) was performed in 16 cases (19.0%) to detect additional CNS abnormalities. The most common CNS abnormalities associated with ventriculomegaly were Dandy–Walker malformation (7 cases), corpus callosum disorders (5 cases), and spina bifida (3 cases). Other CNS abnormalities identified included brain tumour, occipital encephalocele, aqueductal stenosis, lissencephaly, and schizencephaly. The pregnancy outcomes are shown in the Figure. In total, 53 live births were delivered in our cohort at a mean gestational age of 38.1 ± 1.9 weeks. The mean birth weight was 3043 ± 614 g. The mean age at neurodevelopmental outcome assessment of the children was 33 months (range, 14-72); ultrasound, computed tomography, or MRI scanning was performed after delivery in 56.6% (30/53) of the cases.

Amniocentesis was performed in 77.4% (65/84) of cases. Among the 22.6% (19/84) of cases that did not involve amniocentesis, an invasive test was declined in 10; in the remaining nine cases, fetal ventriculomegaly was detected after 24 weeks of gestation, which exceeded the legal limit for termination of pregnancy in Hong Kong. The karyotype and CMA results in four cases were obtained from placental tissue after termination of pregnancy; in one case, the results were obtained from the baby’s peripheral blood after delivery. Altogether, karyotype results were available in 70 cases; CMAs were conducted in 53 of those cases. Fourteen cases (20%) had abnormal karyotype or CMA results (Table 2). In total, 11.4% (8/70) of cases had chromosomal abnormalities that could be detected by conventional karyotyping alone, while six cases (shown in Table 2) had chromosomal abnormalities that could only be detected by CMA testing. Therefore, CMA provided an incremental diagnostic yield of 8.6% (6/70) compared with conventional karyotyping; three cases exhibited pathogenic CNVs (4.3%, 3/70) and three cases exhibited variants of uncertain significance (VOUS) [4.3%, 3/70]. The three pathogenic CNVs included two cases of 17p13.3 deletion: one involved the lissencephaly 1 (LIS1) gene and one involved the YWHAE gene. Deletion of the LIS1 gene has been associated with classic lissencephaly, microcephaly, and mental insufficiency; YWHAE may be a susceptibility gene for schizophrenia.5 The third case of terminal 6p25 deletion involved the FOXC1 gene, which is reportedly associated with CNS anomalies (eg, hydrocephalus and hypoplasia of the cerebellum, brainstem, and corpus callosum) that cause mild to moderate developmental delay.6

Subgroup analysis showed that in the isolated cerebral ventriculomegaly group, 15.2% (5/33) of cases had abnormal karyotype or CMA results; the incidences of abnormal karyotype or CMA results did not significantly differ according to the degree of isolated cerebral ventriculomegaly (P=0.31) [Table 3]. In the mild isolated ventriculomegaly group, 12.0% (3/25) of cases had abnormal karyotype or CMA results, among which two cases could be detected by conventional karyotyping and one case (VOUS) could only be detected by CMA.

Concerning the evolution of isolated ventriculomegaly with live births, 8.3% (3/36) with mild isolated ventriculomegaly and 20% (1/5) with moderate isolated ventriculomegaly at diagnosis showed progression during pregnancy. Fewer cases of mild cerebral ventriculomegaly (10-11.9 mm) were associated with developmental delay than non-mild (≥12 mm) ventriculomegaly in the isolated ventriculomegaly group (9.7% vs 41.7%; P=0.03). Developmental delay tended to be more common in the isolated cerebral ventriculomegaly group with abnormal karyotype or CMA results (66.7% vs 14.8%), compared with isolated ventriculomegaly with normal karyotype or CMA; however, this difference was not statistically significant. The risk of developmental delay was not significantly different according to fetal sex in cases of isolated ventriculomegaly (Table 4). The clinical details of the 12 cases with developmental delay are summarised in Table 5.

The incidence of fetal ventriculomegaly in our cohort was 0.16%, reflecting the incidence of fetal ventriculomegaly detectable antenatally with mid-trimester morphology ultrasound examinations in a large cohort in Hong Kong. Our findings were compatible with previous reports of fetal ventriculomegaly incidence, which has ranged from 0.3 to 3.8 per 1000 pregnancies.7 8 While congenital infection screening was conducted in only 66.7% of our cases, no cases of intrauterine cytomegalovirus or toxoplasmosis infection were identified in our cohort. This is potentially because Chinese pregnant women have a high cytomegalovirus seroprevalence9 but a low prevalence of toxoplasmosis, compared with Caucasian pregnant women.10 Because even mild isolated ventriculomegaly <12 mm carried a 12.0% risk of chromosomal abnormalities, the findings of amniocentesis with CMA appeared to be clinically meaningful, regardless of the degree of fetal ventriculomegaly. In this study, isolated mild ventriculomegaly was associated with a normal outcome in approximately 90% of children, but the risk of developmental delay increased with increasing degree of ventriculomegaly.

Cerebral ventriculomegaly was more prevalent in male fetuses than in female fetuses in our cohort; the male to female ratio was 1.7. This finding is consistent with the results of previous studies, which demonstrated a male predominance regarding isolated cerebral ventriculomegaly (male to female ratio of 1.7).11 A study of isolated fetal ventriculomegaly in China showed no differences in chromosomal abnormalities between male and female fetuses (7.6% vs 8.0%, P=0.924).12 Our cohort demonstrated no significant difference in the risk of developmental delay according to fetal sex in cases of isolated ventriculomegaly. Previous studies also showed no significant differences in neurological outcomes between male and female infants with isolated ventriculomegaly and normal karyotype.11 Further studies are needed to explore the reason for a higher incidence of cerebral ventriculomegaly in male fetuses than in female fetuses.

The incidence of an abnormal karyotype (11.4% overall vs 8.0% in the mild isolated group) in our cohort was similar to the results of previous studies. Previous studies with differences in the proportions of cases with each degree of ventriculomegaly, as well as the proportions of associated abnormalities, demonstrated that the incidence of an abnormal karyotype in cases of fetal ventriculomegaly was between 5% and 11.3%.13 14 15 In a systematic review of isolated ventriculomegaly (10-15 mm), 4.7% (57/1213) of fetuses had abnormal karyotype results.16 Another prospective study, which included 355 cases of mild to moderate ventriculomegaly, showed a higher rate of abnormal karyotype results when other structural abnormalities were present (18.0%), compared with the isolated ventriculomegaly group (10.2%).

Chromosomal microarray analysis testing provided an incremental diagnostic yield of 8.6%, compared with conventional karyotyping in our cohort; 4.3% of cases exhibited pathogenic CNVs, while 4.3% of cases exhibited VOUS. Chromosomal microarray analysis can identify aneuploidies (ie, large structural chromosomal changes); it can also identify submicroscopic (<5 Mb) CNVs that cannot be detected by conventional karyotyping.17 Recent studies have focused on the application of CMA for detecting chromosomal aberrations in cases of fetal cerebral ventriculomegaly. The incremental diagnostic yields of CMA over karyotyping for diagnosing pathogenic CNVs and VOUS in previous studies of fetal cerebral ventriculomegaly conducted in China were 3.0% to 12.8% and 2.0% to 4.5%, respectively.18 19 20 21 A limitation of CMA testing is the reporting of VOUS, which poses counselling difficulties during subsequent management. In a recent cohort in Hong Kong, the rate of VOUS was 2.1% in prenatal samples obtained for various indications (eg, abnormal ultrasound, positive Down syndrome screening, abnormal non-invasive prenatal testing, advanced maternal age, and family history of chromosomal/genetic disorders).22 Our cohort detected 4.3% of VOUS, which is high but generally comparable with the findings of previous studies.

Consistent with our findings, the incidences of abnormal karyotype or CMA results in previous studies did not significantly differ according to the degree of cerebral ventriculomegaly.23 24 Therefore, invasive diagnostic tests are warranted for any degree of cerebral ventriculomegaly identified in prenatal ultrasound, including mild isolated ventriculomegaly. Chromosomal microarray analysis should be performed because of its higher diagnostic yield, compared with conventional karyotyping. The Hospital Authority of Hong Kong has replaced conventional karyotyping with CMA as the primary test for chromosomal studies of structural abnormalities detected in prenatal ultrasound since June 2019. Therefore, the incidences of chromosomal abnormalities detected in fetal cerebral ventriculomegaly are expected to increase in the future. Non-invasive prenatal testing for chromosomal abnormalities by maternal blood DNA testing is a trend among pregnant women because of its non-invasiveness. However, non-invasive prenatal testing for CNVs <5 Mb yielded a detection rate of only 14.3%.25 The above findings suggest that non-invasive prenatal testing should not be offered as an alternative for women with fetal cerebral ventriculomegaly, regardless of the degree of ventriculomegaly, because small pathogenic CNVs can be present in cases that involve any degree of ventriculomegaly.

One of the fetuses in our cohort had mild cerebral ventriculomegaly; MRI of the brain revealed ischaemic changes (Table 5 Case 10). Amniocentesis was performed and showed normal karyotype and CMA results. The baby had progressive hypertrophic cardiomyopathy with global developmental delay after delivery. Trio whole-exome sequencing (WES) was done after delivery, and the baby was diagnosed with autosomal recessive mitochondrial disease caused by SCO2 mutations; both parents were heterozygous carriers. In prenatal fetal structural abnormalities, WES can reveal a high proportion of diagnostic genetic variants, including up to 22% in CNS abnormalities including cerebral ventriculomegaly.26 Mutations in two X-linked genes (L1CAM and AP1S2) and two autosomal recessive genes (CCDC88C and MPDZ) have been described to cause congenital hydrocephalus or aqueductal stenosis, which can cause severe isolated ventriculomegaly.27 There is a potential role for WES in facilitating the genetic diagnosis in cerebral ventriculomegaly with negative karyotype and CMA results, particularly for those fetuses with severe ventriculomegaly suggestive of aqueductal stenosis and in couples with recurrent fetal abnormalities.

Fetal cerebral ventriculomegaly was associated with an increased risk of developmental delay in the child after delivery. The neurodevelopmental prognosis worsened as the degree of ventriculomegaly increased in our cohort (9.7% in cases of mild ventriculomegaly vs 41.7% in cases of moderate or severe ventriculomegaly) and in other studies. In a systematic review and meta-analysis of neurodevelopmental outcomes in cases of isolated ventriculomegaly (10-15 mm), the overall prevalence of developmental delay was 7.9%.16 In a meta-analysis of the neurological outcomes of fetal ventriculomegaly in China, the neurological prognosis was good in 88%, 57%, and 36% of mild, moderate, and severe ventriculomegaly cases, respectively.13 In another systematic review and meta-analysis of severe isolated ventriculomegaly, developmental delay was mild or moderate in 18.6% of children and severe in 39.6% of children.28 More than half (58.3%, 7/12) of the children diagnosed with developmental delay in our study exhibited only mild delay, although there was a background risk of mild developmental delay during counselling. The high incidence of developmental delay in cases of non-mild isolated ventriculomegaly was probably also associated with the presence of chromosomal abnormalities. Nevertheless, our data did not show associations of abnormal karyotype or CMA results with developmental delay among the 43 live births. This finding was presumably biased because pregnancies were terminated in many of the cases with abnormal karyotype or CMA results; the neurological outcomes could not be assessed in those cases.

This study had some limitations. First, it used a retrospective cohort design; thus, congenital infection screening and fetal MRI assessment were not performed in all cases. Second, there was no protocol for routine postnatal imaging evaluation, and the assessment of neurodevelopmental outcomes among the children was not standardised. However, our study provided data regarding the incidences of chromosomal and genetic abnormalities in cases of antenatally detected fetal ventriculomegaly in Hong Kong, as well as a general picture of neurological outcomes of affected children. The findings will allow prenatal counselling in Hong Kong to be performed on the basis of more relevant epidemiological and genomic data, rather than findings from other populations.

All degrees of cerebral ventriculomegaly may be associated with chromosomal abnormalities. Chromosomal microarray analysis has an increased diagnostic yield, compared with conventional karyotyping. Amniocentesis with CMA testing should be offered to all women with fetal cerebral ventriculomegaly. Non-invasive prenatal testing should not be offered as an alternative method of chromosomal analysis. The neurological outcomes of the children are associated with the degree of fetal ventriculomegaly. Whole-exome sequencing may be indicated for selected cases of fetal ventriculomegaly with normal CMA, but further studies are needed to support this recommendation.

Concept or design: WY Lok, CW Kong, WK To.
Acquisition of data: WY Lok, MM Shi, SYA Hui.
Analysis or interpretation of data: WY Lok, CW Kong, WK To.
Drafting of the manuscript: WY Lok, CW Kong.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

All authors have disclosed no conflicts of interest.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Ethics approval was obtained from the Kowloon Central/ Kowloon East Research Ethics Committees (Ref: KC/KE-19-0172/ER-4) and The Joint Chinese University of Hong Kong–New Territories East Cluster Clinical Research Ethics Committee (CREC Ref No.: 2019.468).

1. alomon LJ, Alfirevic Z, Berghella V, et al. Practice guidelines for performance of the routine mid-trimester fetal ultrasound scan. Ultrasound Obstet Gynecol 2011;37:116-26.Crossref

2. International Society of Ultrasound in Obstetrics & Gynecology Education Committee. Sonographic examination of the fetal central nervous system: guidelines for performing the ‘basic examination’ and the ‘fetal neurosonogram’. Ultrasound Obstet Gynecol 2007;29:109-16. Crossref

3. Cardoza JD, Goldstein RB, Filly RA. Exclusion of fetal ventriculomegaly with a single measurement: the width of the lateral ventricular atrium. Radiology 1988;169:711-4. Crossref

4. Society for Maternal-Fetal Medicine (SMFM); Fox NS, Monteagudo A, Kuller JA, Craigo S, Norton ME. Mild fetal ventriculomegaly: diagnosis, evaluation, and management. Am J Obstet Gynecol 2018;219:B2-9. Crossref

5. Online Mendelian Inheritance in Man. #247200 Miller-Dieker Lissencephaly Syndrome. Available from: https://www.omim.org/entry/247200. Accessed 1 Aug 2020.

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7. Weichert J, Hartge D, Krapp M, Germer U, Gembruch U, Axt-Fliedner R. Prevalence, characteristics and perinatal outcome of fetal ventriculomegaly in 29,000 pregnancies followed at a single institution. Fetal Diagn Ther 2010;27:142-8. Crossref

8. Patel SK, Zamorano-Fernandez J, Nagaraj U, Bierbrauer KS, Mangano FT. Not all ventriculomegaly is created equal: diagnostic overview of fetal, neonatal and pediatric ventriculomegaly. Childs Nerv Syst 2020;36:1681-96. Crossref

9. Wang S, Wang TZ, Zhang WQ, et al. Cohort study on maternal cytomegalovirus seroprevalence and prevalence and clinical manifestations of congenital infection in China. Medicine (Baltimore) 2017;96:e6007. Crossref

10. Ko RC, Wong FW, Todd D, Lam KC. Prevalence of Toxoplasma gondii antibodies in the Chinese population of Hong Kong. Trans R Soc Trop Med Hyg 1980;74:351-4. Crossref

11. Melchiorre K, Bhide A, Gika AD, Pilu G, Papageorghiou AT. Counseling in isolated mild fetal ventriculomegaly. Ultrasound Obstet Gynecol 2009;34:212-24. Crossref

12. Zhao D, Cai A, Wang B, Lu X, Meng L. Presence of chromosomal abnormalities in fetuses with isolated ventriculomegaly on prenatal ultrasound in China. Mol Genet Genomic Med 2018;6:1015-20. Crossref

13. Sun Y, Zhang WY. Meta-analysis of fetal lateral ventriculomegaly and prognosis [in Chinese]. Zhonghua Fu Chan Ke Za Zhi 2018;53:677-82.

14. Gezer C, Ekin A, Ozeren M, et al. Chromosome abnormality incidence in fetuses with cerebral ventriculomegaly. J Obstet Gynaecol 2014;34:387-91. Crossref

15. Bijarnia-Mahay S, Puri RD, Kotecha U, et al. Outcome of prenatally-detected fetal ventriculomegaly. J Fetal Med 2015;2:39-44. Crossref

16. Pagani G, Thilaganathan B, Prefumo F. Neurodevelopmental outcome in isolated mild fetal ventriculomegaly: systematic review and meta-analysis. Ultrasound Obstet Gynecol 2014;44:254-60. Crossref

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20. Song TT, Wan SN, LI Y, et al. Application value of chromosomal microarray analysis in prenatal diagnosis of lateral ventriculomegaly fetuses [in Chinese]. PLAMJ Med J Chi People Liberation Army 2017;42:902-8.

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The clinical decision regarding a need for treatment of menstrual bleeding relies on the patient’s perception of flow amount and its effects on her physical, emotional, and social well-being.1 However, retrospective recall regarding the amount of menstrual flow in previous cycles is heavily influenced by a woman’s subjective perception and is not always associated with the measured blood loss.2 The ‘gold standard’ approach for assessment of menstrual blood loss is the alkaline haematin method, which requires a woman to collect all soiled sanitary products for laboratory assessment2; however, this is a cumbersome non-hygienic impractical method outside the research setting.

The Pictorial Blood Loss Assessment Chart (PBAC) is a scoring system developed as a semi-quantitative evaluation of menstrual blood loss, which considers the number of sanitary products used, the degree to which these products are soiled with blood, the number and size of blood clots passed, and the number of flooding episodes.3 The PBAC has been validated with the alkaline haematin method to diagnose heavy menstrual bleeding in several studies in other populations.3 4 5 Furthermore, the PBAC has been used as a measurement tool to evaluate menstrual blood loss in systematic reviews and randomised controlled clinical trials.6

In the clinical setting, it can be difficult for a physician to determine the amount and implication of menstrual flow in a patient reporting heavy menstrual bleeding. Menstruation is a taboo topic in many communities, including among Asian women in Hong Kong.7 8 9 10 Some women may prefer not to, or find it difficult or embarrassing to, articulate details regarding their menstrual problems.7 8 9 Furthermore, some women may be unaware of heavy menstrual bleeding.

The objective of this study was to evaluate the usefulness of the PBAC as a self-evaluation tool for heavy menstrual bleeding. Additionally, we sought to determine the acceptability of the PBAC and whether PBAC scores were associated with menstrual blood loss severity among Asian women in Hong Kong.

This prospective cohort study compared PBAC scores between women who presented with and without heavy menstrual bleeding. Women were recruited between November 2014 and January 2016 through the gynaecology ward or the general gynaecology out-patient clinic of a university-affiliated hospital. They attended the out-patient clinic for routine follow-up or were admitted to the ward for elective or emergent treatment. Inclusion criteria included good general health, absence of other medical conditions which might lead to anaemia, no prior PBAC use, and age ≥18 years. Women were excluded if they were pregnant, in menopause, receiving hormonal treatment, mentally incompetent, and/or undergoing treatment/monitoring of a gynaecological malignancy. Ethics approval was obtained from the Institutional Review Board of The University of Hong Kong/Hospital Authority Hong Kong West Cluster. Written informed consent was obtained from all study participants.

Women were approached by the research nurse and were placed into heavy menstrual bleeding and normal menstrual bleeding groups based on their self-reported menstrual cycle symptoms over the preceding 6 months. All group allocations were noted by the nurse. All participants, regardless of perceived menstrual flow, were instructed by the research nurse to fill in a PBAC for one cycle in the next cycle. They were also instructed to answer a question regarding whether they found the PBAC acceptable (yes/no) and a question regarding the ease of use of the PBAC (scale of 1-5; 1=easiest and 5=hardest). The PBAC originally described by Higham et al3 was used, but diagrams of clot sizes were modified to the sizes of local coins. The PBAC consisted of a series of diagrams representing lightly, moderately, and heavily soaked towels and tampons (depending on the degree of staining) to evaluate menstrual blood loss.3 The numbers of pads or tampons used each day were recorded. In the event of clot passage, the number and size were recorded; flooding episodes were also recorded. A total score was calculated by multiplying by a factor of 1 for each lightly soiled item, 5 for each medium soiled item, 10 for a fully soaked tampon, and 20 for a fully soaked pad.3 Small and large clots were given a score of 1 and 5, respectively.3 Women continued to use their own sanitary products (ie, products used prior to the study) and were asked to document the types and sizes of sanitary products used. Each woman was asked to return the completed PBAC to the research nurse by mail in a stamped envelope. The following clinical data were retrieved from the women’s electronic medical records and used in the analysis: age, haemoglobin level within 3 months before the consultation or on the day of consultation (if available), and the iron supplement status (using/not using).

The sample size was determined based on an anticipated 20% difference in accuracy endpoints between study groups and a standard deviation of 40%. Allowing for 10% non-responders, the calculated sample size per group was 70 women. Statistical tests were performed using SPSS Statistics (Windows version 24; IBM Corp, Armonk [NY], United States). Comparisons between groups were made using the Chi squared test for categorical variables and the non-parametric Mann–Whitney U test for continuous variables. Continuous variables were expressed as median and range. A P value of <0.05 was considered statistically significant. The kappa statistic was used to test agreement between subjective evaluation of heavy menstrual bleeding and the PBAC score at various cut-off scores. Predictions of heavy menstrual bleeding according to the PBAC score and haemoglobin level were determined using area under the receiver-operating characteristic curve analysis.

The response rate was better than expected and more women than expected were recruited in each clinic session; this yielded a final sample size larger than originally planned. However, among 292 women who were asked to complete the PBAC, the return rate was only 206/292 (70.5%). In all, 118 women had self-perceived heavy menstrual bleeding and 88 women had self-perceived normal menstrual flow. Haemoglobin level data were available in 179/292 (61.3%) women (116 in the heavy menstrual bleeding group and 63 in the normal menstrual bleeding group). Table 1 summarises the reasons for presentation in both groups of women. The PBAC scores based on different diagnoses are shown in Table 2. Women with heavy menstrual bleeding were older than women with normal menstrual bleeding (median age 44 years, [interquartile range=40-48] vs 38 years [interquartile range=31-43], respectively, P<0.001). There was no significant difference in education level between groups (Table 3).

Nearly all women in the study used pads; one woman used both pads and tampons. In total, 147/206 (71.4%) women used various brands and sizes of pads with distinct absorbency characteristics during the menstrual cycle; the remaining 59/206 (28.6%) women used only one type of pad. Seven women used diapers and three women used postpartum pads. The median PBAC scores of women who reported heavy and normal menstrual bleeding were 497 (interquartile range=152-1112) and 54 (interquartile range=41-65), respectively (Table 3). Compared with women who had normal menstrual flow, women with heavy menstrual bleeding had significantly higher total PBAC scores and numbers of flooding episodes, larger clot sizes and numbers, more days of bleeding, and lower haemoglobin levels (Table 3). Using cut-off scores of 76, 80, 100, 130, 150, and 185, levels of agreement between PBAC score and self-reported symptoms in the diagnosis of heavy menstrual bleeding are shown in Table 4. Women with anaemia, defined as haemoglobin level <11.0 g/dL, had significantly higher median PBAC scores than did women without anaemia (508 [interquartile range=168-1087] vs 58 [interquartile range=46-84], P<0.01). Receiver-operating characteristic curves demonstrating the predictive abilities of the PBAC and haemoglobin level for heavy menstrual bleeding are shown in the Figure. The area under the receiver-operating characteristic curves of the PBAC and haemoglobin level for prediction of heavy menstrual bleeding were 0.961 (95% confidence=0.940-09.982) and 0.876 (95% confidence=0.821-0.931), respectively. The PBAC cut-off score with the highest Youden index was 76, which yielded a sensitivity of 93.2% and a specificity of 83.0% for predicting self-perceived heavy menstrual bleeding.

All women in our study were able to complete the PBAC. Missing information was filled in with the help of the research nurse via phone contact after return of the PBAC. Twenty-eight women (13.6%) who began the PBAC on the day of consultation were contacted by phone to urge them to return the PBAC using the stamped envelopes. Another 11 women (5.4%) with prolonged menstrual bleeding did not provide full details regarding their menstrual bleeding; they were contacted by phone for confirmation. In all, 200/206 women (97.1%) found the PBAC acceptable: 113/118 (95.8%) in the heavy menstrual bleeding group and 87/88 (98.9%) in normal menstrual bleeding group. Assuming that the reason for non-response was that those women found the PBAC to be unacceptable, the acceptability rate was 200/292 (68.5%). There was no significant difference in the perceived ease of use of the PBAC; the median rating was 2 in both groups (P=0.618; Table 3). Notable written comments from the women concerning the PBAC were that it could not accurately describe their menstrual blood loss (n=19), it required explanation (n=11), it was inconvenient or involved recall problems (n=3), and it did not record other symptoms which were more distressing (n=1).

Our results suggested that the reported PBAC scores in this group of Asian women comprised a useful tool for differentiating self-perceived heavy and normal menstrual bleeding. Heavy menstrual bleeding considerably impacts a woman’s quality of life; interventions should be designed to improve the quality of life, rather than focusing on the exact amount of menstrual blood loss.1 Nevertheless, some women may be unaware of heavy bleeding or find it difficult to describe the amount of menstrual flow. The PBAC offers a semi-objective method for initial self-evaluation of the amount of menstrual bleeding in women whose cultural backgrounds may cause reluctance in discussing their gynaecological or menstrual problems. This self-evaluation can alert women to seek medical attention, thus facilitating clinical evaluation and treatment. The PBAC cut-off scores included in Table 4 have been used in previous studies to imply heavy menstrual bleeding.3 4 5 11 The recommendation of a particular cut-off score depends on the clinical context (ie, whether a higher sensitivity or specificity is required). For example, if the PBAC is used as a screening tool, a lower cut-off score may be appropriate to alert women to seek medical attention. In contrast, if the PBAC is used to evaluate women with heavy menstrual bleeding for potential participation in a research study, a higher cut-off score may be used to recruit women with more severe symptoms to evaluate their response to treatment.

In our study, 10 women (11.4%) in the self-perceived normal menstrual bleeding group had PBAC scores of >100, although they reported normal menstrual bleeding. In the self-perceived normal menstrual bleeding group, 14 women had anaemia (haemoglobin level <11.0 g/dL), among which five women had a haemoglobin level of <10.0 g/dL. Twelve women who reported normal menstrual bleeding were using iron supplements. Although most women accurately recognised heavy menstrual bleeding, use of the PBAC identified an additional 10% of women who might have unperceived abnormal bleeding. Of the 10 women with self-perceived normal menstrual bleeding (PBAC scores of 101-180), seven (70%) had anaemia. Thus, use of the PBAC might enable identification of a small group of apparently asymptomatic women who had unrecognised anaemia, thereby facilitating earlier medical attention.

In our study, women were asked to use their own sanitary products, rather than using specific brands and sizes of pads; thus, our findings are more representative of realistic PBAC use, compared with results acquired in a research setting. Most women used different brands and sizes of pads with different absorbency characteristics, even within a single cycle. In addition, several women used adult diapers or postpartum pads, which implied substantial difference in blood loss compared with the usual sanitary pads. The range of PBAC scores was much larger in our study than in previous studies.3 4 5 11 12 One woman in our study had a PBAC score of 32 301; she had prolonged vaginal bleeding for 56 days and had a haemoglobin level of 4.5 g/dL. Women with adenomyosis and uterine fibroids had significantly higher PBAC scores than did women with other diagnoses. Therefore, the PBAC may be useful for evaluation of responses to interventions during randomised controlled trials involving these groups.

Although women in our study who returned the PBAC found it acceptable and generally easy to use, the return rate should be considered. Notably, 19/206 (9.2%) women commented that the range of icons in the PBAC did not accurately reflect their blood loss on pads or clots because they experienced difficulty in evaluating the amount of blood loss (based on a particular stain) when comparing among pads with different absorbency characteristics. The clots were of irregular size and women felt that a scale or use of items encountered daily (such as ‘tofu’ or ‘palm’, rather than coins) could more accurately describe these clots. Women (particularly in the heavy menstrual bleeding group) who had to sit on the toilet during flooding episodes could not quantify their bleeding; several women with prolonged bleeding did not continue the PBAC evaluation because they felt that continuing the documentation was time-consuming and annoying. In total, 5.3% of the women commented that clearer instructions could be provided. This is consistent with the findings by Zakherah et al,5 who reported that improved instructions led to greater accuracy when a physician or nurse reviewed the documentation with the patient. The role of the nurse in our study was crucial. Our research nurse found it helpful to demonstrate to the women how to fill in the PBAC using their current or previous cycle; the nurse also helped the women to complete the PBAC in the event of substantial missing information, especially among women with prolonged menstrual bleeding. Some women probably completed the PBAC by recall, rather than in a day-by-day manner. This aspect should be considered when the PBAC is applied as a self-screening tool. The development of PBAC-containing mobile apps or websites accessible by the public may improve the usability of the PBAC as a self-screening tool in terms of better convenience and less recall bias, especially among younger women.

Our study had some limitations. First, we only evaluated use of the PBAC in a small group of patients who presented for clinical treatment, rather than the general population; this may limit the generalisability of the results. Second, we did not study the inter-cycle variability in PBAC score or the effects of other demographic factors (eg, household income) which may affect the use of the PBAC. Although only one cycle of menstrual bleeding was charted in our study and women may have unusual menstrual flow in subsequent cycles, previous studies have demonstrated high consistency with low inter-cycle variation in women who completed a second PBAC evaluation without treatment.11 Third, patients may have been offered treatment during the consultation; because the PBAC was completed in the cycle after consultation, the PBAC score may not fully reflect the pre-consultation reported symptoms, especially among women with self-perceived heavy menstrual bleeding. Fourth, compliance with iron therapy was not checked; this could have affected the haemoglobin results. However, the aim of our study was to evaluate the relationship between the PBAC score and self-perceived menstrual flow. Overall, the results of this population-specific study might support the use of the PBAC as a potential self-screening tool for heavy menstrual bleeding among Asian women in Hong Kong.

There is considerable endpoint heterogeneity in the current literature with respect to the outcomes of various treatment options for heavy menstrual bleeding. Furthermore, there is currently no core outcome set for valid comparison and interpretation of data from research studies and assessments regarding abnormal uterine bleeding.6 Although PBAC scores have shown high inter-individual variation, they had low intra-individual variation;11 thus, the PBAC may be useful in future studies of treatment responses in individual women. Despite the large variety of commercially available sanitary products, the PBAC remains a reliable screening tool for semi-quantitative evaluation of menstrual blood loss, which can alert women to seek medical attention for heavy menstrual bleeding. Additional studies are needed to confirm the clinical usefulness of the PBAC, especially in the context of the evolution and advancement of superabsorbent sanitary products currently available. Overall, the advantages of the PBAC are its relative objectivity and flexibility as a tool for screening, diagnosis, and evaluation of treatment effect.

Concept or design: JKY Ko, VYT Cheung.
Acquisition of data: JKY Ko, VYT Cheung.
Analysis or interpretation of data: All authors.
Drafting of the manuscript: JKY Ko.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

All authors have disclosed no conflicts of interest.

The authors thank Ms Wai-ki Choi for patient recruitment, teaching women about the Pictorial Blood Loss Assessment Chart, and managing the database.

The study was presented in an oral presentation at the FOCUS in O&G 2018 Congress in Hong Kong (17-18 November 2018).

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Ethics approval was obtained from the Institutional Review Board of The University of Hong Kong/Hospital Authority Hong Kong West Cluster (Ref: UW 14-299). Written informed consent was obtained from all study participants.

1. National Institute for Health and Care Excellence guideline. Heavy menstrual bleeding: assessment and management. 14 Mar 2018 (last updated 24 May 2021). Available from: http://www.nice.org.uk/guidance/ng88. Accessed 25 Nov 2021.

2. Magnay JL, O’Brien S, Gerlinger C, Seitz C. A systematic review of methods to measure menstrual blood loss. BMC Womens Health 2018;18:142. Crossref

3. Higham JM, O’Brien PM, Shaw RW. Assessment of menstrual blood loss using a pictorial chart. Br J Obstet Gynaecol 1990;97:734-9. Crossref

4. Janssen CA, Scholten PC, Heintz AP. A simple visual assessment technique to discriminate between menorrhagia and normal menstrual blood loss. Obstet Gynecol 1995;85:977-82. Crossref

5. Zakherah MS, Sayed GH, El-Nashar SA, Shaaban MM. Pictorial blood loss assessment chart in the evaluation of heavy menstrual bleeding: diagnostic accuracy compared to alkaline hematin. Gynecol Obstet Invest 2011;71:281-4. Crossref

6. Herman MC, Penninx J, Geomini PM, Mol BW, Bongers MY. Choice of primary outcomes evaluating treatment for heavy menstrual bleeding. BJOG 2016;123:1593-8. Crossref

7. Garg S, Anand T. Menstruation related myths in India: strategies for combating it. J Family Med Prim Care 2015;4:184-6. Crossref

8. The Lancet Child Adolescent Health. Normalising menstruation, empowering girls. Lancet Child Adolesc Health 2018;2:379. Crossref

9. Agampodi TC, Agampodi SB. Normalising menstruation, empowering girls: the situation in Sri Lanka. Lancet Child Adolesc Health. 2018;2:e16. Crossref

10. Wong WC, Li MK, Chan WY, et al. A cross-sectional study of the beliefs and attitudes towards menstruation of Chinese undergraduate males and females in Hong Kong. J Clin Nurs 2013;22:3320-7. Crossref

11. Hald K, Lieng M. Assessment of periodic blood loss: interindividual and intraindividual variations of pictorial blood loss assessment chart registrations. J Minim Invasive Gynecol 2014;21:662-8. Crossref

12. Reid PC, Coker A, Coltart R. Assessment of menstrual blood loss using a pictorial chart: a validation study. BJOG 2000;107:320-2. Crossref

Burnout among doctors is increasingly recognised as a serious threat to medical and dental practice across all specialties; its prevalence is increasing worldwide.1 Burnout is a spectrum of clinical syndromes that were first categorised into three dimensions by Maslach as emotional exhaustion, depersonalisation, and a low sense of personal accomplishment.2 Subsequently, it was added to the International Classification of Diseases as a syndrome that results from poorly managed chronic workplace stress.3

Burnout among doctors can lead to decreased effectiveness and shortening of professional lifespan.4 Burnout exacerbates negative emotions, thereby impeding cognitive performance; it may result in biased decision making. Hence, the well-being of doctors is important for maintaining manpower, quality of care, and equity of care delivery. Multiple studies in different countries have shown that the incidence of burnout among doctors is rising. In the US, a Medscape nationwide survey showed that 59% of emergency medicine doctors experienced burnout symptoms, and the incidence had increased steadily over time.1 In Australia, the National Mental Health Survey found that the level of very high psychological distress was significantly greater in doctors (3.4%) than in the general population (2.6%) or other professionals (0.7%).5 A cross-sectional online survey in the United Kingdom also revealed a high rate of mental health disorders among junior doctors and medical students.6

To our knowledge, studies regarding well-being and burnout among doctors in Asia are limited. Gan et al7 performed a cross-sectional study of general practitioners in Hubei, China; they found a combined prevalence of 2.46% across all three dimensions of emotional exhaustion, depersonalisation, and personal accomplishment. However, that study only included doctors within a single specialty in one province. Huang et al8 found the prevalences of personal burnout and client-related burnout were 44.0% and 14.8%, respectively, among residents in Taiwan; however, they used a non-standardised questionnaire. In Hong Kong, a previous cross-sectional survey showed that 31.4% of respondents among doctors in the public sector had a high rate of burnout, but the sampling criteria were random and non-specific; moreover, that study did not include a substantial proportion of doctors who worked in the private sector.9 Another survey also suggested that burnout was prevalent among doctors in Hong Kong, but it only included graduates from one medical school in Hong Kong.10

Hence, this study aimed to evaluate the prevalence of burnout in the Hong Kong medical and dental workforce by administering standardised questionnaires to a broad population of residents-in-training and doctors within 10 years of their specialist registration. The study also explored well-being among doctors in terms of job satisfaction, depression, lifestyle behaviours, and factors associated with these states.

In this study, all doctors within 10 years of their specialist registration registered with the Hong Kong Academy of Medicine, as well as residents-in-training registered with one of the Academy’s 15 constituent Colleges, were invited to complete a voluntary cross-sectional survey between February 2019 and June 2019. The cut-off of 10 years was selected because the Hong Kong Academy of Medicine considers doctors within 10 years of their specialist registration to be “young Fellows”. The survey consisted of self-reported demographic data, year of entry into medical school, and current professional details. Burnout was assessed using the validated Copenhagen Burnout Inventory (CBI).11 Depression was assessed using the Patient Health Questionnaire-9 (PHQ-9).12 Lifestyle factors were assessed with reference to the respondents’ drinking habits, sleep patterns, and levels of both exercise and activities. Items concerning job satisfaction and lifestyle behaviours were adapted from existing doctor questionnaires and health surveys.13 14

An online survey was developed in-house by the Hong Kong Jockey Club Innovative Learning Centre for Medicine of the Hong Kong Academy of Medicine, then administered electronically. The invitations to participate were sent via e-mail; two separate reminder emails were sent after the initial invitation. As an incentive, respondents were offered coffee or food coupons after completion of the survey. The study protocol was approved by the Institutional Review Board of the University of Hong Kong/Hospital Authority Hong Kong West Cluster (Ref No: UW 19-062).

PASS 2000 (NCSS, LLC., Kaysville [UT], US; www.ncss.com) power analysis software was used for sample size calculation. The prevalence of personal burnout among young doctors in Hong Kong was assumed to be similar to the prevalence of personal burnout among residents in Taiwan (44.0%)8; thus, to achieve a 95% confidence interval (CI) with a precision of 4.5%, 458 participants were required. Our final sample of 514 doctors was sufficient to achieve the desired statistical power.

This instrument consists of three scales that measure personal burnout, work-related burnout, and client-related burnout; the scales can be applied to workers in all industries and cultures. Personal burnout measures the degree of fatigue experienced by the respondent, irrespective of work experience or occupational status. Work-related burnout measures the degree of fatigue related to work; it explores how the respondent’s perception of work contributes to fatigue. Client-related burnout is the perceived degree of fatigue related to work with clients. The burnout level is calculated as a mean score; therefore, each scale has a value between 0 and 100. A score of ≥50 indicates a high degree of burnout.15 16 17 18

The PHQ-9 is a depression assessment tool, which scores each of the nine Diagnostic and Statistical Manual of Mental Disorders IV criteria for depression on a scale ranging from “0” (not at all) to “3” (nearly every day). A PHQ-9 score >9 has a reported sensitivity of 88% and specificity of 88% for major depression.19

The prevalence of burnout is shown using point estimates and 95% CIs. Descriptive statistics were presented concerning demographic characteristics and lifestyle behaviours. Bivariate logistic models were used to describe the distinct relationships of suicide, depression, and burnout with demographic, educational, and professional characteristics. The data were analysed using SPSS software (Windows version 26.0; IBM Corp, Armonk [NY], US). Statistical significance was set at P<0.05.

There were 746 total respondents; of these, 232 did not complete the entire survey and were excluded from the analysis. Of the included 514 respondents, 284 were doctors within 10 years of their specialist registration, while 230 were residents-in-training. The total number of doctors within 10 years of their specialist registration invited to participate in the survey was 2879; thus, the response rate was estimated as 9.9%. However, it was not possible to calculate the response rate for residents-in-training. The respondents included 277 women (54%); the mean age among all respondents was 33.7 ± 6.1 years. The respondents’ demographic data are summarised in Table 1; their current professional statuses are summarised in Table 2.

Overall, 24% (n=125) of respondents were “somewhat dissatisfied” with their present job position, while 4% (n=19) of respondents were “very dissatisfied” with their present job position. Furthermore, 15% (n=76) of respondents were “somewhat dissatisfied” with being a medical doctor, whereas 2% (n=10) of respondents were “very dissatisfied” with being a medical doctor. Finally, 3% (n=14) of respondents indicated they planned to stop practising medicine in the next 12 months, with stress or burnout (86%) cited as the most common reason for such plans.

As measured by the CBI, the mean personal burnout score was 59.6 ± 20.5, work-related burnout score was 57.3 ± 20.1, and client-related burnout score was 49.0 ± 22.3. Using a CBI subscale cut-off score of ≥50 (moderate and higher), 72.6% (n=373, 95% CI=68.5%-76.4%) of respondents reported personal burnout; 70.6% (n=363, 95% CI=66.4%-74.5%) of respondents reported work-related burnout; and 55.4% (n=285, 95% CI=51.0%-59.7%) of respondents reported client-related burnout (Table 3).

The mean physical component summary score of the 12-Item Short Form Survey was 49.6 ± 7.8; the mean mental component summary score of the 12-Item Short Form Survey was 42.3 ± 10.6 (Table 3).

As measured by the PHQ-9, the mean depression score was 6.2 ± 5.1. However, the prevalence of depression among respondents, defined as a score of ≥10, was 21% (n=110) [Table 3].

In total, 79% (n=404) of respondents did not report any suicidal ideation or attempt. The remaining respondents stated that life was “not worth living” or “wished he or she was dead”; some also reported a history of suicidal ideation or attempts. The most commonly cited source of stress in the past year was clinical responsibilities/job demands.

In terms of health conditions, there was a perception among respondents that their health status was “worse” (29%; n=148) or “much worse” (3%; n=17) than among other individuals of the same age. The mean duration of sleep each night was 6.2 ± 1.5 hours. However, most respondents frequently experienced inadequate sleep when at work; 70% (n=361) of respondents indicated that this occurred weekly or more often. In terms of personal habits, the prevalences of alcohol drinking, drug addiction, and smoking were low. However, the prevalences of regular physical activity and personal physical assessments were not high (Table 4).

Logistic regression modelling was performed to investigate bivariate associations of demographic and professional factors with burnout, the presence of depression, or suicide ideation and/or attempts.

The number of working hour(s) per week (odds ratio [OR]=1.02; 95% CI=1.01-1.04; P=0.001) was positively associated with depression (online supplementary Table 1); having children (OR=0.58; 95% CI=0.36-0.93; P=0.024) was negatively associated with suicidal ideation/attempts. Doctors who completed a project-based learning curriculum during undergraduate study were less likely to be depressed or report suicidal ideation/attempts (depression: OR=0.60; 95% CI=0.39-0.91; P=0.017; suicidal ideation/attempts: OR=0.65; 95% CI=0.43-1.00; P=0.049) [online supplementary Table 2].

Older age (OR=0.97; 95% CI=0.94-0.99; P=0.026), possession of a first university degree in medicine or dental surgery (OR=0.37; 95% CI=0.15-0.89; P=0.027), and possession of Academy fellowship status (OR=0.61; 95% CI=0.41-0.92; P=0.017) were associated with lower likelihood of personal burnout. Engagement in longer working hour(s) per week (OR=1.04; 95% CI=1.02-1.05; P<0.001) and working in Hospital Authority clinics (OR=1.95; 95% CI=1.05-3.62; P=0.034; compared with working in government clinics) were positively associated with personal burnout (online supplementary Table 3). Marital statuses of single, separated, or divorced (OR=1.71; 95% CI=1.16-2.53; P=0.007) and engagement in longer working hour(s) per week (OR=1.03; 95% CI=1.02-1.05; P<0.001) were positively associated with work-related burnout (online supplementary Table 4). Conversely, having children (OR=0.66; 95% CI=0.44-0.98; P=0.038), consultant seniority level (OR=0.27; 95% CI=0.09-0.88; P=0.029; compared with associate consultant seniority level), and working in the private sector (OR=0.40; 95% CI=0.17-0.94; P=0.035; compared with working in government) were negatively associated with work-related burnout. Provision of primary care (OR=1.5; 95% CI=1.04-2.16; P=0.031) was associated with client-related burnout (online supplementary Table 5).

This study attempted to quantify well-being and burnout in young doctors (both resident-in-training, and doctors within 10 years of their specialist registration) throughout Hong Kong; there were three main findings. First, the mean burnout score was high in this group of doctors; mean personal and work-related scores of ≥50 were observed on the CBI. Second, there was a high prevalence of job dissatisfaction (28%) in this group of doctors. Third, the self-perceived personal well-being and mental health were worse in this group of doctors than in members of the general population with similar ages.

Burnout is a well-known occupational hazard in people-oriented professions; doctors are at particular risk of burnout because of their frequent engagement in intense personal and emotional contact with patients. Although these therapeutic and service relationships are highly rewarding and engaging, they can also be a source of stress. Burnout among doctors has been recognised as a global crisis20; its effects on personal, patient, and institutional levels can be substantial. The expectation to meet job demands can lead to maladaptive practices which will ultimately compromise relationships with patients and colleagues, with long-term consequences on patient care.21 Hence, efforts to acknowledge that such a problem exists represents the first step in establishing a systematic strategy to address this crisis.

Although there have been multiple published reports regarding burnout among doctors, territory-wide data focusing on junior doctors in Hong Kong are lacking. Siu et al9 conducted a random sample survey of 226 public doctors in 2012; they found that 31.4% of respondents satisfied the criteria for high burnout. Moreover, young but moderately experienced doctors needing to work shifts were most vulnerable to high burnout. However, the questionnaire used in that study was not comprehensive, the random sampling method did not produce a representative cohort, and only public doctors were invited to the survey. More recently, a more comprehensive survey involving medical graduates of one university in Hong Kong found high prevalences of personal (63.1%) and 55.9% (work-related) burnout using the standardised CBI.10 The more comprehensive survey represents the most comprehensive and robust study in Hong Kong thus far, but it only included graduates from one university in Hong Kong; it did not include any doctors trained elsewhere.

The present study of young doctors throughout Hong Kong found high mean personal (59.6 ± 20.5) and work-related (57.3 ± 20.1) scores on the CBI. The mean client-related score was 49.0 ± 22.3, slightly below the score of 50 that constituted the threshold for burnout. These scores were higher than in the previous study performed in Hong Kong by Ng et al,10 which showed mean CBI scores of 57.4 ± 21.4 (personal), 48.9 ± 7.4 (work-related), and 41.5 ± 21.8 (client-related). Moreover, when compared with studies worldwide that used the CBI to measure burnout in doctors,15 16 18 22 the levels of burnout in the present study were among the highest. Contributing factors may differ among regional healthcare systems; causes of burnout and well-being in junior doctors may not be consistent worldwide. Our study attempted to identify sources of stress among junior doctors in Hong Kong; the most commonly cited sources were clinical responsibilities/job demands and professional examinations. Additional in-depth studies are necessary to determine how these factors can be modified to alleviate stress in junior doctors.

The respondents’ general health statuses (in terms of medical conditions) were not substantially worse than the general population, although 32% of the respondents indicated self-perceived health worse than their peers. The present study also showed that the prevalence of depression was 21%, according to the PHQ-9. This is more than double the prevalence previously reported in Hong Kong (8.4%).23 Despite the high prevalence of depression in the present study, respondents indicated low rates of suicidal ideation/attempts. Although a causal relationship could not be established because of the observational nature of the study, the number of working hours per week and having children were factors that affected risk of depression and suicidal ideation/attempts, respectively. The mean number of hours worked per week was 53.5 ± 14.8 hours. Junior doctors who work >55 hours per week are reportedly twofold more likely to have frequent health problems (OR=2.05, 95% CI=1.62-2.59; P<0.001) and suicidal ideation (OR=2.0, 95% CI=1.42-2.82; P<0.001).24 A previous systemic review showed an association between long working hours and a depressive state in other professions in general.25 Positive effects of reduced working hours among junior doctors have been found in some studies,26 27 but this relationship is not consistently observed. For example, in the United Kingdom, the Working Time Regulations were fully applied to junior doctors beginning in 2009; these comprised a limit of 48 hours per week, averaged across a reference period of 26 weeks, with additional minimum rest periods. However, implementation of the Working Time Regulations has not fully resolved the effects of long hours and fatigue.28 Furthermore, there are implications for professional training and manpower planning if rigid enforcement of such working hours is performed.

Our study did not find any substantial evidence that young doctors were reliant on alcohol, smoking, or drugs as coping mechanisms. This contrasts with findings from the US, which indicated that high levels of alcohol and substance abuse were associated with burnout among doctors.29 It was beyond the scope of the present study to explore other avenues that junior doctors in Hong Kong might use to alleviate their stress levels and burnout. Other health and lifestyle behaviours (eg, exercise levels and personal physical assessments) may be indicative of time constraints related to work or personal obligations; they may also be indicative of self-neglect caused by such constraints and work-related burnout.

This study had several limitations. First, it was a cross-sectional study with voluntary participation, and the results might not be representative of all doctors throughout public and private sectors in Hong Kong. However, to our knowledge, this study performed the most comprehensive survey regarding burnout among doctors in Hong Kong thus far. Second, the study was not designed to avoid selection bias concerning doctors who were more prone to burnout and therefore more interested to participate in such surveys. Third, because the survey did not allow free text entry in the questionnaire responses, more in-depth analysis was not possible in some instances. Fourth, because this was a cross-sectional survey, no causal relationships or risk factors could be established regarding the development of burnout or depression. Fifth, our definition of “young” was based on the 10 years of specialist registration, which included doctors with various levels of experience and responsibilities; thus, the results might not be representative of a specific subset of doctors.

The present study showed that junior doctors in Hong Kong had a high level of burnout, and there was a high prevalence of depression among the respondents. A substantial proportion of the respondents were dissatisfied with their present job position. Future studies to determine causal factors will allow the development and implementation of specific strategies to address these problems within Hong Kong. The maintenance of well-being in junior doctors is vital for sustaining a healthy medical workforce and long-term patient care.

Concept or design: All authors.
Acquisition of data: KYH Kwan, LWY Chan, PW Cheng.
Analysis or interpretation of data: KYH Kwan, LWY Chan, PW Cheng.
Drafting of the manuscript: KYH Kwan.
Critical revision of the manuscript for important intellectual content: All authors.

The authors have no conflicts of interest to disclose.

The authors thank all members of the Young Fellows Chapter of the Hong Kong Academy of Medicine for their active participation in this study; the secretariat and staff of the Hong Kong Academy of Medicine and its Hong Kong Jockey Club Innovative Learning Centre for Medicine for their administrative and information technology support; and the Council of the Hong Kong Academy of Medicine for their active support, encouragement, and funding of the coupons. The authors especially thank Dicken CC Chan for statistical assistance.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

This study was approved by the Institutional Review Board of The University of Hong Kong/Hospital Authority Hong Kong West Cluster (Ref No: UW 19-062).

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29. Oreskovich MR, Shanafelt T, Dyrbye LN, et al. The prevalence of substance use disorders in American physicians. Am J Addict 2015;24:30-8. Crossref

Considerable physical and psychosocial benefits are associated with participation in sporting activities.1 2 Physical activity has been demonstrated to reduce the risks of coronary heart disease, some cancers, obesity, hypertension, and type 2 diabetes mellitus.2 3 4 5 6 Its obvious merits have prompted several national health programmes, including the health programme in Hong Kong, to promote sports to the general public.7 8 9 However, sports participation carries a risk of injury, especially traumatic brain injury (TBI). It has been estimated that 20% of all TBIs are sports-related.10 In addition, up to 20% of sports-related TBI survivors (usually adolescents or young adults) experience chronic symptoms including headache, fatigue, and cognitive and balance difficulties.11 There is a global trend of increasing sports-related TBI incidence: from 3.5 to 31.5 per 100 000 population in the past decade.12 13 Because many patients with mild TBI do not seek medical attention, these figures likely underestimate the total burden of this condition.13 Population-based studies reviewing sports-related TBI are sparse; most target specific groups of individuals (eg, professional athletes) or rely on self-reporting surveys that lack a uniform definition and comprehensive assessment of brain injury.14 For similar reasons, studies reviewing outcome predictors have also been inadequate, thus hindering the generation of meaningful conclusions to guide governmental policy initiatives.14

Hong Kong is highly urbanised with an established public transport system, such that cycling is mainly regarded as a recreational activity.15 16 In terms of fatality rate, Hong Kong is among the most dangerous areas for cycling, compared with other cities such as New York, the US, or countries such as France.17

This study was performed to document the epidemiology of sports-related TBI among patients who required inpatient care by adopting territory-wide uniform diagnostic coding criteria, clear data definitions, and systematic assessments of radiologic findings. Because cycling is a popular sport in Hong Kong, factors predictive of intracranial haemorrhage (eg, the effect of helmet use) and poor functional outcomes among cyclists hospitalised with TBI were determined.

Patients who required inpatient care at any Hospital Authority institution for sports-related TBI from 1 January 2015 to 31 December 2019 were reviewed. The Hospital Authority is a public health service highly subsidised by the Hong Kong SAR Government; it is responsible for 90% of inpatient bed days in the city. Patients were identified by the International Classification of Diseases, Tenth Revision, Clinical Modification code (ICD-10-CM) designation for TBI 854.0 secondary to a sports-related external cause (E codes: E006-10). Data from clinical records, operation notes, medication prescriptions, and computed tomography (CT) brain scans from a central digital imaging repository were reviewed. In particular, the type of sport played, the clinical presentation of symptoms, the Injury Severity Score (ISS), the need for neurosurgery, length of hospitalisation, and diagnosis of post-concussion syndrome were recorded. Head injury was classified into mild (presenting Glasgow Coma Scale [GCS] score, 14-15); moderate (presenting GCS score, 9-13), and severe (presenting GCS score, 3-8), in accordance with criteria established by the Neurotraumatology Committee of the World Federation of Neurosurgical Societies.18 Post-concussion syndrome was defined in accordance with ICD-10 criteria. This required a 4-week duration of symptoms from at least three categories following a traumatic loss of consciousness. The symptom categories were headache, irritability, concentration impairment, insomnia, and a preoccupation with the aforementioned symptoms. For neurosurgical patients with cycling related–TBI, the mechanism of injury and their experience level (ie, professional athlete or amateur rider) were documented. All CT scans were reviewed by an independent assessor with 6 months of neurosurgical training experience who was blinded to the patients’ clinical characteristics and outcomes. The scans were first evaluated using the Rotterdam CT score, a commonly utilised validated radiological assessment system for the prognosis of patients with TBI. The classification has four distinct elements that require the appraisal of the degree of basal cistern obliteration, degree of midline shift, the presence (or absence) of an epidural mass lesion, and the presence (or absence) of intraventricular or traumatic subarachnoid haemorrhage (Table 1). In addition, the scans were assessed for skull fractures, cerebral contusions, and acute subdural haematomas (ASDHs). The primary outcome of the study was the presence of intracranial haemorrhage on the admitting CT scan. All potential predictors were categorised into patient-related, trauma-related, and radiological factors. The secondary outcome was unfavourable functional performance, defined as a Glasgow Outcome Scale (GOS) score of 3 to 5 on discharge from the hospital (3, severe disability; 4, persistent vegetative state; and 5, death).

Statistical analyses utilised the Chi squared test and Fisher’s exact test were used for categorical data such as patient gender or the use of antiplatelet medication. Independent-samples t test was used for continuous data such as patient age or duration of hospitalisation. Multivariate binary logistic regression was used to identify independent factors for the presence (or absence) of traumatic intracranial haemorrhage. A P value of <0.05 was considered statistically significant. Statistical analysis was conducted using SPSS (Windows version 20.0; IBM Corp, Armonk [NY], US).

In total, 720 consecutive patients were hospitalised with sports-related TBI during the 5-year study period, and 705 (97.9%) of them were admitted under neurosurgical care. This was equivalent to a crude incidence of 1.9 per 100 000 general population. The mean (± standard deviation [SD]) age was 32 ± 19 years; 521 (72.4%) patients were adults (≥18 years) and 568 (78.9%) were male. The most common sport was cycling (59.2%), followed by football (21.3%) and basketball (7.5%) [Fig a]. On admission, most (86.1%) patients were fully conscious. Overall, 658 (91.4%) patients had mild TBI, 41 (5.7%) patients had moderate TBI, and 21 (2.9%) patients had severe TBI. Post-traumatic seizures occurred in 36 (5.0%) patients. Furthermore, 324 (45.0%) patients had a loss of consciousness and 269 (37.4%) patients experienced post-traumatic retrograde amnesia. Only 19 (2.6%) patients were taking either antiplatelet or anticoagulant medication. Extracranial injuries were sustained by 208 (28.9%) patients; among them, injuries were mainly either limb abrasions or contusions (62.1%). The median ISS was 2 (interquartile range=2-8).

Intracranial haemorrhage was noted in 283 (39.3%) patients with TBI; 166 (23.1%) patients exhibited traumatic subarachnoid haemorrhage and 157 (21.8%) exhibited ASDH. Skull fractures were detected in 179 (24.9%) patients, with a median Rotterdam CT score of 2 (interquartile range=2-2). In total, 59 (8.2%) patients required neurosurgical intervention; 32 (54.2%) of them had good recovery with a median GOS score of 5 on discharge from the hospital and at 6 months. The mean (± SD) duration of hospitalisation was 5 ± 28 days. Among 307 (42.6%) patients in whom 6-month GOS scores could be assessed, good recovery was observed in 260 (84.7%). Post-concussion syndrome was diagnosed in 30 (6.2%) of 482 patients who attended scheduled follow-up outpatient consultations.

The crude incidence of recreational cycling-related TBI requiring hospitalisation was 1.1 per 100 000 population. A comparison was performed between cyclists with sports-related TBI and patients who had TBI because of other sports (Table 2). Cyclists were significantly older (P<0.001) [Table 2; Fig b]. Among 426 cyclists, 306 (71.8%) were male and 120 (28.2%) were female. However, the proportion of patients who were female was significantly higher among those who had TBI because of cycling (28.2%) than among those who had TBI because of other sports (10.9%; P<0.001). Cyclists were likely to exhibit more severe TBI with an almost three-fold greater risk of sustaining extracranial injury (odds ratio [OR] 2.8; 95% CI: 1.9-4.0), resulting in a higher ISS (P<0.001). Of cyclists admitted for head injury, 201 (47.2%) had intracranial haemorrhage, which was radiologically more extensive in terms of the Rotterdam CT score, compared with haemorrhage in non-cyclists (P<0.01). As a consequence, a greater proportion of cyclists had a worse GOS score on discharge from hospital (OR 2.8; 95% CI: 1.3-6.2) and at 6 months (OR 4.7; 95% CI: 2.1-10.5). The cause of death for all cyclists with 30-day mortality was severe TBI with medically refractory intracranial hypertension. Although the overall incidence was low, cyclists also had a greater risk of post-concussion syndrome (OR 2.5; 95% CI: 1.2-5.4).

Among the 426 cyclists in this study, 128 (30.0%) experienced bicycle accidents during the weekend; 10 (2.3%) of the cyclists were professional athletes. Most cyclists (273; 64.1%) accidently fell off their bicycle on their own (ie, without colliding into another object) on level ground. Of the injuries, 103 (24.2%) were sustained when the cyclist was traveling downhill; for the 28 patients with records of self-reported velocities, the estimated mean (± SD) velocity at the moment before injury was 40 ± 15 km/h. At the time of injury, 361 (84.7%) cyclists had not been wearing a helmet. Among eight (1.9%) patients who subsequently died, none had been wearing protective head gear.

Risk factors for traumatic intracranial haemorrhage among cyclists are shown in Table 3. Univariate analysis identified the following risk factors: age ≥60 years, use of antiplatelet medication, involvement in a motor vehicle collision, presence of moderate to severe TBI, and skull fracture. In univariate analysis, helmet wearing was protective against intracranial haemorrhage. Multivariate logistic regression identified the following independent risk factors: age ≥60 years, antiplatelet medication intake, moderate or severe TBI, and the presence of a skull fracture. Table 4 shows independent significant predictors for unfavourable GOS score on discharge from hospital: age ≥60 years, antiplatelet intake, severe TBI, intracranial haemorrhage, and the need for neurosurgical operative intervention.

As shown in Table 2, 375 (88.0%) hospitalised cyclists had mild TBI, whereas only 36 (8.5%) cyclists had moderate TBI and 15 (3.5%) had severe TBI. No protective effect of helmet use was noted in terms of reducing TBI severity across these GCS-defined categories (Table 3). However, among cyclists with mild TBI, helmets were significantly protective against intracranial haemorrhage and skull fracture, regardless of age, antiplatelet medication intake, or mechanism of injury (Table 5). Although the median Rotterdam CT score was comparable between cyclists with mild TBI who did or did not wear helmets (P=0.68), significantly fewer patients with head protection had epidural haematoma or ASDH. For patients with mild TBI who had intracranial haemorrhage, this difference in radiological factors led to a significantly shorter mean (± SD) duration of hospitalisation for patients who wore helmets (2.6 ± 2.9 days), compared with patients who did not (7.1 ± 11.6 days, P<0.001). However, there was no difference in the need for neurosurgical intervention among patients with mild TBI who had intracranial haemorrhage according to head protection status (P=0.17). Similarly, unfavourable GOS scores on discharge from hospital (P=0.43) and at 6 months (P=0.71) were comparable among patients with mild TBI who had intracranial haemorrhage, regardless of head protection status (Table 5).

The incidence of sports-related TBI in Hong Kong is 2 per 100 000 general population; this is lower than in other countries (eg, the US, Australia, or Italy), where the incidences range from 4 to 32 per 100 000 population.12 The lower incidence in Hong Kong is consistent with a previous finding that Hong Kong residents (especially children and adolescents) have lower physical activity and fitness levels than in other regions, according to a global evidence-based evaluation of such indicators from 49 countries.19 Considering the health benefits of an active lifestyle, there is a clear need to promote sports engagement in Hong Kong. A survey of 5701 residents performed by the Transport Department of the Hong Kong SAR Government estimated that 10% of households had bicycles available for use; moreover, 69% (4 million) of residents aged 15 years or older knew how to ride one.16 In addition, most survey respondents (73%) cycled for recreational or fitness purposes.15

Previous epidemiological studies of sports-related brain injuries revealed that cycling was one of the most frequent activities involved.10 12 20 21 In 2019, 1738 road traffic accidents involving cyclists were reported to the Hong Kong Transport Department.22 Half of these accidents (50.6%, 879/1738) occurred in recreational areas such as cycling tracks, parks, or playgrounds; eight (0.5%) patients experienced fatal injuries.22 In the past 10 years, the number of cyclist injuries in Hong Kong has increased by 5.2% per year.17 Compared with other regions worldwide, Hong Kong is one of the most dangerous areas for cycling.17 The fatality rate (per billion minutes cycled) in the city was 34, substantially higher than the rates in Stockholm, Sweden (3), France (4), and other metropolitan areas (eg, New York City [18] and Los Angeles [8]).17 These studies included riders primarily involved in commuting and the causes of death were not elucidated, but they indicate a growing need to enhance the safety of vulnerable road users.

To our knowledge, this is the first multicentre study to comprehensively document the outcomes of inpatients with recreational cycling-related TBI using standard assessment criteria. By comparison with patients who had TBI because of other sports, we found that cyclists in Hong Kong exhibited greater risks of more severe injury, intracranial haemorrhage, unfavourable GOS score at discharge from hospital, and post-concussion syndrome. Despite these findings, our results suggest that cycling is generally safe and hospitalised patients had a high (92.7%) likelihood of favourable functional outcomes on discharge from hospital.

Single-centre reviews of cycling-related injuries among various suburban districts in Hong Kong found that limb injuries were the most common form of trauma followed by head injury (10%-39% of patients).23 24 25 26 Among patients with TBI, 16% to 53% exhibited “severe” injury; however, the studies did not provide explicit definitions to qualify this categorisation, and did not describe radiological data regarding the extent of injury or the need for neurosurgical intervention.23 26 In the present study, 12% of hospitalised cyclists with head injury had moderate to severe TBI. There was also a high incidence of intracranial haemorrhage involving almost half of the patients. Both these factors were independent predictors of poor GOS score on discharge from hospital. Our results are consistent with the findings in a previous study where 75% of all cycling-related deaths were caused by severe TBI.27 The lack of an independent association with motor vehicle collisions, which constituted only a minority of injuries in this cohort, suggests that recreational cycling at comparatively low speeds can be fatal. Notably, the mechanism of injury for four (50%) of the eight recreational cyclists who died in this study was a loss of balance, followed by a fall on level ground without colliding into another object, person, or motor vehicle.

Previous studies in Hong Kong, the most recent of which was performed >10 years ago, revealed that recreational cyclists rarely wore protective headgear (eg, frequencies of 0.2% to 2.2% among emergency department attendees).24 25 26 Our findings revealed that significantly more patients (15%) wore helmets at the time of injury. Governmental advocacy initiatives for promoting helmet wearing in recent years may have resulted in heightened public awareness regarding the risks of head trauma.28 There is little doubt that helmets are protective. In the past 30 years, several case-control and epidemiological studies have delivered compelling evidence to support the efficacy of bicycle helmet wearing in reducing the risk of life-threatening TBI.29 30 31 32 33 34 35 36 37 In a case-control prospective multicentre study of over 3000 patients, Thompson et al33 noted that helmets (irrespective of design) conferred up to a 74% reduction in TBI during accidents. A subsequent meta-analysis of five studies observed that helmets provided a 63% to 88% reduction in the risk of head, brain, and severe TBI for all ages of cyclists; this included equal levels of protection for collisions involving motor vehicles and collisions due to other causes.38 In the present study, helmet wearing did not reduce TBI severity according to our broadly predefined categories. However, among hospitalised recreational cyclists with mild head injury, helmets did provide significant protection against intracranial haemorrhage, including potentially life-threatening epidural haematomas and ASDHs, as well as skull fractures. Thus, our findings may have important public health implications with regard to introducing mandatory bicycle helmet wearing legislation in the city.

Whether such laws should exist is a particularly divisive issue among public health experts and interest groups.39 40 41 42 43 In Australia, a nation with all-age helmet wearing safety laws, an overall 46% decline in cyclist fatalities per 1 000 000 population has been reported, compared with the pre-legislation period.44 Similar findings were noted in New Zealand: a 67% decline in severe TBI was recorded after the introduction of helmet laws.45 In the US, a significant reduction in paediatric cyclist fatalities involving motor vehicles was observed in states with such laws.46 A meta-analysis of the effectiveness of bicycle helmet legislation revealed that it increased helmet usage, while significantly reducing head injuries and mortality.47 Several medical associations have expressed support for introducing such legislation; these include the World Health Organization, the British Medical Association, the American Medical Association, and the Royal Australasian College of Surgeons.48 49 50 51 However, critics of such compulsory policies have hypothesised that helmets could encourage risk-compensation behaviour, whereby cyclists may be more willing to engage in potentially injurious risks or for motorists to exercise less caution when encountering them.39 52 53 Other reasons for opposition include infringement on individual liberties; some public health scholars have theorised that such laws could discourage cyclists from participating in gainful physical activity.39 40 41 42 54 From a Hong Kong Transport Department survey (5701 respondents) regarding attitudes towards possible helmet law and enforcement measures, the majority of respondents (78%-90%) were in favour of introducing such legislation, especially when riding on carriageways.16 However, among respondents who knew how to ride a bicycle (3933 respondents), 23% declared they would ride less frequently if mandatory helmet wearing was required.16

An inherent limitation of a retrospective study of this nature was the likely under-reporting of the number of patients with sports-related head injuries. In the only existing population-based study of TBI epidemiology that included community-based injuries, 95% were considered mild and 28% of respondents did not seek medical attention.55 Among professional or university-level athletes, under-reporting is more apparent: questionnaire surveys reveal that 31% to 78% of respondents neglected to pursue medical care despite experiencing a concussion during the preceding 12 months.56 57 At the emergency department level, no territory-wide TBI registry exists in Hong Kong; moreover, diagnostic coding to facilitate data retrieval is typically not performed after consultations. Therefore, we could only identify hospitalised patients with sports-related TBI by means of an administrative database that utilised the ICD-10 coding system. However, the validity of such administrative data for research has been questioned.58 Studies have shown significantly lower TBI rates among young adults, men, and patients with less severe injuries when the ICD system was utilised, compared with thorough medical record review.59 Analysis of a population-based TBI sample showed that only 19% of individuals were assigned a TBI-related diagnostic ICD code.60 In addition, a degree of selection bias may have existed because some non-hospitalised helmet-wearing cyclists with mild head injury may have been discharged from the emergency department, mitigating the protective effects of helmet use. This may explain why no considerable differences in outcomes were detected for patients with moderate or severely injured patients. Despite the low rate of helmet use among recreational cyclists (15%), significant protective effects were detected among mildly injured patients with regard to intracranial haemorrhage and skull fracture. This limited participant identification approach also allowed for a pragmatic review of patients with clinically significant TBI who were hospitalised following evaluation by an emergency care physician. Computed tomography scans are generally performed only for hospitalised patients with head injury in our public healthcare system; this approach offered an opportunity to evaluate imaging data for intracranial haemorrhage. Because the ICD coding system for traumatic intracranial haemorrhage reportedly has high sensitivity and specificity (both >80%),59 we adopted this coding outcome as the study’s primary endpoint. Another important limitation was the definition of mild TBI, which affected most patients in this study. The definitions offered by several authorities range from conventional GCS-based criteria such as the US Centers for Disease Control and Prevention,61 and the American College of Surgeons62 to additional symptoms of confusion, memory impairment, transient loss of consciousness, and irritability proposed by the World Health Organisation and the American Congress of Rehabilitation Medicine.18 63 64 A better delineation of these symptoms would have enhanced the identification of patients with “high-risk” mild TBI; however, because these relevant symptoms were often not systematically documented in most medical records retrieved in our study, we used GCS-based criteria to reduce the overall rate of underdiagnosis. Using GOS score on discharge from hospital as a secondary study endpoint, we found that only 31 (7%) patients had unfavourable outcomes. Although statistically significant predictors for TBI were identified, the wide confidence intervals for these predictors suggest that the sample size was insufficient to draw robust conclusions. Finally, we could only retrospectively assess GOS score as a fundamental measure of functional outcome. More sensitive instruments (eg, the extended GOS or the Sport Concussion Assessment Tool65 66) might have been better for assessing the psychosocial and cognitive aspects of TBI, considering that a large proportion of mildly injured cyclists had intracranial haemorrhage.

The incidence of sports-related TBI in Hong Kong is low and cycling is the most frequently associated activity. Almost half of hospitalised recreational cyclists sustained intracranial haemorrhage. Compared with patients who had head injury because of other sports, cyclists are more likely to experience severe consequences. There is evidence that helmet use offers protection against intracranial haemorrhage and skull fracture among cyclists with mild head injury. Cycling is a safe physical activity, but further legislative measures should be introduced to promote and protect the welfare of individuals enjoying this sport.

Concept or design: PYM Woo, E Cheung.
Acquisition of data: PYM Woo, E Cheung, FWY Lau, NWS Law, CKY Mak, P Tan, B Siu, A Wong.
Analysis or interpretation of data: PYM Woo, E Cheung, CKY Mak.
Drafting of the manuscript: All authors.
Critical revision of the manuscript for important intellectual content: All authors.

All authors had full access to the data, contributed to the study, approved the final version for publication, and take responsibility for its accuracy and integrity.

All authors have disclosed no conflicts of interest.

This research has not been presented or published in any form prior to submission.

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

This study was approved by the Kowloon Central Cluster/Kowloon East Cluster research ethics committee (Ref KCC/KEC-2020-0331). All patients were treated in accordance with the Declaration of Helsinki. Informed consent was obtained from either the patient, next-of-kin, or their legal guardian.

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